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J. Anim. Sci. 2002. 80:3053-3059
© 2002 American Society of Animal Science

Seasonal effects on estrous behavior and time of ovulation in nonlactating beef cows1,2

F. J. White*, R. P. Wettemann*,3, M. L. Looper*,4, T. M. Prado{dagger} and G. L. Morgan{dagger}

* Departments of Animal Science, Oklahoma Agricultural Experiment Station and and {dagger} Medicine and Surgery, College of Veterinary Medicine, Oklahoma State University, Stillwater 74078-0425

3 Correspondence:
Phone: 405-744-6077; fax: 405-744-7390; E-mail:
rpw{at}okstate.edu.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Estrous behavior and time of ovulation relative to the onset of estrus were determined in mature Angus x Hereford cows (n = 17 to 21 each season) during summer, winter, and spring for 2 yr. Estrous behavior was evaluated during the first of two consecutive estrous periods, and time of ovulation was determined during the second estrus. Concentrations of progesterone were quantified in twice weekly blood samples to ensure all cows had normal estrous cycles. The HeatWatch system was used to measure the duration of estrus, number of mounts received per estrus, and duration of the longest interval between mounts received. Commencing 16 h after the onset of the second estrus, transrectal ultrasonography was performed every 4 h until the dominant follicle was no longer present on the ovary, and time of ovulation was defined as 2 h preceding the absence of the dominant follicle. There was a seasonal effect on the duration of estrus; cows were estrus longer in summer (17.6 ± 0.8 h) than in winter (15.5 ± 0.8 h; P = 0.07) or spring (13.9 ± 0.9 h; P < 0.05). Cows were mounted more times per estrus (P < 0.05) in winter (59.0 ± 5.3) than in summer (43.6 ± 5.3) or spring (38.2 ± 5.8). Intervals between mounts of estrous cows were longer (P < 0.05) in summer (4.1 ± 0.4 h) than in spring or winter (2.7 ± 0.4 h). During all seasons, cows were mounted more times (P < 0.01) between 0600 to 1200 (3.2 ± 0.2 mounts received/h of estrus) than during other times of the day (2.1 ± 0.2 mounts received/h of estrus). Cows ovulated 31.1 ± 0.6 h after the onset of estrus, and time of ovulation was not influenced by season. We conclude that season influences estrous behavior of beef cows; cows are mounted more times per estrus in winter than in summer or spring. Time of ovulation relative to the onset of estrus is constant during all seasons and averages 31.1 h.

Key Words: Beef Cows • Behavior • Estrus • Ovulation


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Use of AI in beef cattle is limited because of the difficulty in detecting the onset of estrus. Initiation of estrus is the best external sign to estimate time of ovulation and when to inseminate cows. When dairy cows were monitored continuously with the HeatWatch system (DDx Inc., Denver, CO) the duration of estrus averaged 7 to 10 h, and cows were mounted an average of 8 to 14 times (Walker et al., 1996; Dransfield et al., 1998; Xu et al., 1998). In contrast, beef heifers were in estrus for 14 h and were mounted 50 times (Stevenson et al., 1996).

Dairy cows ovulated 10 to 15 h after the end of estrus (Nalbandov and Casida, 1942; Trimberger, 1948) or 27.6 ± 0.6 h after the onset of estrus (Walker et al., 1996). Greatest pregnancy rate occurred when dairy cows were inseminated between 4 and 12 h after the onset of estrus (Dransfield et al., 1998). Seasonal and thermal stress are detrimental to reproductive efficiency of dairy cows (Gwazdauskas et al., 1975; Cavestany et al., 1985) and alter endocrine function and follicular dynamics (Wolfenson et al., 1995, 1997; Wilson et al., 1998). However, the effects of season on estrous behavior and time of ovulation have not been determined for beef cows.

Characterization of seasonal effects on estrous behavior and time of ovulation relative to the onset of estrus will allow development of recommendations for time of AI to enhance pregnancy rates. The objectives of this study were to determine the time of ovulation relative to the onset of estrus in beef cows and to determine if season influences estrous behavior and time of ovulation.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Animals
Estrous behavior and time of ovulation relative to the onset of estrus were determined during summer (August and September), winter (December and January), and spring (April and May) of two consecutive years in Oklahoma. These 2-mo periods were selected because the maximum, minimum, and intermediate ambient temperatures typically occur during these periods. Daily high, low, and mean ambient temperatures were determined from temperatures recorded every 5 min for 24 h by the Oklahoma Mesonet (http://www.mesonet.ou.edu) at Marena, OK (6 km from research location). Nonpregnant, nonlactating Hereford x Angus cows (2.5 to 8 yr of age with normal estrous cycles; n = 17 to 21 each season) were managed each season in a 12 ha pasture with shade. Cows received water from metal tanks and did not have access to ponds for cooling. Cows weighed 522 ± 22 kg, had a body condition score of 5.5 ± 0.1 (1 = emaciated, 9 = obese; Wagner et al., 1988), and had access to native grass pasture and hay. A 20% CP supplement (1.2 kg/d) was fed when protein content of forage was inadequate.

Estrus Detection
The HeatWatch system (DDx Inc.) is composed of a pressure sensor and battery-operated radio transmitter that attaches in a patch to the rump of a cow to continuously monitor when a cow is mounted. Hair on the rump anterior to the tail head of a cow was trimmed, and the patch was attached with industrial strength glue (OSI Quickbond; Ohio Sealants Inc., Mentor, OH). Cows were monitored during two consecutive estrous periods. The first estrus was induced with PGF2{alpha} (Lutalyse, 25 mg; Pharmacia Animal Health, Kalamazoo, MI), and treatment was planned to ensure that usually only one or two cows, and never more than four cows, were in estrus at any time. The second estrus occurred spontaneously 18 to 22 d after the first. The first estrus was used to quantify estrous behavior, and time of ovulation was determined relative to the onset of the second estrus. Two estrous periods were studied to avoid possible alterations in estrous behavior when cows were removed from the herd for ultrasonography to determine time of ovulation. During summer and winter of yr 1, cows were observed twice daily (at 0700 and 1900 in summer and 0730 and 1730 in winter) for 30 min to detect estrus.

Duration of estrus, number of mounts received, the longest interval between subsequent mounts received, and the number of mounts received per hour of estrus were determined. Onset of estrus was defined as the first of two mounts received within 4 h. The end of estrus was the last mount received, with a mount 4 h before, and no mounts during the next 12 h. Number of mounts received was the number of times a cow was mounted by herdmates. The daily distribution of mounting activity was determined by dividing the day into four 6-h periods, and data were analyzed as mounts received per hour of estrus.

Ovulation
Time of ovulation relative to the onset of estrus was determined at the second estrus each season. Commencing 16 h after the onset of estrus (determined with HeatWatch) transrectal ultrasonography (Aloka 500-V ultrasound and a 7.5-MHz transducer; Corometrics Medical Systems, Wallingford, CT) was performed every 4 h until the dominant follicle was not present on the ovary. Time of ovulation was defined as 2 h preceding the time that the dominant follicle was absent. Ultrasound images of the ovary were recorded at each evaluation, and the diameter of the follicle was the average of the length and the width (Pierson and Ginther, 1988). Most cows were maintained in the herd throughout the experiment unless culled for health reasons.

Steroid Hormones
Blood samples were collected every 3 or 4 d by tail venipuncture. Additional samples were collected daily commencing 5 d before the second expected estrus and every 4 h between 12 and 56 h after the initiation of estrus from 12 cows during summer or winter of yr 2 to quantify progesterone and estradiol. Samples were cooled in ice and centrifuged within 1 h at 2,500 x g for 15 min, and plasma was stored at -20°C until hormones were quantified. Concentrations of progesterone and estradiol were determined by RIA (Vizcarra et al., 1997). A normal luteal phase of an estrous cycle was defined as concentrations of progesterone greater than 0.5 ng/mL in consecutive samples for 11 to 15 d (Wettemann et al., 1972).

Experimental Design and Statistical Analyses
The experimental design was a completely randomized block design. Duration of estrus, mounts received, longest interval between mounts received, mounts received per hour of estrus, time from onset of estrus to ovulation, and time from end of estrus to ovulation were analyzed for season effects, with year as a block, using the PROC GLM procedure of SAS (SAS Inst., Inc., Cary, NC). The simple correlation between duration of estrus and number of mounts received per estrus was analyzed with the PROC CORR procedure of SAS. Seasonal effects on the size of the dominant follicle were analyzed by ANOVA as a repeated measures experiment using the PROC MIXED procedure of SAS. The model included observed mean, block (year), season, the random experimental error of cows within season, time when the follicle was measured, interaction between season and time, and the random experimental error. Time of day when the greatest estrous activity occurred, effects of duration of estrus on the number of mounts received, and influence of size of the dominant follicle on time of ovulation were determined with the PROC GLM procedure of SAS with season and year in the model. Means were compared with a Student’s t-test with the PDIFF procedure in GLM of SAS. Effects of season and time on concentrations of estrogen and progesterone in plasma before and after estrus and ovulation were analyzed using the PROC MIXED procedure of SAS. Orthogonal contrasts (Steel et al., 1997) were used to compare means at times before and after estrus when the time effect was significant.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Season influenced ambient temperature on the day of estrus (Table 1Go; P < 0.01). During the two summers, there were 14 d when the maximum temperature was greater than 42°C. Daily minimum temperature was less than 0°C on 19 d during the two winters.


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  		Table 1. Ambient temperatures on the first day cows were in estrus
 
Estrus
Twice daily visual observation during the first summer failed to detect 29% (5 of 17) of estrous cows that were identified by HeatWatch and confirmed by concentration of progesterone in plasma. Four of the five cows not observed in standing estrus were mounted but did not stand, or they mounted other cows during the observation periods. Visual observation failed to identify only 5% (1 of 20) of estrous cows in the winter of yr 1.

Cows were in estrus longer in summer (Table 2Go) than in winter (P = 0.07) or spring (P < 0.05). During all seasons, the range for duration of estrus was 0.5 to 36.3 h (Table 2Go), and 70% of cows were in estrus for 11 to 20 h (Figure 1Go). The onset of estrus was not related to time of day (Figure 2Go). Season (P < 0.05; Table 2Go) affected the number of times cows were mounted by herdmates. Cows were mounted more times (P < 0.05) per estrus in the winter than summer or spring. The number of mounts that cows received per estrus ranged from 3 to 182 (Table 2Go), and 59% of cows were mounted between 20 and 79 times per estrus (Figure 3Go). The longest interval between subsequent mounts received also was influenced by season (Table 2Go; P < 0.05). Cows in estrus during summer had longer periods of inactivity between mounts received than in spring or winter. The maximum duration between mounts received during an estrus was 11.4 h.


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  		Table 2. Influence of season on estrus and ovulation of beef cows
 


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  		Figure 1. Percentage of cows that had various durations of estrus.

 


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  		Figure 2. Percentage of cows with the onset of estrus at various times of the day (0 = midnight).

 


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  		Figure 3. Percentage of cows that received various numbers of mounts during estrus.

 
Cows were mounted more times (Table 2Go; P < 0.05) per hour of estrus during winter than during other seasons. During all seasons, mounting activity was greatest (P < 0.01) between 0601 and 1200 (3.2 ± 0.2 mounts received/h of estrus) than during other times of the day (2.1 ± 0.2 mounts received/h of estrus; Figure 4Go). Duration of estrus and number of times a cow was mounted per estrus were correlated (r = 0.32; P < 0.01). Cows that were in estrus longer than 15 h received 58.4 ± 4.0 mounts, compared with 34.3 ± 4.0 mounts when cows were in estrus less than 15 h (P < 0.001).



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  		Figure 4. Number of mounts per hour of estrus during 6-h periods in beef cows. Means without a common letter (a, b) differ (P < 0.01).

 
Ovulation
The interval from the onset of estrus until ovulation was not influenced by season (Table 2Go; P > 0.1). Cows ovulated 31.1 ± 0.6 h after the onset of estrus. Time of ovulation after the onset of estrus ranged from 21.5 to 42.8 h (Table 2Go), and 64% of cows ovulated between 28 and 33 h after the onset of estrus (Figure 5Go). Time of ovulation was not related to time of day (P > 0.1). During each of six 4-h periods, between 13 and 23% of the cows ovulated. Interval from the end of estrus to ovulation was longer (P = 0.06) in winter and spring than during summer. Diameter of the ovulatory follicle (13.2 ± 0.2 mm) did not change during the 12 h prior to ovulation (P > 0.1), and season did not affect (P > 0.1) the size of the ovulatory follicle. Size of the ovulatory follicle and time of ovulation after the onset of estrus were not correlated (P > 0.1).



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  		Figure 5. Percentage of cows that ovulated at various hours after the onset of estrus.

 
Steroid Hormones
Concentrations of progesterone in plasma during the periovulatory period were not influenced by season (P > 0.1) and were greatest (Figure 6Go) 4 d before estrus and lowest the day before estrus (P < 0.01). Concentrations of progesterone were less than 0.5 ng/mL from d -1 through d 2 after the onset of estrus. Concentrations of estradiol in plasma increased (P < 0.01) from 1 d before estrus to a maximal concentration on the day of estrus. Concentrations of estradiol in plasma increased (P < 0.01) after concentrations of progesterone were less than 1 ng/mL. Plasma concentrations of estradiol decreased (P < 0.01) from 3.6 ± 0.5 pg/mL at 8 h after the onset of estrus to 1.7 ± 0.6 pg/mL by 16 h after the onset of estrus.



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  		Figure 6. Least squares means concentrations of progesterone and estradiol in plasma before and after estrus in beef cows. Day effect (P < 0.01; n = 12 cows per day) for progesterone (mean square error = 3) and estradiol (mean square error = 0.4).

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
The HeatWatch system identified 29% more cows in estrus during summer and 5% more during winter than twice daily visual observation for 30 min. Cows had more mounts per hour of estrus in winter than in summer, which may have resulted in more estrous cows identified by visual observation. Similarly, Stevenson et al. (1996) found that HeatWatch identified 27% more estrous beef heifers than twice daily visual observations for 45 min. Geary et al. (2000) found that observation for 2 h twice daily and using HeatWatch identified a similar number of estrous cows.

Concentrations of progesterone in plasma of all cows during the two estrous cycles were typical for cows with normal cycles (Garverick et al., 1971; Swanson et al., 1972; Wettemann et al., 1972) and began to decrease 3 d before estrus with lowest concentrations on the day before estrus. Similar to the results of Stevenson et al. (1998), concentrations of estradiol in plasma were greatest on the day of estrus determined by HeatWatch. In previous studies when estrus was determined by observation, concentrations of estradiol were greatest between 1 d before and the day of estrus (Wettemann et al., 1972; Chenault et al., 1975).

Seasonal effects on estrous behavior of dairy cows are not consistent. Trimberger (1948) observed dairy cows twice daily and concluded that season did not alter estrous behavior. Walker et al. (1996) found that increased temperature did not influence the duration of estrus in dairy cows when estrus was monitored continuously with a HeatWatch system. We found that beef cows were mounted more frequently during estrus in winter, and duration of estrus was longer during summer, with longer intervals between mounts. Using continuous visual observation, Pennington et al. (1985) also found that dairy cows had a longer, less intense estrus in hot weather, with longer intervals between mounts received. Seasonal effects on estrous behavior may differ among studies due to breed of cow, climate, or management practices. In our study, mean maximal ambient temperature was 34.6°C, whereas it was 24.4°C in the study by Walker et al. (1996) and 33.9°C in the study by Pennington et al. (1985). Management factors such as frequency of milking, movement of cows, feeding, and the types of footing surface may alter estrous behavior and could contribute to differences between studies (Pennington et al., 1985; Britt et al., 1986). Number of cows in estrus, age, or stage of the estrous cycle of cows mounting estrous cows also could influence estrous behavior (De Silva et al., 1981; Helmer and Britt, 1985; Floyd et al., 2001).

The effects of season on estrous behavior in this study may be related to differences in ambient temperature. Gwazdauskas et al. (1983) concluded that the number of mounts received increased linearly in dairy cows with increasing temperature up to 25°C, but decreased linearly after 30°C. During hot weather, Holstein cows exhibit signs of estrus (rubbing and licking), other than mounting, with greater frequency (Pennington et al., 1985). Seasonal effects on estrus could be due to climate effects on the willingness of herd mates to mount, rather than to a physiological effect of temperature on the cow in estrus.

A shorter duration of estrus with fewer mounts received has been observed for dairy and Bos indicus cows compared with an average estrus of 15 h with 48 mounts received that we found in nonlactating beef cows during spring and winter. In agreement with our study, Stevenson et al. (1996) observed that beef heifers were in estrus for 14 h with 50 mounts. Duration of estrus for dairy cows determined with continuous visual observation (Pennington et al., 1985; Walton et al., 1987) or the HeatWatch system (Walker et al., 1996; Dransfield et al., 1998; Xu et al., 1998) ranged from 7 to 13 h with 8 to 33 mounts received. Similarly, the duration of estrus for B. indicus cows ranged between 7 and 8 h with 19 to 25 mounts received (Rae et al., 1999; Yelich et al., 1999). Rae et al. (1999) found breed effects on duration of estrus and number of mounts received in Angus, Brahman, and crossbred cows. In addition, the first postpartum estrus in primiparous Angus x Hereford heifers (Ciccioli et al., 2001) and mature beef cows (Lents et al., 2000) was shorter (4 and 6 h, respectively) and had fewer mounts received (10 and 11 mounts received per estrus, respectively) than estrus in nonlactating cows in this study.

Cows were mounted more times per hour of estrus from 0601 until 1200. Similarly, dairy cows had their greatest estrous activity during the morning hours (De Silva et al., 1981). Other studies with dairy cows have not found an effect of time of day on estrous activity (Xu et al., 1998), or greater activity from midnight until 0600 was observed (Walton et al., 1987). Variation in times when cows were milked, moved, or fed (Pennington et al., 1985; Britt et al., 1986) or ambient temperature could influence when greatest estrous activity occurred.

Size of the ovulatory follicle was not influenced by season. The effect of heat stress on size of dominant follicles is inconsistent. Badinga et al. (1993) found that heat stress decreased size and fluid content of dominant follicles on d 8 of the cycle, and McNatty et al. (1984) and Badinga et al. (1994) observed that season influenced size of first wave dominant follicles and ovulatory follicles. Other studies determined that neither heat stress (Wolfenson et al., 1995; Trout et al., 1998) nor season (Wolfenson et al., 1997) influenced size of dominant follicles. Inconsistent effects of heat stress on follicle growth could be due to differences in duration of exposure, maximal ambient temperatures, or nutrient intake.

Ovulation occurred 31.1 ± 0.6 h after the onset of estrus, and season did not influence time of ovulation. Early studies determined that dairy heifers and cows ovulated 10.5 h after the end of estrus (Trimberger 1948). In the current study, the time of ovulation relative to the end of estrus was influenced by season, and cows ovulated between 8.3 h before and 16.6 h after the end of estrus. The slightly shorter interval from the end of estrus to ovulation in summer is associated with a slightly longer estrus in summer than in winter and spring. Since time of ovulation relative to the onset of estrus is not influenced by season, and time of ovulation relative to the end of ovulation is influenced by season, timing of AI should be from the onset of estrus. Dairy cows may ovulate earlier after the onset of estrus than beef cows. Based on ultrasonography, dairy cows ovulated 27.6 ± 0.6 h after the onset of estrus (Walker et al., 1996). Yelich et al. (1999) found that Angus, Brahman, and Senepol cows ovulated at 30.8 h after the onset of estrus. The shorter interval from onset of estrus to ovulation in dairy than beef cows may be influenced by management, nutritional requirements, stress associated with lactation, or physiological differences between breeds. In agreement with our results, Trimberger (1948) concluded that season did not influence the time of ovulation relative to the onset of estrus in dairy cows.

Dransfield et al. (1998) found that the greatest conception rate for dairy cows occurred when cows were inseminated 4 to 12 h after the first mount identified by HeatWatch. The optimal time of insemination may be different for dairy and beef cows because dairy cows may ovulate sooner after the onset of estrus than beef cows. The interval from the onset of estrus to AI to achieve maximal fertility has not been determined for beef cows. Although sperm are in the oviduct within minutes after AI (VanDemark and Moeller, 1951), it is not until about 8 h after AI that sperm with the ability to fertilize ova reach the upper oviduct. By 24 h after insemination, only a small percentage of sperm are still present in the bovine reproductive tract (reviewed by Hawk, 1987). Fertilization of aged ova may result in greater embryonic degeneration (Saacke et al., 2000). Trimberger (1948) determined that the optimum time to inseminate dairy cattle was between 6 and 24 h before ovulation, and conception rates were drastically decreased if cows were inseminated after ovulation. Fertilization rate was greater when dairy cows were inseminated 24 h compared with 0 and 12 h after the first mount received, as determined with the HeatWatch system (Saacke et al., 2000). However, embryo quality decreased as cows were inseminated later after the onset of estrus, and cows inseminated 24 h after the onset of estrus had a greater percentage of degenerating embryos than those inseminated at 0 and 12 h. When 32 primiparous cows were inseminated 14 to 20 h after the onset of estrus, 72% become pregnant (Ciccioli et al., 2001). In the current study, cows ovulated between 21 and 43 h after the onset of estrus. For maximal pregnancy rates, we speculate that beef cows should be inseminated 14 to 20 h after the onset of estrus.

We conclude that season alters estrous behavior of beef cows in Oklahoma. Cows receive fewer mounts in the summer and spring than in winter, and cows have longer intervals between mounts received during the summer when compared with winter and spring. Estrous cows are mounted more times between 0601 and 1200 than during other times of the day. Cows ovulate 31.1 ± 0.6 h after the onset of estrus, and time of ovulation after the onset of estrus is not influenced by season.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
The intensity of estrus detection should be increased during the summer. Estrus-detection aids should be used to identify cows with a short estrus, few mounts, or long intervals between mounts. Cows should be inseminated approximately 12 h after they are first observed in estrus, if twice daily visual observation is used to identify estrous cows. When beef cows are monitored continuously for estrus, precise timing of AI relative to the onset of estrus may increase pregnancy rates. Additional studies under different environmental conditions should be conducted to determine when to inseminate beef cows after the onset of estrus for maximal pregnancy rates.


   Footnotes
 
1 Approved for publication by the Director, Oklahoma Agric. Exp. Sta. This research was supported under project H-2331. Back

2 The authors acknowledge Pharmacia Animal Health for the Lutalyse and C. Lents, R. Jones, M. Anderson, S. Welty, D. Cox, M. Warner, and L. Mackey for technical assistance. Back

4 Present address: USDA-ARS, Dale Bumpers Small Farms Research Center, Booneville, AR 72927. Back

Received for publication April 5, 2002. Accepted for publication July 15, 2002.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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