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Effects of sequential or group exposure to unrestrained estrual females on expression of sexual behavior in sexually experienced beef bulls^1,2

Department of Animal Sciences, University of Kentucky, Lexington 40546-0215

	Abstract

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We tested the hypothesis that expression of sexual behavior in bulls is affected by the manner in which they are exposed to unrestrained, sexually receptive females. Twelve Angus bulls were used in a crossover design involving two treatments, each tested four times for a total of eight tests for each bull. Sexual interactions were quantified for each of four, 30-min periods under the following treatments: 1) exposure to each of four estrual females in sequence (SEQ); or 2) exposure to four estrual females as a group (GRP). Bulls were blocked into three testing groups, the order of which was stratified across eight test days. The order in which bulls were tested on a particular day had no effect on bulls’ expression of mount interactions, or flehmen responses, suggesting that each group of bulls had similar sexual motivation at the beginning of each test. However, the bull testing order x treatment x time interaction influenced mounting interval (P = 0.08), copulation frequency (P <0.05), and copulation success ratio (P <0.05). When bulls were in GRP and tested first on test days, more (P <0.05) copulations were distributed to the first three females encountered compared with either the fourth female (P <0.05) or to each of the other females in SEQ (P <0.05). During later tests, other bulls in GRP were not able to copulate as frequently (P <0.05) with each female, displayed lower (P <0.05) copulation success ratios, and were allowed copulations by fewer (P <0.05) females during each 30-min test. When bulls were in SEQ, they displayed similar numbers of copulations regardless of the order in which they were tested, and had stable mounting intervals; however, copulation success ratio decreased (P <0.05) more rapidly during subsequent tests. Flehmen responses were initially displayed more frequently (P <0.05) when bulls were in GRP, but this effect diminished during subsequent 30-min tests. In conclusion, exposure of bulls to GRP induced greater sexual responsiveness than SEQ; however, this effect was due to enhanced sexual activity during the early stages of sexual encounters and with females that were not recently mated. Interestingly, bulls seem to repeatedly copulate with each individual female until, apparently, female sexual receptivity became attenuated. Thereafter, recently mated females allowed fewer episodes of repeated copulations, but they did not completely cease copulating with novel bulls.

Key Words: Bulls • Coolidge Effect • Copulation • Intromission • Mounting • Serving Capacity

	Introduction

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Research concerning regulation of sexual behavior in bulls is impeded by the fact that existing methods involve conditions that may not be compatible with pasture mating. One of the more popular methods involves the use of severely restrained females (Blockey, 1976b, 1981; Price and Wallach, 1991); such females are usually not in estrus and may be sedated (Landaeta-Hernandez et al., 2001); thus, they do not represent natural mating stimuli. Despite the prevalence of their use, these approaches have not fully evaluated temporal changes in the expression of sexual behavior between males and females. This failure may be an underlying issue associated with reports that bull serving capacity has little relationship with herd fertility (Smith et al., 1981; Chistensen et al., 1982; Boyd et al., 1989). Some bulls that do not copulate with restrained females during such tests go on to display normal sexual behavior during pasture mating (Barth et al., 2004). Additionally, severely restraining females during these tests has been criticized as inhumane (Fraser, 1983). We recently described methods for quantifying sexual behavior of bulls using unrestrained females and concluded that the temporal expression of bull sexual behavior varies with the type of female stimulus. Specifically, we reported that the sexual activity of bulls exposed sequentially to each of four estrual females was greater than when bulls were exposed repeatedly to a familiar estrual female; however, bulls exhibited a decrease in sexual response after 2 h, in spite of having access to an additional novel, estrual female. The current study was undertaken to explore further the influence of unrestrained female stimuli on expression of bull sexual behavior in small-pen tests. We tested the hypothesis that bulls would show a greater sexual response in small-pen tests when paired with a group of unrestrained estrual females compared with tests involving sequential exposure to individual females.

	Materials and Methods

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General

We used 12 Black Angus bulls and 67 Black Angus females in a simple crossover design with repeated measures. The repeated measures were four, 30-min tests nested within eight different test days for each bull. The experiment was conducted between December 12, 2002, and January 3, 2003. With the exception of the seventh test, bulls were evaluated every 4 d. Due to the formation of a thick sheet of ice in the observation pen, the seventh test was postponed for an additional 4 d. Figure 1 illustrates the testing environment for this study. On test days, females were visually examined for behavioral estrus in a large observation pen (14.8 m x 3.05 m). Females were deemed to be in standing estrus when they would stand firm to at least three mounts from other females, indicated by no lateral or forward movement after being mounted. Behavior tests were conducted between approximately 1200 and 0200, when ambient air temperatures ranged from –8°C to 13.3°C. All experimental procedures were conducted at the University of Kentucky Animal Research Center in Wood-ford County, and were evaluated and approved by the University of Kentucky Institutional Animal Care and Use Committee.

View larger version (29K): [in this window] [in a new window]   Figure 1. Experimental procedure and testing environment for evaluating bull sexual behavior in small-pen tests, with unrestrained female stimuli paired individually or as a group. A) Overall pen dimensions and positions of surveillance cameras. B) Sequestration of test males and females during the pretest stimulation period, which was used to provide male test subjects with visual stimulation and to allow investigators to determine behavioral estrus status of female test subjects. C) Treatments and the method we used for exposing individual bulls to females. Treatments were exposure sequentially to four estrual females (SEQ) or exposure to a group of four estrual females (GRP). In the SEQ treatment, bulls received 30-min exposure to each female individually, after which the female was removed from the pen and replaced by a new female. In GRP, four estrual females were placed in each pen for 2 h.

The 12 Black Angus bulls were chosen at random from a larger group of bulls (n = 40) that had been reared and housed together. Bulls were assigned randomly to three different bull testing groups (bull groups 1, 2, and 3, respectively), with each group having four bulls. The order in which bull groups were tested on a particular day was numerically stratified across the eight test days. This procedure was followed to ensure that the order in which access to the females was allowed would not be confounded within bulls. Before the start of the experiment, bulls were subjected to a standard breeding soundness exam (Spitzer et al., 1988), and were all deemed acceptable for breeding based on these criteria. At the beginning of the experiment, mean age of bulls within groups was 640, 642, and 633 ± 8.8 d, respectively. Mean BW of the bulls within testing groups, measured at the beginning of the experiment, were 658, 607, 637 ±20 kg, respectively. All bulls used in this experiment had previous sexual experience, as they had been used in single-bull breeding pastures during the previous breeding season.

Figure 2 illustrates the experimental design for one hypothetical test day. Bulls were assigned to treatments based on a randomly chosen crossover arrangement, in which treatments were alternated across the eight behavior tests for each bull. The arrangement was balanced such that half of the bulls within each bull group were on the same treatment each day. We used four 30-min test periods to administer the following treatments: 1) individual exposure to each of four estrual females in sequence (SEQ), or 2) exposure to four estrual females as a group (GRP).

View larger version (16K): [in this window] [in a new window]   Figure 2. Experimental design and method for exposing bulls to treatments on one hypothetical test day. After testing a particular bull group, females were re-evaluated for estrus behavior; after replacing nonreceptive females (i.e., females that showed three instances of aversion to mounting), the next bull group was tested accordingly. This procedure was again followed for a third group of bulls each test day. This methodology was used in a replicated, simple crossover experiment with 12 bulls tested on eight different days. Treatments were balanced such that half the bulls in each bull group were on the same treatment each day. Treatments were: exposure sequentially to four estrual females (SEQ) or exposure to a group of four estrual females (GRP).

Sixty-seven Black Angus females of various ages (ranging from 20 mo to 9 yr) and parity were available to use as sexual stimuli. Females were blocked into three groups based on synchrony of induced behavioral estrus (see below). Mean BW of the females in female groups 1, 2, and 3 (measured at the beginning of the experiment) were 615, 601, and 549 ± 19 kg, respectively.

Induction of Female Sexual Receptivity for Sexual Behavior Tests

Initially, behavioral estrus was induced by providing 7 d of progesterone exposure from a controlled internal drug-releasing device (CIDR) (EAZI-Breed CIDR, Pfizer Animal Health, New York, NY), followed by an i.m. injection of 25 mg of PGF₂ (Lutalyse, Pfizer Animal Health) coincident with CIDR removal. Twenty-four hours later, an i.m. injection of 1 mg of estradiol cypionate (ECP; Pharmacia and Upjohn, Kalamazoo, MI) was administered to synchronize expression of behavioral estrus. Based on the temporal distribution of this induced behavioral estrus, females were blocked into three groups (female groups 1, 2, and 3; n = 22, 22, and 23, respectively) and then subjected to additional PGF₂/ECP injections 9/10, 12/13, and 15/16 d later, respectively. The first three behavior tests were conducted approximately 24 h after the second ECP injections. Thereafter, PGF₂/ECP injections were given at 10- and 11-d intervals, respectively, alternating the three female groups among the subsequent behavior tests, each of which was conducted 24 h after ECP injection.

Behavior Test Procedure

On each test day, when the first 16 females were determined to be in standing estrus, they were separated from the rest of the females, and gates within the large observation pen were closed, resulting in four testing pens of equal size (3.05 x 3.7 m; Figure 1). Bulls were sequestered in the testing pens, and equal numbers of females were distributed randomly within the pretest observation pens, still sequestered from the bulls. Video-recording equipment was set to capture all events in all pens simultaneously on one video cassette tape as previously described (Bailey et al., 2005). Females were allowed into pens either sequentially and switched every 30 min (SEQ) or as a group for 2 h (GRP; Figure 1C). Study personnel left the testing area immediately to allow animals to interact in a manner free of human interference; investigators could observe behavior in pens using a monitor interfaced with the recording equipment, which was located out of the sight of animals.

A particular group of females served as sexual stimuli for all three groups of bulls on each test day. Each group of bulls was allowed to observe mounting activity among the females as described previously (Bailey et al., 2005); additionally, the last two groups of bulls were allowed to view heterosexual activity. By consistently monitoring female mounting activity, we were able to ensure that only females allowing mounting were placed with bulls during subsequent tests. This monitoring included females that were not placed with bulls initially. Based on three instances of aversion to mounting, we consistently replaced two to three females after the first bull group, and three to five additional females after the second bull group; all other females continued to allow mounting. On occasions when animal welfare concerns arose (e.g., fatigue or injury), females were immediately removed from the test pen and replaced by another female that had previously allowed three mounts. Out of the 384 individual test periods we recorded, nine females were replaced in this manner.

Categories of Bull Sexual Behavior

As we have previously suggested (Bailey et al., 2005), it is difficult to evaluate ejaculation frequency in bulls due to an inability to account for all ejaculations that occur (Bailey, 2003). Hence, we quantified mount interactions, mounts with intromission (i.e., copulation), and mounts without intromission. As in our previous study (Bailey et al., 2005), we defined a mount interaction as any movement by the bull toward a female, during which both front feet of the bull were raised off the ground, culminating in physical contact with the female, regardless of orientation. A mount with intromission was defined as a properly oriented mount on the posterior portion of the female accompanied by insertion of the penis into the vagina and followed by obvious pelvic thrusting, with or without a final, deep pelvic thrust. On some occasions, penis insertion could not be verified on the video tapes. If we could not verify penis insertion on the tape and the bull did not display a final, deep pelvic thrust, the behavior was classified as a mount without intromission. Mounts without intromission also included other instances when the bull displayed a properly oriented mount but verifiably failed to display intromission and pelvic thrusting.

Because bull mounting activity could potentially be altered in terms of both frequency (i.e., the number of mounts during each 30-min period) and/or intensity (i.e., how close in time a series of mounts is expressed), we calculated mean mounting interval (i.e., the intermount time interval), which represents the mean time (in minutes) that elapsed between mount interactions displayed by each bull during each of the 30-min periods. If a bull did not display mount interactions (or displayed only one) during a test, this was classified as a no-response for mounting interval and was not included in the final analysis. To investigate the possibility that a group of estrual females would induce a greater response in the expression of male appetitive behaviors (Beach, 1979), we quantified bull flehmen responses. A flehmen response was defined as a flexing of the bull’s nostrils and retraction of the upper lip following investigation of a female’s perineal, flank, or leg region.

Statistical Analyses

Numbers of mounts, mounts with intromission, mounts without intromission, mean mounting interval (minutes), copulation success ratio (i.e., the proportion of mount interactions culminating in copulation), and flehmen responses were subjected to statistical analyses. Data were analyzed by ANOVA using the MIXED procedure of SAS (v. 8.02; SAS Inst., Inc., Cary, NC). The models included effects for treatment, time (i.e., the 30-min tests nested within test day), test day, the order in which bulls were tested (bull testing order), and bull group. In addition, we included the interactions of treatment x time, treatment x bull testing order, time x bull testing order, and treatment x time x bull testing order. We used animal nested within treatment as a random subject effect and bull group was used as a random group effect; both effects were included in the model to account for possible between-subject heterogeneity of variance/covariance structure (Littell et al., 1996, 1998). Least squares means procedures were used to calculate means and standard errors, and the PDIFF option of SAS was used to compare statistically means associated with significant (P <0.05) effects in the model(s).

Orthogonal polynomial analysis was used to describe changes in bull sexual behavior over the four 30-min test periods. Data were analyzed for linear, quadratic, and cubic trends within each treatment. All data presented in this manuscript are least squares means ±pooled SEM, using individual animal as the experimental unit.

To evaluate the manner in which bulls distributed copulations among females, an additional ANOVA was conducted using the same procedure as above. In this analysis, the total number of copulations received by each female and the order in which they received them (i.e., female copulation order) were calculated and used as dependent variables. We included effects and interactions in this analysis involving female order (e.g., female copulation order x treatment, female copulation order x treatment x time, etc.). To determine the temporal distribution of copulations among stimulus females, we conducted an additional analysis using the average number of females receiving copulations during each of the 30-min tests as the dependent variable.

One bull in bull group 1 displayed a condition best described as macrophallus. We do not know how this condition manifested itself but with attempts to copulate, the bull’s penis would become wedged between the two animals, resulting in a high rate of intromission failure (>75%). We could not reliably determine the extent to which the bull was displaying mounts with intromission vs. mounts without intromission. This condition also resulted in the bull displaying increasingly decreased mounting intervals (approximately one mounting event every 25 seconds), which was well outside three standard deviations of the mean. We chose to eliminate this bull from all statistical analyses.

	Results

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Mount Interactions

The effects of treatment, time, and the treatment x time interaction were all significant (P <0.01) in the analysis of mount interactions. Overall, when bulls were in GRP, they expressed more (P <0.01) mount interactions and, overall, mount interactions changed across time in a quadratic manner (P <0.01). The treatment x time interaction for mount interactions suggested that during the first 30-min tests, there were more (P <0.001) mount interactions when bulls were in GRP compared with when they were in SEQ. During the second, third, and fourth 30-min tests, mount interactions were similar when bulls were in either SEQ or GRP. Mount interactions did not change across time in SEQ, whereas they decreased in a quadratic manner (P <0.001) when bulls were in GRP. For continuity, we show the bull testing order x treatment x time interaction (P = 0.87) associated with bull mounting behavior in Figure 3A.

View larger version (21K): [in this window] [in a new window]   Figure 3. Mount interactions (A) and mounting intervals (B) displayed by bulls tested first (1), second (2), or third (3) on particular test days. Treatments were exposure to four estrual females in sequence (SEQ; white bars) or exposure to four estrual females as a group (GRP; black bars). More mount interactions (P <0.05) occurred when bulls were in the GRP treatment, but only during initial 30-min tests (Bars with different letters differ (P <0.05) and are associated with the treatment x time interaction, P <0.05). Within Panel B, bars with different letters differ, P <0.05. Data are least squares means ±pooled SEM.

The effects of time and the treatment x time interaction were significant (P <0.05) in the ANOVA for mounting interval; bull testing order and the bull testing order x treatment x time interaction tended (P = 0.07 and 0.08, respectively) to influence mounting interval. The treatment x time interaction associated with mounting interval showed that during the first 30-min tests, mounting intervals were decreased (P <0.05) when bulls were in GRP compared with when they were in SEQ. During the second 30-min tests, mounting intervals were similar when bulls were in GRP compared with when they were in SEQ. During the third and fourth 30-min tests, respectively, mounting intervals were increased (P <0.05) when bulls were in GRP compared with when they were in SEQ. Mounting interval did not change across time when bulls were in SEQ, whereas it increased in a linear manner (P <0.05) when bulls were in GRP. For continuity, we show the bull testing order x treatment x time interaction (P = 0.08) associated with mounting interval in Figure 3B.

Mounts with Intromission (i.e., Copulations)

The effects of treatment, time, treatment x time interaction, bull testing order, and the bull testing order x treatment x time interaction were all significant (P <0.05) in the analysis of mounts with intromission. The bull testing order x treatment x time interaction (Figure 4A) was caused by the following: 1) bulls tested first on a particular test day and in the GRP treatment showed the highest frequency of copulations during the first 30-min tests, followed by decreasing (but maintained) copulation rate thereafter; bulls in GRP and tested second or third on particular test days copulated just as frequently as bulls tested first, but only during the first 30-min tests; thereafter, copulation rate decreased more dramatically during subsequent tests; 2) when bulls were in GRP, they expressed more copulations (approximately twice the level) compared with bulls in SEQ, but only during the first 30-min tests; thereafter, the number of copulations during each test was similar between SEQ and GRP; and 3) when bulls were in SEQ, copulation frequency did not change across time, regardless of the order in which bulls were tested. However, when bulls were tested last and in SEQ, they displayed fewer copulations (P <0.05) during each of the 30-min tests compared to when they were tested first or second and in SEQ, respectively.

View larger version (21K): [in this window] [in a new window]   Figure 4. A) Mounts with intromission (i.e., copulations) and B) copulation success ratio displayed by bulls tested first (1), second (2), or third (3) on particular test days. Treatments were exposure to four estrual females in sequence (SEQ; white bars) or exposure to four estrual females as a group (GRP; black bars). Data presented are least squares means ±pooled SEM. Within each panel, bars with different letters differ, P <0.05.

The ANOVA for copulation success ratio revealed that treatment, time, and bull testing order, were all significant (P <0.05), as were the interactions of treatment x time and bull testing order x treatment x time. All other effects and interactions were not significant. The bull testing order x treatment x time interaction (Figure 4B) shows that copulation success ratio increased in a quadratic manner (P <0.05) when bulls were in SEQ, regardless of the order in which they were tested. However, when bulls were tested last on a particular test day and in SEQ, maximal copulation success ratio was lower (P <0.05) compared with when bulls were tested first or second on test days and in either SEQ or GRP. When bulls were in GRP and tested first or second on a particular test day, copulation success ratio did not change over time; however, when bulls were tested last on a particular test day and in GRP, copulation success ratio decreased in a linear fashion (P <0.05) over the four 30-min test periods. The other differences we noted between these treatments at particular times with respect to copulation success ratio came during the final tests, where bulls in GRP had higher copulation ratios (P <0.05) during the first two 30-min periods compared with when bulls were in SEQ during these times. Thereafter, copulation success ratio was similar between treatments.

Mounts Without Intromission

The effects of time and the order in which bulls were tested were significant (P <0.05) in the analysis of mounts without intromission. All other effects, including treatment and the treatment x time interaction were not significant. The time effect indicates that mounts without intromission decreased in a quadratic fashion (P <0.01) across the four 30-min tests, whereas the order effect indicates that bulls tested first with stimulus females expressed fewer (P <0.05) mounts without intromission than when bulls were tested second or third, respectively. Mounts without intromission were similar when bulls were tested second or third on a particular test day, regardless of treatment.

Flehmen Responses

Flehmen responses decreased over time (P <0.05) in a quadratic manner, whereas when bulls were in GRP, they tended (P = 0.08) to express more flehmen responses than when bulls were in SEQ. The treatment x time interaction (P <0.05) suggested that flehmen responses did not change over time when bulls were in SEQ; however, more flehmen responses (P <0.05) were concentrated in the first 30-min tests when bulls were in GRP and decreased in a quadratic manner (P <0.05). All other effects and interactions were not significant, including those involving bull testing order and associated interactions. For continuity, we show the bull testing order x treatment x time interaction (P = 0.19) in Figure 5.

View larger version (10K): [in this window] [in a new window]   Figure 5. Flehmen responses over time of bulls exposed to four estrual females in sequence (SEQ; white bars) or exposed to four estrual females as a group (GRP; black bars). Bars with different letters differ (P <0.05) but are associated with the treatment x time interactions, P <0.05. Flehmen responses decreased in a quadratic manner (P <0.05) when bulls were in GRP, whereas they did not change over time when bulls were in SEQ, regardless of the order in which bulls were tested. The bull testing order x treatment x time interaction was not significant, P = 0.19. Data are least squares means ±pooled SEM.

The ANOVA for the distribution of mounts with intromission among stimulus females revealed that treatment, female copulation order, and the female copulation order x treatment interaction were all significant (P <0.05). Additionally, the bull testing order x female copulation order x treatment interaction also was significant (P <0.05). This interaction is shown in Figure 6A and was caused by the following: 1) bulls distributed copulations among stimulus females equally when they were in the SEQ treatment, regardless of the order in which bulls were tested on a particular day; 2) when bulls were in GRP, they repeatedly copulated with the first three females encountered, whereas the fourth female encountered in GRP received fewer (P <0.05) copulations; 3) when bulls were in GRP and tested second on a particular test day, the first female received more copulations (P <0.05) than each of the other three females in the pen; and 4) when bulls were in GRP and tested last on a particular test day, the first three stimulus females received similar numbers of copulations, which were not different from the numbers of copulations received by the first three females in the SEQ treatments. Thereafter, the fourth female in GRP received fewer (P <0.05) copulations compared with the fourth female in SEQ.

View larger version (22K): [in this window] [in a new window]   Figure 6. A) Distribution of copulations among stimulus females when bulls were tested first (1), second (2), or third (3) on particular test days, and B) the average number of females receiving copulations during each of the 30-min tests when bulls were tested first (1), second (2), or third (3) on particular test days. White bars = exposure to four estrual females in sequence (SEQ). Black bars = exposure to four estrual females as a group (GRP). Within each panel, bars with different letters differ, P <0.05. Data are least squares means ±pooled SEM.

The ANOVA for average number of females receiving copulations during each of the 30-min tests revealed that treatment, time, and the treatment x time interaction were all significant (P <0.05) effects. In addition, bull testing order and the bull testing order x treatment x time interaction were significant (P <0.05). The bull testing order x treatment x time interaction is shown in Figure 6B and was caused by the following: 1) by default, bulls repeatedly copulated with similar numbers of females in each of the 30-min tests when they were in SEQ, regardless of the order in which they were tested on a particular test day; 2) when bulls were in GRP and tested first on a particular day, they copulated with more females during each of the 30-min tests compared with when they were in SEQ and tested first; and 3) when bulls were in GRP and tested either second or third on a particular test day, bulls copulated with more females (P <0.05) during only the first and second 30-min tests than when they were in SEQ; thereafter, the number of females receiving copulations decreased to a level that was not different from when bulls were in SEQ.

	Discussion

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Many investigators have suggested that bulls express sexual behavior merely as a result of innate or inherent sexual libido (Blockey, 1979a; Chenoweth, 1981, 1983), and that restraint of females is necessary to allow bulls to display this. This notion is related to other suggestions, for example, that an immobile, inverted, U-shaped object is the strongest stimulus inducing copulatory behavior in bulls (Chenoweth, 1981; Price, 1987). The notion that an immobile, inverted, U-shaped object induces copulatory behavior in bulls also has been cited as justification for the use of sedated, severely restrained females in tests (Chenoweth, 1981; Price, 1987), and this approach is still being practiced today (Barth et al., 2004). These assertions seem tenuous based on the results of our present experiment. Specifically, our data show that a group of unrestrained, sexually receptive females induces greater sexual responsiveness in bulls than sequentially pairing them with individual females, even though the duration of such tests was equivalent. This is the first direct report of such a phenomenon in small-pen tests of sexual behavior in the bull, and it seriously calls into question the validity of short-term tests that use single, restrained estrual females. The underlying assumption concerning bull sexual behavior (i.e., males are sexually active, females are sexually passive) has led to these and other practices that seem questionable based on our observations. These practices include using restrained, nonestrual females (Wallach and Price, 1988) or even restrained male cattle (Amann and Almquist, 1976; Henney et al., 1990; Brockett et al., 1994) as sexual stimuli for bulls.

Although we agree that these methods decrease stimulus variation, and that bulls certainly express mounting behavior in these tests, it is important to point out that investigators using these methods have assumed that stimulus condition is negligible in terms of regulating the temporal expression of copulatory behavior in the bull. This is an unfounded assumption based on observations made by Barth et al. (2004), who found that some bulls will not copulate with restrained females, whereas they will readily display normal copulatory behavior during pasture mating. Similarly, researchers studying Bos indicus bulls have reported that many bulls do not display intense sexual behavior under small-pen tests with restrained females (Chenoweth and Osbourne, 1975; Chenoweth, 1981), especially in the presence of investigators. In this regard, traditional approaches to quantifying bull sexual behavior completely ignore potentially important sexual interactions that occur within the normal context of natural mating. The normal context of natural mating involves oscillating patterns of sexual responsiveness, which are mediated by reciprocal attractiveness of the stimulus partner(s) (Pfaus, 1996; Beach, 1979) and temporal sexual satiety, which may be transient (Pfaus, 1996; Beach, 1979). With specific reference to cattle, temporal sexual responsiveness seems to be related to variation in the novelty of conspecifics, sexual receptivity of stimulus females (Bailey et al., 2005) and, at least in small-pen tests, the method used to introduce stimulus partners. Additionally, investigators who have used restrained male or female conspecifics have not fully considered whether bull sexual responsiveness under these conditions is being influenced by phenomena related to classic Pavlovian conditioning. This is a possibility that has not received much attention, although some researchers have reported there may be decreases in bull reaction time to first copulation when they are repeatedly exposed to stimuli that are restrained (Landaeta-Hernandez et al., 2001).

Importantly, we found that the aforementioned increases in bull sexual responsiveness were concentrated within the initial stages of sexual encounters. Moreover, bulls preferentially distributed copulations through repeat breeding when females were presented as a group, as suggested by de Araujo et al. (2003) and by data from Williams (1988). This is suggested because, based on the order in which females allowed copulation, the last female in the group received less copulation than the other females. However, we do not know whether postcopulatory inhibition of male sexual behavior precluded copulation with the last female or whether the duration of the tests was insufficient to allow further copulation with the female. Based on the results of our previous study (Bailey et al., 2005), where almost all bulls tested showed transient sexual satiety after 2 h of copulation, it is likely that bulls in the present study also were transiently sated as the initial tests came to an end. In support of this conclusion, we found that mounting intervals increased in a linear fashion for bulls tested first on a particular day, suggesting that their mounting activity was becoming less intense. This finding is likely related to the observations of Katz and Price (1986), who noted that as bulls express a series of ejaculatory responses, postcopulatory inhibition becomes evident, as a notable increase in mounting interval ensues (Katz and Price, 1986). Under our study conditions, as additional tests ensued, novel bulls were not able to distribute as many copulations among all stimulus females presented as a group, despite the fact that we documented that each female presented was receptive to mounting. In this regard, mounting intervals during these tests seemed to be less dramatically altered and were maintained by bulls.

As the previous statement suggests, our data also illustrate an important aspect of female sexual receptivity that has not been extensively studied. Females receiving access to novel bulls continued to allow some level of copulation, although copulation frequency was markedly attenuated in terms of bulls’ ability to repeat-breed each female intensely. In this regard, even though females did not allow copulations as intensely as novel bulls were attempting them, the "Coolidge Effect" in cattle may not be a sexually dimorphic phenomenon. This brings up the possibility that individual females prefer longer intervals between copulatory bouts with one particular bull and after some time, may completely cease copulation. Their willingness to allow further copulation may be changed if they are allowed a period of rest (Bailey et al., 2005) or encounter novel bulls, as in the present experiment. These observations may be related to paced-mating in females (for review, see Paredes and Vasquez, 1999), which is a hypothesis that has yet to be tested in cattle. It is possible that females prefer a few copulations with several bulls rather than numerous copulations with one bull, which adds another aspect of complexity to natural mating in the bovine. Future studies in this area would do well to consider game theory concepts, evolutionarily stable strategies, sperm competition, and female mate-selection theory as potentially important in determining how cattle interact sexually to affect how sperm is allocated dynamically.

Our observations clearly contrast with the work of Blockey (1976b), who reported that Bos taurus bulls rarely copulate with the same female more than twice when a group of them are available and instead distribute one or two copulations equally among them all. Blockey (1976a,b) failed to acknowledge that bulls show periods of transient sexual satiety, which diminishes the probability that a bull will continue to display copulatory bouts with additional estrual females, even if they are novel (Bailey et al., 2005). Importantly, the work by Blockey (1976a) did not recognize that female sexual receptivity is variable and that some estrual females that allow mounting will not allow copulation; still others may allow as many as 30 copulations in a 2-h period (Bailey et al., 2005). These factors would directly modify a bull’s ability to distribute copulations equally with every estrual female available under natural mating conditions. These criteria ultimately determine how sperm is allocated dynamically among several estrual females that are simultaneously soliciting copulation, factors that may need further research as the use of estrous synchronization in the beef cattle industry will likely increase.

Our observations on breeding patterns of bulls agree with those of other researchers studying both Bos taurus bulls (Boyd et al., 1989; Godfrey and Lunstra, 1989; de Araujo et al., 2003) and Bos indicus bulls (Williams, 1988; Silva-Mena et al., 2000), wherein bulls display preferences for repeat-breeding females. Our data add to these assertions that there are temporally relevant considerations to be made with respect to this phenomenon. Our data show that bulls repeat-breed individual females until female sexual receptivity becomes attenuated and/or bulls approach sexual satiety. In the present experiment, we documented individual variation in mating patterns of bulls. Figure 7 shows these data, which were taken from when bulls were tested first on particular test days. We found that some bulls show little diminution of sexual responsiveness during the 2 h of testing, regardless of whether females were presented sequentially or as a group (Figure 7A, Bull L135; Figure 7B, Bull L115). Some bulls failed to respond to all estrual females presented sequentially and showed similar sexual attenuation despite access to a group of estrual females not recently mated (Figure 7E, Bull L152; Figure 7F, Bull L125). Some bulls copulated continually, but at a much lower frequency (Figure 7C, Bull L027; Figure 7D, Bull L120). These variable mating patterns displayed toward unrestrained, estrual females may constitute new selection criteria for retention of breeding bulls; however, future studies will need to determine the relationship between bull sexual responsiveness in small-pen tests, dynamic mating patterns at pasture, and how these patterns influence semen quality, quantity, and distribution.

View larger version (24K): [in this window] [in a new window]   Figure 7. Variation in cumulative copulatory responses among individual bulls exposed to females sequentially (SEQ) or as a group (GRP). Data are least squares means ±SEM of repeated measurements on individual bulls taken from when they were first tested on particular test days.

	Implications

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	Footnotes

 
¹ Published with the approval of the Director of the Kentucky Agric. Exp. Stn. as Publication No. 05-07-051.

² This work supported by a predoctoral fellowship (J. D. Bailey) through the Training Program in Reproductive Sciences, NIH T32 HD07436. The authors thank B. Hightshoe, J. Greenwell, S. Rudd, J. Peil, J. D. Rhinehart, and A. M. Arnett for their excellent technical assistance. In addition, we thank W. J. Silvia for assistance in designing this experiment.

³ Current address: Dept. of Anat. and Neuro., Univ. of Kentucky Coll. of Med., Chandler Med. Center, MN 225, Lexington 40536-0298.

⁴ Correspondence: 803 W. P. Garrigus Bldg. (phone: 859-257-7512; fax: 859-257-3412; e-mail: kkschi1{at}uky.edu).

Received for publication December 22, 2004. Accepted for publication April 8, 2005.

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