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Effects of novel females and stage of the estrous cycle on sexual behavior in mature beef bulls^1,2

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

	Abstract

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The objective of this experiment was to determine the effects of unrestrained females on sexual behavior of bulls. Twelve Angus bulls were used in three Latin square replicates where sexual interactions between one bull and one female were quantified for each of four 60-min tests (T1, T2, T3, and T4, respectively). All bulls received the following treatments: 1) exposure to four estrual females in sequence (A-B-C-D); 2) exposure to two estrual females in alternating sequence (E-F-E-F); 3) exposure repeatedly to one estrual female (G-G-G-G); and 4) exposure repeatedly to one diestrous female (CON). During T1, mount interactions, mounts with intromission and mounting intervals were similar when bulls were in A-B-C-D, E-F-E-F, or G-G-G-G. Fewer mount interactions, no mounts with intromission, and increased mounting intervals (P < 0.05) occurred in CON. During T2, there were more mount interactions, more mounts with intromission, and decreased mounting intervals (P < 0.05) when bulls were in A-B-C-D or E-F-E-F compared with when they were in G-G-G-G or CON. More mount interactions (P < 0.05) occurred in G-G-G-G compared with CON, but mounts with intromission and mounting intervals did not differ. During T3, more mount interactions (P < 0.05) occurred in G-G-G-G than in CON; otherwise, sexual behaviors were similar among treatments. Mounting intervals during T3 were similar among A-B-C-D, E-F-E-F, and G-G-G-G, but were all decreased (P < 0.05) compared with CON. During T4, more mount interactions, more mounts with intromission, and decreased mounting intervals (P < 0.05) occurred when bulls were in A-B-C-D compared with other treatments. Mount interactions were similar when bulls were in E-F-E-F, G-G-G-G, or CON; however, more (P < 0.05) mounts with intromission occurred when bulls were in E-F-E-F compared with G-G-G-G or CON. Mounting intervals during T4 were decreased (P < 0.05) in E-F-E-F compared with the CON treatment, whereas in G-G-G-G, they were intermediate. Mounts without intromission were not affected by female novelty or receptivity, but novel females induced more flehmen responses. In conclusion, novel, females, overall, enhanced sexual activity of bulls; however, bull sexual responses diminished after 2 h, even when a novel female was presented. Estrual females that were repeatedly paired with bulls displayed diminished sexual receptivity, but if mated females were rested for 60 min, they allowed further copulation from familiar bulls that were not sexually sated.

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

	Introduction

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Although the sexual behavior of bulls has been described (Blockey, 1976b; Chenoweth, 1983; Price, 1987), and methods for quantifying "serving capacity" in bulls have been developed (Blockey, 1976, 1981; Boyd et al., 1989), few studies have focused on quantifying sexual interactions between males and females. Most serving capacity tests that have been used to assess bull sexual performance ignore the female as an active participant in mating. Usually, females are severely restrained (Blockey, 1976a, 1981; Bertram et al., 2002), sexually nonreceptive (Blockey, 1976a; Chenoweth et al., 1979; Wallach and Price, 1988), and/or sedated (Landaeta-Hernandez et al., 2001), and thus do not represent natural mating stimuli. These tests are not useful for understanding the biological basis of sexual interactions nor do they evaluate temporal changes in the expression of bull sexual behavior. An ethological approach is needed to investigate sexual responses of bulls that are repeatedly subjected to stimuli that more closely mimic natural mating. Although some researchers have used unrestrained, sexually receptive females to assess bull serving capacity (Dykeman et al., 1982; Carpenter et al., 1992; de Araujo et al., 2003), the effects of changes in female sexual receptivity on the expression of bull sexual behavior have not been determined. Earlier investigators (Almquist and Hale, 1956) reported that sexually sated bulls show renewed sexual responsiveness when paired with a novel, estrual female (i.e., the "Coolidge Effect"). We took advantage of this phenomenon and developed an ethological approach to studying sexual behavior in the bull and tested the hypothesis that their sexual responsiveness is influenced by both the novelty and receptivity of the female stimulus. This approach allowed us to more thoroughly evaluate how the temporal expression of bull sexual behavior changes with respect to variable female stimulus condition.

	Materials and Methods

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General

Twelve Black Angus bulls and 97 females of predominantly Black Angus breeding were used in three replicates of our experiment. The experimental design involved exposure of the bulls (n = 4 in each replicate) to each of four treatments for each of four periods (i.e., test days) in a Latin square arrangement (Snedecor and Cochran, 1989) with repeated measures. Each bull was subjected to a different treatment each test day, where they were imposed on bulls during four 60-min tests (i.e., the repeated measures). Bulls were repeatedly tested in this manner to evaluate temporal changes in sexual responsiveness exposed to variable female stimuli. Bulls were exposed to only one female at a time and were tested individually to eliminate intermale aggression. The 60-min tests were administered under the following treatments: 1) exposure to four estrual females in sequence (A-B-C-D); 2) exposure to two estrual females in an alternating sequence (E-F-E-F); 3) repeated exposure to one estrual female (G-G-G-G); and 4) repeated exposure to one diestrous female (CON). Hence, a novel female was introduced during the first, second, third, and fourth 60-min tests when bulls were in the A-B-C-D treatment, whereas a novel female was introduced during only the first and second 60-min tests in the E-F-E-F treatment. The same individual female was introduced, removed, and then reintroduced in each 60-min test when bulls were in the G-G-G-G and CON treatments, respectively. Figure 1C illustrates these treatments.

View larger version (26K): [in this window] [in a new window]   Figure 1. Experimental procedure and testing environment for evaluating bull sexual behavior in small-pen tests with variable, unrestrained female stimuli. 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 estrous behavior of female test subjects. C) Treatments and the method we used for exposing individual bulls to individual females. Bulls received 60-min exposure to each female individually, after which the female was removed from the pen and either replaced by a new female or reintroduced, depending on the treatment. This procedure was used in replicated, Latin square experiments using 12 male test subjects.

Replicates 1, 2, and 3 were conducted between December 20, 2001, and February 8, 2002; March 18 and May 8, 2002; and November 4 and November 16, 2002, respectively. Sexual behavior tests were conducted between 1500 and 0400, 1500 and 0100, and 1300 and 2300, when ambient air temperatures ranged from –13 to 20°C, from 0.5 to 25°C, and 2 to 14°C, respectively. Intervals between testing days were between 14 and 17 d in Replicates 1 and 2, whereas a 4-d test interval was used in Replicate 3. Tests were postponed during excessive rain, snow, or during icy conditions. All experimental procedures were conducted at the University of Kentucky Animal Research Center in Woodford County, KY, and were approved by the University of Kentucky Institutional Animal Care and Use Committee.

Bulls

Twelve sexually experienced Black Angus bulls were chosen randomly from two different bull herds for use in this experiment. Eight different bulls were used from the first herd for the first two replicates, whereas four bulls were used from the second herd for the third replicate. Each of these bulls was determined to be reproductively sound based on a breeding soundness exam (Spitzer et al., 1988). At the beginning of each replicate, bulls were 1.7 ± 0.04, 1.9 ± 0.01, and 1.6 ± 0.06 yr of age and weighed 557 ± 17, 669 ± 9.9, and 574 ± 13 kg for Replicates 1, 2, and 3, respectively.

Females

Replicates 1 and 2 involved a group of 30 heifers (Black Angus and Black Angus x Hereford were the predominant breeds) ranging in age from 1.7 to 2 yr of age and weighing 442 ± 11 and 551 ± 20 kg at the beginning of each replicate, respectively. They were subjected to estrous synchronization, which involved feeding melengestrol acetate for 7 d followed by an i.m. injection of 25 mg of PGF₂ (Lutalyse, Pfizer Animal Health, New York, NY) coincident with melengestrol acetate withdrawal. Ten heifers were chosen for use in each of the first two replicates based on homology of ovarian structures (i.e., presence of a corpus luteum determined via transrectal ultrasound) and expression of estrous behavior (i.e., female would stand to allow at least three mounts from other females) within 48 h of PG administration. We observed these females for 30 min every 8 h after PG administration to evaluate estrous behavior. The first 10 females to display estrous behavior served as stimuli for a particular replicate.

For Replicate 3, 67 Black Angus females, ranging in age from 1.6 to 9 yr and weighing 508 ± 24 kg, were blocked into three herds (n = 22, 22, and 23, respectively) based on time of induced estrus expression. Estrus was induced by providing 7 d of progesterone exposure from a controlled internal drug-releasing device (CIDR; EAZI-Breed CIDR, Pfizer Animal Health), followed by i.m. injection of PG at the time of 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 estrus, which was evaluated for 30 min every 8 h after this injection until all females expressed estrous behavior.

Induction of Female Sexual Receptivity for Sexual Behavior Tests

After the first observed estrus, females in each replicate were administered PG and ECP 9 and 10 d later, respectively, to induce sexual receptivity coinciding with each of the first behavior tests. Thereafter, each group consistently received additional injections of PG and ECP every 9 and 10 d, respectively. One female chosen at random did not receive these injections and remained in diestrus to serve as stimulus for the CON treatment. This animal was treated with PG immediately after a behavior test to keep its estrous cycle synchronized with the rest of the group.

Facilities for Evaluating Bull Sexual Behavior

Facilities used to evaluate bull sexual behavior are depicted in Figure 1. They included a large (14.8 m x 3.05 m) observation pen and four smaller adjoining pens (1.85 m x 3.7 m). The large pen could be subdivided by gates to create four separate pens in which to individually test bulls. Before subjecting bulls to the four 60-min tests, we provided a pretest stimulation period, during which females were allowed to interact and bulls were allowed to observe these interactions. This allowed us to verify that females were in standing estrus (i.e., females allow at least three mounts from other females) and provided an opportunity for bulls to become sexually stimulated.

Once the required number (n = 7) of females was determined to be in standing estrus, all females were removed from the observation pen and placed in an adjacent holding pen, where nonreceptive females were separated. Gates were then closed to partition the large observation pen into four test pens of equal size (3.7 m x 3.05 m). Each of the four bulls was then sequestered into one of the four observation pens.

Once individual bulls were placed in test pens, an individual female was allowed to enter and was removed after 60 min, regardless of treatment; this procedure was followed for the three additional 60-min tests. Male/female sexual interactions were captured continuously by four surveillance cameras (SVC-1700, Speco Technologies, Amityville, NY). Each camera was positioned to provide a complete view of each test pen and captured digital images in black and white. During testing, images were recorded on a videocassette tape using a duplex-multiplexer (Robot MVP19P-30, Sensormatic Electronics Corp., Boca Raton, FL) interfaced with a 24-h real-time videocassette recorder (SRT-2400, Sanyo Electric Co., Ltd., San Diego, CA). This equipment permitted simultaneous recording of behavior in all four test pens, as well as viewing test pens simultaneously or individually. In addition, this equipment allowed personnel to leave the test area immediately, providing the animals the opportunity to interact in a manner free of human interference. At the completion of each replicate of the experiment, videotapes were examined to quantify various categories of sexual behaviors.

Categories of Bull Sexual Behavior

Previous researchers have suggested the term "service" to describe a behavior wherein a bull displays a properly oriented mount, penile insertion into the vagina (i.e., intromission), followed by several thrusts culminating with a final, deep pelvic thrust, indicative of ejaculation. Many researchers have reported the number of "services" (or mounts with ejaculation) in serving capacity tests as a measure of bull sexual performance. We found this definition of ejaculation to be problematic. Although it was obvious that the majority of bulls displayed a final, deep pelvic thrust after most mounts with intromission, it was also quite evident that bulls can ejaculate without displaying such a thrust (Bailey, 2003). Specifically, we observed bulls displaying properly oriented mounts, penile insertion, and obvious pelvic thrusting but with no final, deep thrust. On some occasions, we noted that bulls would withdraw the penis while ejaculate was being expelled, indicating that they had ejaculated without displaying a final thrust. Therefore, previous attempts to quantify ejaculation frequency may have been inaccurate. To avoid this problem, we simply quantified mount interactions, mounts with intromission (i.e., copulation), mounts without intromission, and flehmen responses. We chose these behaviors because of their relevancy to both appetitive and consummatory responses (Beach, 1976; Pfaus, 1996) associated with male sexual motivation.

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 of the ground, culminating in physical contact with the female, regardless of orientation (e.g., bull mounts the female’s head, bull displays a properly oriented mount, bull mounts but then dismounts without copulation, etc.). 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 videotapes. Nevertheless, we assumed that intromission occurred on these occasions if the bull 1) exhibited a properly oriented mount, 2) displayed obvious pelvic thrusting, and 3) also displayed a final, deep pelvic thrust. 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 where we could verify that the bull displayed a properly oriented mount but failed to display intromission and pelvic thrusting. Because bull mounting activity can be altered in terms of both frequency and intensity, we calculated 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 test. If a bull did not display any mount interactions (or displayed only one) during a 60-min test, this was classified as a nonresponse and was not included in the analysis. To investigate the possibility that novel females induce a maintenance in the expression of appetitive behaviors, 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 (e.g., Senger, 1999).

Statistical Analyses

The numbers of mount interactions, mounts with intromission, mounts without intromission, mean mounting interval, and flehmen responses were subjected to statistical analyses. Data were analyzed by analysis of variance for repeated measures using the Proc Mixed procedure of SAS (Ver. 8.02; SAS Inst., Inc., Cary, NC). The model included effects of treatment, time (i.e., each of the four, 60-min tests nested within test day as repeated measures), test day and replicate, as well as the following interactions: treatment x time (i.e., differences among treatments across the four 60-min tests), replicate x time, treatment x replicate, and test day x time.

Animal within treatment was treated as a random subject effect, whereas replicate was used as a random group effect. Both of these 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 least squares means associated with significant (P < 0.05) effects in the models.

Orthogonal polynomial analysis was used to describe changes in bull sexual behaviors over the four 60-min tests. The previously noted dependent variables 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.

Chi-squared analyses were used to evaluate differences between treatments for proportions of bulls mounting and copulating over the four 60-min tests. We also calculated cumulative copulatory response curves and constructed 95% confidence intervals when bulls where in A-B-C-D, E-F-E-F, and G-G-G-G. Finally, we include individual cumulative copulatory response curves for representative bulls to provide examples of the variation in copulatory patterns that we observed. We removed one bull in Replicate 2 from all statistical analyses because he did not express a sexual interest in females.

	Results

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Mount Interactions

The ANOVA for mount interactions indicated that treatment, time, and the treatment x time interaction were significant (P < 0.01), whereas effects involving replicate were not. The treatment x time interaction for mount interactions is shown in Figure 2A. During the first 60-min tests, mount interactions were similar when bulls were in A-B-C-D, E-F-E-F, and G-G-G-G, but fewer (P < 0.05) mount interactions occurred when bulls were in the CON treatment. During the second 60-min tests, more (P < 0.05) mount interactions occurred when bulls were in A-B-C-D and E-F-E-F compared with when they were in either G-G-G-G or CON; more (P < 0.05) mount interactions occurred in G-G-G-G compared with when bulls were in CON. During the third 60-min tests, mount interactions did not differ when bulls were in A-B-C-D, E-F-E-F, or G-G-G-G; however, there were more (P < 0.05) mount interactions when bulls were in G-G-G-G compared with when they were in the CON treatment. Mount interactions were similar when bulls were in A-B-C-D, E-F-E-F, or CON during this time. During the fourth 60-min tests, more (P < 0.05) mount interactions occurred when bulls were in A-B-C-D compared with when they were in the other treatments, whereas mount interactions did not differ when bulls were in E-F-E-F, G-G-G-G or the CON treatment. When bulls were in A-B-C-D, mount interactions changed across time in a cubic fashion (P < 0.001), whereas they decreased in a linear manner (P < 0.05) when bulls were in E-F-E-F. Mount interactions decreased in a quadratic (P < 0.05) manner when bulls were in G-G-G-G. Mount interactions did not change across time when bulls were in the CON treatment.

View larger version (24K): [in this window] [in a new window]   Figure 2. Effects of variable female stimuli on the temporal expression of bull sexual responses. Graphs depict the treatment x time interactions for mount interactions (A; P < 0.05), mounts with intromission (B; P < 0.05), mounts without intromission (C; P = 0.25), and mounting interval (D; P < 0.05). Data presented are least squares means ± pooled SEM. Black bars = exposure to four estrual females in sequence (A-B-C-D); white bars = exposure to two estrual females in an alternated sequence (E-F-E-F); bars with diagonal lines = exposure repeatedly to one estrual female (G-G-G-G); and gray bars = exposure repeatedly to one diestrous female (CON). Bars with different letters within each graph differ at P < 0.05. Mount interactions, mounts with intromission, and mounting interval changed across time in a cubic manner in A-B-C-D, a linear manner in E-F-E-F, a quadratic manner in G-G-G-G, and did not change in CON. See text for actual P-values.

The ANOVA for mounts with intromission indicated that treatment, time, and the treatment x time interaction were all significant (P < 0.01), whereas effects involving replicate were not. The treatment x time interaction for mounts with intromission is shown in Figure 2B. Throughout the experiment, during all 60-min tests, there were no mounts with intromission expressed when bulls were in the CON treatment. During the first 60-min tests, mounts with intromission were similar when bulls were in A-B-C-D, E-F-E-F, or G-G-G-G. During the second 60-min tests, there were more (P < 0.05) mounts with intromission when bulls were in A-B-C-D or E-F-E-F compared with when they were in G-G-G-G or the CON treatment, which were similar. During the third 60-min tests, mounts with intromission were similar among treatments (i.e., not different from zero). During the fourth 60-min tests, more (P < 0.001) mounts with intromission occurred when bulls were in A-B-C-D compared with other treatments. Additionally, when bulls were in E-F-E-F they also exhibited more (P < 0.01) mounts with intromission compared with when they were in treatments G-G-G-G or CON, which did not differ. When bulls were in A-B-C-D, mounts with intromission changed across time in a cubic fashion (P < 0.01), decreased in a linear manner when bulls were in E-F-E-F (P < 0.05), and decreased in a quadratic manner (P < 0.03) when bulls were in G-G-G-G.

Mounts Without Intromission

The ANOVA for mounts without intromission indicated that time and treatment were significant (P < 0.01), whereas the treatment x time interaction, as well as effects involving replicate, were not significant. For the sake of completeness, we show the treatment x time interaction for mounts without intromission in Figure 2C. Overall, more (P < 0.01) mounts without intromission were expressed when bulls were in treatments AB-C-D, E-F-E-F, or G-G-G-G compared with when they were in the CON treatment. Additionally, mounts without intromission, overall, changed across time in a quadratic manner.

Mounting Interval

The ANOVA for mounting interval indicated that treatment, time, and the treatment x time interaction were significant (P < 0.05), whereas effects involving replicate were not. The treatment x time interaction associated with mounting interval is diagrammed in Figure 2D. During the first 60-min tests, mounting intervals were similar among A-B-C-D, E-F-E-F, and G-G-G-G, whereas they increased (P < 0.05) when bulls were in the CON treatment. During the second 60-min tests, mounting intervals were increased (P < 0.05) when bulls were in either G-G-G-G or the CON treatment compared with when they were in either A-B-C-D or E-F-E-F. During the third 60-min tests, mounting intervals did not differ when bulls were in A-B-C-D, E-F-E-F, or G-G-G-G, but they were increased (P < 0.05) when bulls were in CON. During the fourth 60-min tests, mounting intervals were decreased when bulls were in A-B-C-D compared with when they were in other treatments. In addition, mounting intervals were decreased (P < 0.05) when bulls were in the E-F-E-F treatment compared with when they were in the CON treatment; mounting intervals when bulls were in G-G-G-G were intermediate of E-F-E-F and CON during the fourth 60-min tests. When bulls were in A-B-C-D, mounting intervals changed across time in a cubic (P < 0.01) manner, increased in a linear manner when bulls were in E-F-E-F (P < 0.05), and increased in a quadratic manner (P < 0.01) when bulls were in the G-G-G-G treatment. Mounting intervals did not change across time when bulls were in the CON treatment.

Flehmen Responses

The ANOVA for expression of flehmen responses revealed significant (P < 0.05) effects of time and treatment (Figure 3A), whereas the treatment x time interaction (Figure 3B) and effects involving replicate were not significant. Overall, more flehmen responses were exhibited when bulls were in A-B-C-D compared with when bulls were in other treatments, but flehmen responses did not differ when bulls were in E-F-E-F, G-G-G-G, or the CON treatment. Additionally, flehmen responses, overall, decreased in a quadratic manner (P < 0.05) over the four 60-min behavior tests.

View larger version (22K): [in this window] [in a new window]   Figure 3. Effects of variable female stimuli on the expression of bull flehmen responses. A) Overall treatment effect (P < 0.05) associated with bulls’ expression of flehmen responses. Bars with different letters differ at P < 0.05. B) Treatment x time interaction (P = 0.26) associated with bulls’ expression of flehmen responses during four 60-min behavior tests. Black bars = exposure to four estrual females in sequence (A-B-C-D); white bars = exposure to two estrual females in an alternated sequence (E-F-E-F); bars with diagonal lines = exposure repeatedly to one estrual female (G-G-G-G); and gray bars = exposure repeatedly to one diestrous female (CON). Data presented are least squares means ± pooled SEM.

Based on ² analyses (data not shown), there were no differences among the treatments with respect to the proportion of bulls displaying mount interactions during the 60-min tests (Figure 4A), with the exception that during the fourth 60-min tests a lower proportion of bulls mounted when they were in the CON treatment compared with when they were in the A-B-C-D treatment. Furthermore, the proportion of bulls displaying mount interactions decreased in a linear manner (P < 0.05) for the CON treatment. The proportion of bulls displaying mount interactions in each of the other treatments did not change over time.

View larger version (35K): [in this window] [in a new window]   Figure 4. Effects of variable female stimuli on the percentage of bulls displaying mount interactions and the percentage of bulls copulating. Treatment x time interaction (P < 0.05) associated with the percentage of bulls displaying mount interactions (A) and copulating (B) during four 60-min behavior tests. Black bars = exposure to four estrual females in sequence (A-B-C-D); white bars = exposure to two estrual females in an alternated sequence (E-F-E-F); bars with diagonal lines = exposure repeatedly to one estrual female (G-G-G-G); and gray bars = exposure repeatedly to one diestrous female (CON). Data presented are least squares means ± pooled SEM. Bars with different letters differ at P < 0.05.

	Discussion

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By repeatedly pairing mature, sexually experienced beef bulls with individual, unrestrained females of varying novelty and receptivity, we were able to characterize temporal changes in sexual behavior of bulls. As expected, novel and sexually receptive females elicited the greatest amount of sexual activity in bulls; continually pairing bulls with novel females also induced the most flehmen responses. Interestingly, even though bulls were usually stimulated by novel females to maintain sexual responsiveness, almost all bulls showed a decrease in copulation after 2 h of mating. Below, we discuss our findings in relation to the specific temporal changes in bull sexual responses in association with the various female stimuli and elaborate on the variable patterns of copulation in bulls we noted. Finally, we discuss how our approach differs from that of the traditional serving capacity tests.

Bulls repeatedly exposed to a diestrous female were never allowed to exhibit mounts with intromission and this was a useful negative control in that regard. We found, as Price (1987) wrote, that diestrous females display aversive behaviors upon attempted copulation by bulls, which precludes male consummatory behaviors. Generally, bulls were motivated to attempt copulation of the diestrous females, as the average number of mount interactions did not change over time; however, even though the proportion of bulls attempting copulation of diestrous females was initially similar to the other treatments, it steadily decreased thereafter. In part, these observations disagree with the notion that bulls do not attempt mounting of nonestrual females and only "sniff their vulvae" (Sambraus, 1971, cited and translated by Blockey, 1976b) to determine receptivity. Bulls test female receptivity by attempting copulation, as suggested by Chenoweth (1981, 1983); however, we found that bull mounting behavior, when repeatedly paired with a diestrous female, changed dramatically with respect to the frequency and intensity with which bulls attempted copulation. Hence, our observations cast some doubt on the notion that the single greatest stimulus that induces mounting behavior in bulls is an "immobile, U-shaped object" (Chenoweth, 1979, 1983). This is suggested because, even though bulls did not mount diestrous females as frequently or as intensely as estrual ones, and over time, fewer and fewer bulls attempted copulation of diestrous females, bull mounting behavior was induced nonetheless. Our observations provide the first detailed descriptions of mounting behavior when bulls are individually paired with unrestrained, sexually nonreceptive females.

In general, the pairing of bulls with novel, estrual females resulted in maintenance of sexual responsiveness, with the exception of the third 60-min behavior tests. Although the vast majority of bulls displayed mounting behavior with novel, estrual females, a smaller proportion of bulls usually were allowed to copulate. This indicates that some estrual females, despite their willingness to stand firm for homosexual mounting, do not allow copulation. This supports the work of Katz and Price (1986), who also observed variation in sexual receptivity of estrual females. Nevertheless, the sexual responsiveness of bulls toward novel females seems appreciable based on our findings.

In a recent review, from the field of behavioral ecology, Wedell et al. (2002) provided compelling evidence that males have evolved mechanisms for allocating sperm in strategic ways that optimize reproductive fitness. Wedell et al. (2002) indicated that preferential sperm investment in novel females could be a mating strategy that has evolved to allow a male to decrease the number of sperm that he invests in each particular female, which is in agreement with Dewsbury (1981). Variable sexual responsiveness and postcopulatory refractoriness in familiar females may induce bulls to solicit copulations from novel females, which would allow bulls to distribute sperm more evenly and adaptively among numerous mates. Interestingly, this would also allow females to solicit copulations from other bulls, which is a hypothesis that has yet to be fully tested. One interesting consequence of a polygynous mating system, such as that in cattle, is that not all females have the same opportunity for maximal sperm allocation from bulls. As Pizzari (2002) pointed out, it is important to remember that successive copulations with a particular male results in diminishing numbers of spermatozoa for any particular female thereafter. Hence, females also may have evolved alternative patterns of mating that include obtaining a few copulations from multiple partners (Wedell et al., 2002).

Although Blockey (1976b, 1978b, 1981) suggested that bulls distribute copulations equally among all receptive females, it is important to point out that it is not clear what this behavioral pattern implies in terms of the costs associated with optimal sperm allocation. For bulls to allocate sperm optimally and dynamically among all estrual females available, a particular bull must limit the number of copulations per female and/or selectively modify the volume of ejaculate expelled therein. These considerations have been consistently ignored in the traditional serving capacity tests. In fact, the notion that bulls likely limit the number of copulations per female to optimize reproductive fitness is the antithesis of presently accepted notions regarding sexual performance of bulls. Future research in this area will be necessary to evaluate changes in copulatory patterns among bulls and how ejaculate properties change dynamically within the natural mating herd. Through such research, we may be able to further understand how changes in bull sexual behavior and fertility are either correlated to, or directly influenced by, female sexual receptivity and/or fecundity.

In the present study, there was a steady decrease in the proportion of bulls that were allowed to express mounts with intromission with familiar, estrual females. Interestingly, the proportion of bulls attempting copulation remained relatively stable during such pairings. This observation further supports the notion that unrestrained estrual females allow a series of copulations and then cease responding (at least to a familiar bull). On the other hand, we found examples where familiar females allowed as many as 30 copulations over the four 60-min tests with a familiar bull (see Figure 5B, bull No. K075, treatment G-G-G-G). Therefore, it is apparent that there is variability in the overall amount and intensity of copulation that sexually receptive females allow. Price (1987), citing unpublished data, suggested that unrestrained, estrual females completely cease allowing intromission after four to eight copulations. Katz and Price (1986), however, found that unrestrained, estrual females will exhibit highly variable postcopulatory refractory periods. Blockey (1976b) reported that some estrual females will allow as many as 10 copulations from the same bull, whereas others allow only one. Presently, there is an unmet need to characterize the incidence and underlying physiological mechanisms associated with variation in female sexual receptivity and the various afferent and efferent factors mediating complete sexual satiety in the bovine female.

View larger version (23K): [in this window] [in a new window]   Figure 5. Cumulative response curves when bulls were exposed to variable female stimuli (A) and variation in copulatory responses of individual bulls (B). For panel A, data presented are mean copulatory responses ± 95% confidence intervals. Treatments were: exposure to four estrual females in sequence (A-B-C-D); exposure to two estrual females in a repeated sequence (E-F-E-F); and exposure repeatedly to one estrual female (G-G-G-G).

We hypothesized that estrual females might recover from sexual satiety and allow further copulations if we regulated the duration of exposure to bulls. This was the major factor underlying our inclusion of the E-FE-F treatment in this experiment. Females that had already allowed copulation during the second 60-min tests allowed further copulations during the fourth 60-min test. They allowed more copulations at this time than females allowed in the G-G-G-G treatment after an equivalent amount of time. Although this effect seemed appreciable in the E-F-E-F females during the last test, other rested, familiar females (i.e., those in the third 60-min tests) received much less copulation. Whereas it is true that copulatory responses were not as prominent during the third 60-min test in this regard, this was due to attenuation of sexual responsiveness in the bulls and not to female sexual aversion per se. This is suggested because when bulls had access to a novel, estrual female during the third 60-min test, reduced sexual responsiveness also was evident.

Our data do not entirely support the work of Chenoweth (1983), Price (1987), and Blockey (1976b), who all implied that estrual females will cease displaying sexual receptivity following several copulations. In our study, the data show that female sexual receptivity becomes thoroughly diminished if the female receives an intense series of copulations with a particular bull. However, it may become partially restored if the female receives (or achieves) a period of postcopulatory recovery. Researchers studying the sexual behavior of golden hamsters have demonstrated that sexually sated females display renewed sexual receptivity when paired with a novel male that has not been copulating (Lisk and Baron, 1982). Hence, the Coolidge Effect may not be a sexually dimorphic phenomenon in the bovine. We do not know whether bovine females show a preference for breeding multiple times with one bull or a few times with multiple bulls.

Although the Coolidge Effect has not been extensively studied in bulls, and the origin of the term is anecdotal, Dewsbury (1981) critically defined the Coolidge Effect as a progressive decrease in the propensity of a male to mate with a particular female over successive inseminations, combined with a renewed sexual interest with a novel female. As we wrote above, bull sexual responsiveness decreased substantially after 2 h, even when bulls were presented with a novel, estrual female. In fact, bull sexual responsiveness during this time was comparable to when bulls were paired with a nonreceptive female. Furthermore, only 4 of the 11 bulls achieved copulation during these tests. This was a surprising observation, given the fact that most researchers have implied that bulls are continuously motivated to copulate with novel, estrual females (Almquist and Hale, 1956; Hale and Almquist, 1960; Blockey, 1976b). One article that included a description of the Coolidge Effect in bulls (Almquist and Hale, 1956) has been cited frequently (Dewsbury, 1981). Almquist and Hale (1956) allowed three bulls to copulate to satiety with a single stimulus animal and then exposed the bulls to one or two novel females in succession. Cumulative ejaculation curves for these three bulls showed that in the constant presence of a stimulus female, there was a gradual decrease in the number of ejaculations per unit of time until, eventually, they ceased displaying sexual behavior (Almquist and Hale, 1956). Substantial increments in ejaculations were observed in all three bulls upon presentation of a novel female (Almquist and Hale, 1956). In a subsequent study, Hale and Almquist (1960), used four 60-min behavior tests, and found that the number of ejaculations showed little diminution with successive, novel females.

It is not clear why our results differ from those of Hale and Almquist (1960); however, Dewsbury (1981) noted that the experiments of Hale and Almquist (1960) lacked appropriate controls, had no statistical analyses, and employed few experimental units with no replication. In addition, differences between the two studies could be related to differences in sexual behavior that may be genetic (e.g., beef bulls compared with dairy bulls, Bos indicus compared with Bos taurus, etc.), environmental (e.g., seasonal effects, permanent or temporary housing conditions, presence of investigators), or due to differences in interpretation of sexual behaviors. Nevertheless, the fact that a large proportion of bulls in our study ceased copulating after 2 h, despite access to a novel female, indicates that the so-called Coolidge Effect should be reevaluated in bulls.

The decrease in bull sexual responsiveness to novel females was most likely related to general, physical fatigue and/or other physiological changes that rendered bulls incapable of further copulation or decreased their motivation to copulate. As in our experiment, Katz and Price (1986) observed that with each successive series of copulations, bulls display longer mounting intervals and, eventually, sexual satiety between series of ejaculations. However, it was not clear in these studies under what conditions bulls recover from sexual satiety. The vast majority of bulls in our experiment resumed both intense mounting and copulation in the subsequent 60-min test, indicating that bull sexual behavior became fully reinstated, especially when a novel, estrual female was available. Although bulls’ sexual responses to novel females seemed appreciable in the experiments by Almquist and Hale (1956) and Hale and Almquist (1960), our present experiment is the first to incorporate proper controls and statistical analyses using specified stimulus conditions with both novel or familiar unrestrained females of varying receptivity. We found that, under these conditions, bull sexual behavior oscillates between periods of activation and satiety and that novelty of the female may prolong the duration of sexual responsiveness, but it did not completely eliminate impending sexual satiety. Novel females, however, have a demonstrable effect in inducing renewed copulation after this period of transient sexual satiety, an observation that has not been previously documented.

In our experiment, we documented various patterns of bull copulatory responses. Overall, the mean cumulative response curves (Figure 5A) show a stimulatory effect of exposing bulls to novel females, whereas when bulls were exposed repeatedly to the same estrual female, an initial stimulatory response was followed by a decrease in response. Although these cumulative response curves are important for ascertaining the general effects of female stimuli on copulatory responses of bulls, it is also important to note that we found individual variation in mating patterns that may constitute new selection criteria for breeding bulls. We found, for example, that some bulls did indeed copulate equally with each novel, estrual female presented; however, Blockey (1976a,b) assumed that this is the only pattern of copulation expressed by bulls. Contrary to the assumptions of Blockey (1976a,b), we found that some bulls failed to respond to all estrual females or that some bulls copulated with all females but at a lower frequency.

The fact that nonreceptive females do not allow intromission behavior, and unrestrained estrual females show a strong and seemingly irreversible aversion to continual copulation by a particular bull, provides justification for using restrained females in serving capacity tests (Blockey, 1976a; Chenoweth et al., 1979; Bertram et al., 2002). This approach is based on the assumption that removing variability in responsiveness associated with female sexual receptivity will allow bulls to display their "innate" sexual behavior (Blockey, 1976a; Price, 1979). We agree that this practice completely eliminates the female’s influence on bull sexual responsiveness; however, it is not useful in understanding bull sexual behavior in the context of natural mating. Natural mating stimuli include variable female sexual receptivity and oscillating patterns of sexual responsiveness, including postcopulatory inhibition and complete sexual satiety, followed, perhaps, by recovery (Beach, 1976; Pfaus, 1996).

The disparity between stimulus conditions during serving capacity tests and those during natural mating may be a mitigating factor involved with the seemingly contradictory findings in previous research in this area. For example, some researchers have indicated that serving capacity tests are poor indicators of herd fertility (Smith et al., 1981; Christensen et al., 1982; Bertram et al., 2002) and may only be useful in determining whether a particular bull can copulate. Still others have reported that there are strong, positive correlations between bull sexual responsiveness toward restrained females and overall herd pregnancy rates (Crichton and Lishman, 1988; Blockey, 1978, 1989).

	Implications

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
Our results support the hypothesis that heterosexual mating in the bovine involves oscillating behaviors that depend on the degree to which each partner is novel and motivated to copulate. Female novelty and receptivity affect the expression of bull sexual behavior, and there are temporally relevant factors associated with bull sexual satiety that are not well defined at present. Any attempt to assess breeding potential of bulls should take into account these variables.

	Footnotes

 
¹ Published with the approval of the Director of the Kentucky Agric. Exp. Stn. as Publication No. 04-07-185.

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 Neurobiol., Univ. of Kentucky Coll. of Med., Chandler Medical 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 September 24, 2004. Accepted for publication December 10, 2004.

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Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 


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