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a Department of Animal Sciences, Rutgers, the State University of New Jersey, New Brunswick, New Jersey 08901-8525
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ABSTRACT |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Examples of cue transmission in domestic species include the phenomenon known as the "ram effect" in sheep [3, 4] and the observed quantitative increase in sexual performance by male goats, cattle, horses, and pigs after viewing copulating conspecifics (for a review, see [5]). Whereas male domestic sheep (Ovis aries) do not show enhanced sexual performance after viewing a copulating pair [5], Maina and Katz [6] reported that rams displayed improved sexual performance after brief contact with a male pen mate that had recently mated an estrous ewe. The differing sexual performance responses to visual cues were explained in terms of the differences in mating strategies between male sheep and males of other domestic species. It was hypothesized that olfactory cues were present on the wool of the recently mated male pen mates. These stimulating cues were then transmitted as the rams interacted with one another prior to a sexual performance test.
The present experiment was designed to identify which social or sexual situations provide the olfactory cues that enhance ram sexual performance. The transmission and the source of the olfactory cues may be similar to those for wild sheep species, thus providing a model for male-male interactions and sexual stimulation in ovids.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Eight sexually experienced Dorset rams (O. aries) approximately 18 mo of age were obtained from Rutgers University farm stock. Animals were housed and fed in compliance with the Consortium Guide for the Care and Use of Agricultural Animals, and all work with animals was approved by the Rutgers University Institutional Review Board for the Use and Care of Animals. All rams had previously demonstrated the full range of sexual behaviors and were involved in weekly sexual performance tests 5 mo prior to the present experiment. Six intact Dorset ewes approximately 1–2 yr of age were used. The ewes had been mated on several occasions prior to the experiment. Ewes were induced to show estrus by an i.m. injection of prostaglandin F2
and insertion of progesterone-releasing intravaginal devices (CIDR; Inter-Ag, Hamilton, New Zealand) 6 days before the test. The devices were removed after 4 days; 24 h later, ewes received 200-µg i.m. injections of estradiol-17ß (Steraloids, Wilton, NH). Sexual performance tests were conducted 24 h after the estradiol-17ß injections. Non-estrous ewes received no hormone treatments. Estrous state of all ewes was checked before the start of each test.
Experimental Procedures
The tests were conducted between 0900 and 1130 h, once each week for a period of 5 wk. On experiment days, rams (n = 8) were separated into two test groups (n = 3 in each group) in adjacent home pens for the duration of the testing day. The remaining rams (n = 2) were designated as the stimulus rams, and one was assigned to each test group. These stimulus rams were placed in a small test pen (2 m x 2 m) in one of five conditions for 10 min. Then the test rams in each group were exposed to their respective stimulus ram in separate home pens for 5 min. The five conditions consisted of placing the stimulus ram with another ram (R); with a non-estrous ewe (N); with an estrous ewe fitted with a cloth perineal patch (P) to block intromission; with an estrous ewe (E); and alone (A). Males in each group were exposed to one of the five conditions on each of the five test days. The test groups were exposed to the conditions in the order ARNPE and EPNRA, so that a different condition was experienced by each group each test day. The two stimulus rams were assigned to the same test group for the duration of the experiment and were not tested for sexual performance. However, it was confirmed that the stimulus rams mated estrous ewes during the 10-min exposure.
Behavioral Observations
While the test rams were exposed to their respective stimulus rams (preperformance period), the frequencies of anogenital sniffs (Sniffs), in which a test ram sniffed the stimulus ram's perineal area, and leg kicks (Kicks) in which test rams raised their forelegs in an upward and outward motion while in close proximity to the stimulus ram, were recorded. Also, the observers recorded flehmen lip curls (Lip Curls), in which test rams curled their upper lips and raised their head; mount attempts (Mount Attempts) in which both forelegs of the test ram were raised off the ground but not placed securely on the stimulus ram; and mounts (Mounts) in which rams secured both forelegs on the rump of the stimulus ram. Mounts may or may not have included pelvic thrusting movements. After the 5-min preperformance periods were over, each test ram was allowed to interact with an estrous ewe in a small test pen for 20 min (sexual performance test). During the sexual performance test, the frequencies of Sniffs, Kicks, Lip Curls, Mount Attempts, Mounts, and ejaculations (Ejaculations) were recorded. Ejaculations were recorded when observers saw either a more vigorous thrust and arching of the back when the ram was thrusting, or when seminal fluid was seen on the ewe's vulva and the ram's prepuce. The latencies to mount (Latency Mount) and ejaculate (Latency Ejaculate), which were the time in seconds from the start of the test to the expression of the respective behaviors, as well as the post- and interejaculatory intervals (PEI and IEI), were recorded. The PEI was recorded as the interval between the completion of an ejaculation and the next Mount Attempts or Mounts, and the interval between ejaculations was recorded as the IEI. After the sexual performance test, each test ram was placed in an outside pasture, away from the rams that had not yet been tested. Mating efficiency scores were calculated as the number of Ejaculations divided by the sum of Mount Attempts and Mounts for each ram in each condition, i.e., mating efficiency = Ejaculations/Mount Attempts+Mounts.
Data Analysis
The frequencies of behaviors directed toward the stimulus ram during the preperformance period were examined using ANOVA procedures with ram and treatment as main effects [7]. Mean comparisons were tested for significance using Duncan's multiple range test. Sexual performance data were analyzed using ANOVA for repeated measures, with ram and treatment as the repeat variables. Data were normally distributed, and significance levels were designated at p < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Preperformance period The mean frequencies of Sniffs and Lip Curls directed toward the stimulus ram were different among the conditions (ANOVA: F4,25 = 12.54, p = 0.01 and F4,25 = 11.0, p = 0.02, respectively). Rams performed more Sniffs and Lip Curls when the stimulus ram had been paired with a ewe (N, P, and E conditions) in comparison to the A condition; however, the Sniffs frequencies did not differ between the N and R conditions (Table 1). There were no significant differences due to stimulus condition for Kicks, Mount Attempts, or Mounts during the 5-min preperformance period with the stimulus ram (Table 1). In addition, rams exhibited nonsexual behaviors toward the stimulus ram, such as body sniffs. These behaviors occurred more frequently when the stimulus ram had been paired with an estrous ewe versus having been alone or with another ram (D. Maina, unpublished results). The test rams approached the stimulus ram immediately upon introduction, and the majority of the behavioral activity occurred within the first 2 min (D. Maina, unpublished results).
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Sexual performance tests Rams displayed no differences (p > 0.05) in the total frequencies of Sniffs, Kicks, and Mount Attempts among the five testing conditions. Mean Lip Curls expression was highest in the R condition and lowest in the A condition (3.3 ± 1.4 and 0.2 ± 0.1, respectively; repeated measures ANOVA: F4,25 = 7.02, p = 0.04). The mean frequency of Mounts was highest in the A condition and lowest in the P condition. Ejaculation frequency was highest in the E condition and lowest in the A and R conditions (Table 2). Mating efficiency scores were highest in the conditions in which the stimulus ram had been paired with a ewe (N, P, and E) and significantly lower in the A condition (Fig. 1). The ratio of Sniffs to Lip Curls was highest in the A condition; however, few Lip Curls were expressed by rams in that condition. Rams in the N condition had higher Sniffs:Lip Curls ratios in comparison to the R, P, and E conditions (Table 2).
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Behavioral Latencies
The mean Latency Mount in the five conditions did not differ. Although not significant, the mean Latency Ejaculate tended to be longer when the stimulus ram had been placed alone in the pen (repeated measures ANOVA: F4,24 = 2.88, p = 0.06) (Table 3). The range of Latency Ejaculate in the A and E conditions was from 1 to 1002 and from 13 to 85 sec, respectively. The mean PEI in the A condition were longer relative to those in all other conditions; however, the differences were significant only in the N (repeated measures ANOVA: F4,22 = 14.9, p = 0.02) and E (repeated measures ANOVA: F4,22 = 10.5, p = 0.03) conditions. Rams in the conditions involving a ewe had significantly shorter IEI relative to values for the A (repeated measures ANOVA: F4,21 = 21.3, p = 0.006; F4,21 = 13.4, p = 0.01; and F4,21 = 16.6, p = 0.01; for N, P, and E conditions, respectively), but not the R condition (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The effect of social cue transmission on ram sexual performance in this experiment was essentially limited to consummatory behavior expression and sexual motivation. The variability in courtship behavior expression accounted for the ineffectiveness of the experimental condition in affecting the courtship behavior frequencies (Table 1). Human assistance in breeding may have resulted in considerable variation in the quantitative aspects of sexual behavior in male farm species [8]. For example, certain rams performed many Kicks or Lip Curls, whereas others performed relatively few or none. This was also the case with respect to Mount Attempts. Certain rams were more adept, or perhaps motivated to perform proper mounts, with fewer mount attempts, whereas others required more attempts.
With respect to consummatory behaviors, only rams in the E condition performed more ejaculations relative to the A and R conditions. Rams in the N and P conditions had intermediate values (Table 2). However, in terms of mating efficiency, rams in the N, P, and E conditions had greater mating efficiency scores relative to rams in the A condition; that is, they ejaculated with fewer Mounts and Mount Attempts as compared to rams in the A condition (Fig. 1). All rams ejaculated at least twice in the N, P, and E conditions. The fact that some rams tested in the A and R condition did not achieve ejaculation or achieved only a single ejaculation during the 20-min test underscores the performance-enhancing effect of exposure to the cues carried by the stimulus ram exposed to ewes.
Rams had similar sexual performances for the first mating bout (Table 3). However, after the first ejaculation, treatment differences were evident in the ability or motivation to begin mounting again and subsequently ejaculate. Rams exposed to the N and E conditions had significantly shorter PEI values with respect to the other conditions. It was expected that the PEI values in the P condition would be similar to those in the N and E conditions, since the ewe was in estrus and the ram could display all sexual behaviors except intromission and ejaculation. Perhaps the cloth patch covering the genitalia blocked excitatory olfactory cues.
The PEI and IEI values were shorter when test rams were exposed to a stimulus ram that had been paired with a ewe, regardless of her estrous state. However, there was a tendency for the excitatory values of the stimulus ram to increase in the order E > P > N > R > A. Cues from the stimulus ram could have been associated with mating (E vs. P), estrous state (E or P vs. N), or sex (N, P, or E vs. R). The differences between cues from stimulus rams exposed to another ram in contrast to being held alone could be associated with either stress of being alone or the excitement of interacting with another ram (agonistic behavior).
The scent of a non-estrous ewe was stimulating to rams. O. aries rams can determine the estrous state of ewes upon olfactory investigation [9]; however, the mechanism by which they use the information is not understood. Perhaps O. aries and O. canadensis rams routinely investigate the changing estrous state of ewes with Sniffs and the resulting Lip Curls. During the rutting (O. canadensis) season, ewes that are in the vicinity may not be in estrus upon joining with rams but will enter estrus within a few days [1]. Therefore, social cues from a ewe, transmitted by the stimulus ram, may be sufficient to stimulate rams and enhance their sexual performance.
Sexually stimulating cues would most likely be some combination of environmental cues, such as those obtained by visual, auditory, tactile, and olfactory stimulation. Visual stimulation (i.e., watching a copulating pair) was found to enhance sexual performance in male cattle [10], goats [11], horses [12], and pigs [13], but not male sheep [5]. The difference in estrous female behavior between sheep and other domestic ruminant species could explain the ineffectiveness of visual stimulation on ram sexual performance. Estrous ewes do not form sexually active groups in which female-female mounting occurs, thus not providing rams the visual cues that normally stimulate male goats and cattle. Ewes will seek out rams for mating [14–20] and express proceptive behavior. In view of this, those rams receiving cues directly from a ewe should demonstrate enhanced sexual performance. However, Price and colleagues [21] reported that ram sexual performance was not enhanced by direct stimulation from estrous ewes. The fact that rams did not benefit from direct sexual stimulation was surprising, since rams had the opportunity to receive most of the important cues upon investigation of a restrained estrous ewe. The difference between the experiments by Price and others and the present experiment was the context in which these cues were obtained. In this experiment, rams received the cues from their male pen mates, not from direct investigation of estrous ewes.
Upon investigation of the stimulus males, rams expressed greater Sniffs frequencies toward the stimulus ram and subsequently had greater Sniffs:Lip Curls ratios when exposed to a stimulus ram that had interacted with a ewe. Lip Curls were not expressed upon exposure to a stimulus ram in the A condition. The lack of novel olfactory cues present on the stimulus male may explain this result. In conditions in which the stimulus ram had been placed with another sheep (male or female), the rams performed Lip Curls upon olfactory investigation of the stimulus ram. In addition, the stimulus rams received more Sniffs accompanied by Lip Curls if they had been paired with a ewe, regardless of estrous state.
The question then arises as to the mechanism of cue transmission. Tillbrook and colleagues [22–24] reported that the wool is a vehicle for pheromonal transmission in domestic sheep. Certain breeds of O. aries rams preferred (courted and copulated with increased frequency) unshorn ewes relative to shorn ewes. In addition, data from experiments with O. aries rams [22–26] suggest that olfactory cues can be retained in wool. Then the cues in a ram's wool are transferred to the other rams as they sniff his body, including the anogenital region. Subordinate O. canadensis rams interact with each other and with dominant rams [5] and could obtain mating-related olfactory cues via transmission from other rams that have come in contact with estrous ewes. This would signal the existence of mating opportunities. To take advantage of these opportunities, subordinate rams would have to use mating strategies that allow them to copulate quickly. The need to copulate quickly is essential, since dominant rams "protect" their estrous ewes by reacting aggressively toward any other male in the vicinity of these ewes [5]. Alternative strategies used by subordinate rams such as coursing, or blocking, in which subordinate rams move ewes away from a traditional breeding area, allow rams to create brief "windows of opportunity." Rams that used the blocking strategy directed their attention to ewes that were either non-estrous or were near-estrous; however, the rams preferred near-estrous ewes [6] and remained with the ewes for copulation at estrus. The success rate of these blocking males varied over the years of the study; however, in the least successful year, 18% of estrous ewe observations included interaction with rams using the blocking strategy [6].
In domestic and wild rams, studies on intermale activity and its effects on sexual performance have largely been restricted to the domain of social hierarchy effects, namely the suppression of subordinate rams' sexual performance (for review, see [5, 8]). In light of the data presented here, it is conceivable that male-male competition for females allows for the acquisition of sexually stimulating cues, either by tactile and olfactory interaction with males or by viewing of combating males. Other behavioral or environmental cues that were not measured should not be dismissed, although the results from this and previous experiments suggest that wool-borne olfactory cues from females are most likely the source of the stimulation that enhanced ram sexual performance.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Correspondence: L.S. Katz, Rutgers, the State University of New Jersey, 84 Lipman Drive, New Brunswick, NJ 08901-8525. FAX: 732 932 6996; katz{at}aesop.rutgers.edu
Accepted: January 19, 1999.
Received: October 27, 1998.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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  D. B. Imwalle, A. R. Lehrer, and L. S. Katz Intravaginal impedance and sexual behavior of ovariectomized goats given estrogen alone or in combination with progesterone J Anim Sci, August 1, 2007; 85(8): 1908 - 1913. [Abstract] [Full Text] [PDF]
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