Bull Sex Drive and Reproductive Behavior

Introduction

Although they are not generally considered to be seasonal breeders, cattle are subject to seasonal influences upon reproduction [1] which may be associated with ambient temperature, feed availability and parasite loads. Evolutionary adaptation to regional environments often resulted in a consistent pattern of a predominantly Spring calving pattern, with mating occurring in the early summer [2]. Prehistoric cattle are assumed to have formed relatively small matriarchal groups on local range, which bulls inhabited during the period of breeding opportunity. Here, dominant males derived pre-eminent access to receptive females. Cattle are polygynous; a system which allows individual males to mate with multiple females [3]. In general, beef cattle systems throughout the world are still heavily reliant upon natural breeding [4,5]. Modern production systems, whether employing natural or artificial breeding, have challenged many evolutionary adaptations, by altering environments, changing social groupings, and by reducing both breeding "season" length and male to female ratios. This places greater emphasis on those factors important for male reproductive success, including male sex-drive, or libido [6].

Definitions

Sexual behavior in the bull includes the detection, courtship and service of estrous females. Libido, or sex drive, has been defined as the "willingness and eagerness" of a bull to attempt mount and service of a female [7], whereas mating ability describes his physical ability to complete service. Serving capacity is a measure of the number of services achieved by a bull under stipulated conditions [8] and thus includes aspects of both libido and mating ability. Reaction time is that time which elapses between male cognition of an appropriate stimulus and the completion of service [7].

Cattle Reproductive Behavior

At pasture or range, bulls are initially attracted towards females by the sight of mounting activity. The major incentive to attempt mount or service is an immobile female or similar inverted U structure. Where this exists, the bull will often attempt service regardless of the estrous status of the female; in fact, steers are successfully employed as mount animals in semen collection centers. Pheromones also play a role in allowing bulls to detect receptive females, although this mechanism evidently requires close physical contact for activation in cattle [9]. The major special sense used by bulls to detect estrous females is vision [10,11]. The task of identifying estrous females is facilitated by the tendency of females in both late pro-estrus and estrus to form a mobile sexually-active group (SAG) which usually stays within visual contact of the bull or bull group [7,12]. Females in heat generally become more active and vocal than at other phases of the estrus cycle. Bulls tend to be most attracted to females newly in estrus and provision of a fresh stimulus female can restore libido in satiated males [13,14]. Bulls test the receptivity of females by making real or sham mounting attempts, by chin resting and by licking and sniffing around the perineal region. The last actions are often closely followed by a characteristic curling of the upper lip, termed flehmen. This action is most probably associated with fluid transfer to the vomeronasal organ where it is assessed for pheromonal activity [9]. Females can exert considerable control over mating by determining the timing of sexual access, and discriminating between competing males. Bulls form hierarchal groups, with social status influencing reproductive success [7,14]. Prestimulation of males increases their sexual response [15]. Bulls possess a fibro-elastic penis and copulation generally occurs rapidly (1-2 seconds) once intromission is achieved [16]. Bulls are capable of short bursts of great reproductive activity, dependent upon their inherent sex drive and stimulus pressure. Breeding trials with both natural and induced-estrus females indicate that it is not uncommon for bulls to serve multiple times (20 - 30 plus) within a 24 hour period.

Biostimulation

Male animals are capable of triggering neuroendocrine reflexes which alter ovarian function in conspecific females [17]. Where stimulatory, such effects have been collectively termed biostimulation [18]. In various species, biostimulation has been shown to advance onset of puberty, initiate estrus postpartum and alter temporal relationships associated with estrus and ovulation. In cattle, biostimulatory effects do occur, although they are less dramatic compared with sheep and swine. There are indications that biostimulation is advantageous in reducing postpartum interval in cows, although nutritional interactions occur [19]. Androgenized females can be as effective as biostimulators as can bulls. Less evidence is available in support of positive biostimulatory effects on the advancement of puberty in heifers where the appropriate nutritional and social interactions remain to be adequately defined [19,20].

Tests for Bull Sex Drive

Libido, or sex-drive, is a measurable behavioral trait. Testing procedures for bulls generally rely on the exploitation of several or more of the following findings:

1. Libido in bulls has a large genetic component [21-26].
2. Bulls are polygamous and tend to distribute their services among receptive females [8].
3. The greatest single stimulus for a bull to attempt mount and service is the immobile rear end of a female, or something he perceives as similar [27-29].
4. Prestimulation of bulls increases their sexual response [15,28]
5. Competition among bulls can increase their sexual response [4,30].

Many attempts have been made to assess sex-drive in bulls and other male livestock [31]. As simple observation of male sexual activity in the breeding pasture has generally yielded disappointing quantitative results, a number of researchers have devised formalized, pen-type testing regimes. Early studies on bull sexual behavior sought to counter difficulties in maintaining sex drive in dairy bulls in AI centers [32], and subsequently, to determine the role of sexual behavior in optimizing sperm harvests [13,33]. In Sweden, a "libido index" used to assess both libido and mating ability in A.I. sires [22] was subsequently modified ("libido score") for assessing range-type beef bulls [7,34]. A "serving capacity" test was developed in which bulls are group-tested with restrained, non-estrus females at BFRs of either 5:2 or 5:3 for 40 to 60 minutes [8] and scored on the basis of services performed during the observation period. Comparison of reaction time, serving capacity and libido scores in young Bos taurus bulls [27] indicated the following; 1) that libido score was most repeatable, restrained females were equally attractive to bulls whether they were in induced estrus or not, and a 10 minute test provided as much comparative information on bull sex drive as did a 30 minute test. The use of estrous females was shown to be unnecessary for the assessment of sex drive in Bos indicus bulls also, providing females are adequately restrained [35], although one study showed that estrous status (as well as cow identity) influenced service rates in Santa Gertrudis bulls [36]. Testing procedures for bulls have been developed which exploit elements of both the libido and serving capacity score systems [31,37-39].

Test Predictability and Repeatability

The ideal sex drive assessment for bulls should be simple, quick, highly repeatable, predictive of reproductive performance and esthetically acceptable. At present, no single current procedure fulfils all of these criteria. However, it is possible to reliably estimate relative differences in sex drive between bulls [14]. For example, moderate phenotypic correlations (r = 0.67 and 0.60 respectively) were obtained between libido and serving capacity scores in yearling bulls tested on different days [27], although reaction times to service in the different tests were not significantly correlated. Lack of predictability for reaction time was confirmed in a subsequent study with young Hereford and Angus bulls [40]. With Bos indicus bulls, the repeatability of libido scores was relatively low (r = 0.44) [41], although this procedure was regarded as being superior in repeatability and logistics to the serving capacity method for assessing sex drive in mature Bos indicus bulls [35]. When 26 yearling Bos taurus bulls were assessed a total of 8 times (two tests per day on four occasions over a 9 week period) for libido and serving capacity scores, four or more tests were required to significantly reduce test variance [4], although bulls which scored highly in the first test period generally scored highly in subsequent tests. Bulls which achieved low scores at the first test period either improved dramatically at some point in the testing regime, or else remained at a low level throughout. For the former group, a maturing and/or learning process was evident - a process which can adversely affect test results in young, inexperienced bulls. This phenomenon has been observed in other trials [4, 27,37] where young bulls obtained low serving capacity scores which improved with subsequent mating experience. Young, virgin bulls which achieve poor serving capacity results should be retested after they obtained sexual experience [37]. This resulted in improved scores in young virgin Santa Gertrudis bulls [42]; a group which has been difficult to adequately pen-test [43]. Best results have generally been obtained when assessments of libido or serving capacity are used to rank bulls or place them into categories or groups (with high scoring bulls being most predictable). Thus it was found that eight Hereford bulls maintained their relative ranking for both libido scores and fertility when assessed at both 16 and 40 months of age [44]. In another study [28], high correlations (r = 0.82 to 0.91) were obtained for rankings in mating activity between simulated pasture tests and subsequent pen tests of 12 Bos taurus bulls.

Fertility Relationships

Cattle fertility is a multifactorial trait with involvement of both male and female factors. From the male aspect, there is good evidence that bull libido is one of the more important contributing factors. For example, in one study, better first-cycle pregnancy rates were obtained in heifers mated with higher serving capacity bulls than in those mated with bulls of low serving capacity [45]. More recently, differences in pregnancy rates were demonstrated between high, medium and low serving capacity Hereford bulls [46]. Other studies have shown advantages in herd fertility for higher sex drive bulls [47-50]. Close relationships were reported between bull rankings for fertility, libido score and testosterone response to parenteral GnRH challenge [51]. In a Florida study, bull libido and semen quality both significantly influenced pregnancy rates achieved by naturally mated Brangus bulls, with libido having most effect (A.C. Warnick, personal communication), while a study with Bos indicus bulls in Mexico provided positive relationships between tests for bull sex-drive (libido and serving capacity scores) and reproductive performance [52]. Other studies have indicated either that bull libido assessment provided greater prediction of bull fertility than did semen assessment alone [50], or that it augmented traditional breeding soundness evaluation [53]. Using multi-sire mating and progeny identification by blood typing, the number of services performed in libido/serving capacity tests was positively correlated with fertility up to a level of approximately four services [54]. Above this level of services, however, fertility appeared to decline.

Despite such reports, however, others have shown either poor or inconclusive relationships between bull libido/serving capacity assessment and either herd fertility or bull performance at pasture [37,41,55-59]. In some studies, although higher libido bulls serviced more often, and serviced more females, than did lower libido bulls, more pregnancies did not result [4,37,58]. In northern Australia, prior assessment of bull sex-drive was generally not predictive of bull performance in multi-sire breeding trials [42].

A number of reasons may occur for such apparently contradictory findings, including differing approaches and methodologies. For example, bulls may not have been placed under sufficient breeding stress to demonstrate real differences. Such differences may have become apparent with use of higher BFRs or shorter breeding periods. Social interactions between bulls may mask differences in reproductive potential. In addition, in cooperator breeding trials, bulls of potentially low fertility are often excluded. A major potential problem exists whenever investigators attempt to demonstrate that a single trait (e.g., bull sex drive) has a consistent, decisive influence on herd fertility. This is because cattle fertility is a factorial, influenced by both male and female factors. Male factors include sex drive, mating ability, sperm numbers and semen quality. Scrotal circumference, sperm motility and morphology can separately influence fertility [53], and these are apparently not linked with sex drive in bulls [23,37,49,60,61]. Bulls may be superior in one trait, or several, but their fertility may be compromised by deficiencies in others. This was demonstrated in one study [58] where 92 beef bulls were placed both into satisfactory and questionable BSE categories, as well as into high (score 9 to 10) and medium (score 7 to 8) libido categories prior to single-sire mating with groups of estrus synchronized heifers. Here, pregnancy rate was 9.1 percent higher for satisfactory BSE bulls compared with those in the questionable BSE category. However, pregnancy rate did not differ between bulls of high and medium libido score even though high libido bulls serviced more females and served more times than did medium libido bulls. This paradox apparently occurred because a lower percentage of serviced females in the high libido group became pregnant than in the medium libido group. Here, differences between bulls in sex drive were masked by differences in BSE traits.

The ability of bulls to service females is related not only to their inherent sex drive but also to their mating ability. Problems in mating ability may be due to a number of physical and pathological causes including skeletal and penile abnormalities [18].

Factors Influencing Bull Sex Drive

1. Age, Rearing and Nutritional Effects

Age and (or) experience of bulls can influence their mating ability and thus their apparent sex- drive. Competent mating ability does appear to have a learning component in bulls [26,37,62-64] , even though exposing young Polled Hereford bulls to heifers post-weaning did not influence subsequent libido or mating ability [65]. In this trial, individually-penned bulls initially showed greater serving capacity than did group-penned bulls, but this difference did not persist. Male-male mounting in group penned bulls was not indicative of libido, serving capacity or mating behavior with heifers. It was concluded that social restriction of young bulls was not detrimental to their mating ability. In young tropical beef bulls, libido score increased with bull age between 16 and 31 months of age [38]. Bull age affected sexual behavior traits in crossbred bulls, with yearling bulls showing lower libido and a higher proportion of mounts than older bulls [54]. In Florida, sexual performance assessments generally increased with age in young (12 - 24 month) Bos taurus bulls, although not in Bos indicus bulls [66] which generally displayed a lower level of sexual activity. More information is needed to differentiate the effects of age and experience on bull sexual behavior from those due to environmental and managerial influences. Zebu bulls raised on open range exhibited slower sexual responses compared with those reared more intensively [67], although no permanent sexual inhibitions are attributable to rearing methods in bulls [48]. It is, however, possible that temporary sexual inhibitions in bulls may compromise pregnancy rates in herds which have restricted breeding seasons [7].

Nutritional effects on bull sex-drive have generally not been well characterized [21,68-71]. Prolonged nursing was considered to retard, or compromise, the expression of normal sexual behavior in Angus bulls [72] as was feeding high concentrate levels to crossbred bulls [69]. However, postweaning dietary energy levels were not found to affect sex drive in young bulls of synthetic breeds [53]. Negative relationships were obtained between sex-drive and production traits (average daily gain (ADG) and final test weight) in yearling beef bulls in one study [25], whereas underfeeding had no adverse effects on bull sexual behavior in another [70]. Indirect effects of overfeeding might include obesity as well as feet and leg problems; all of which could contribute to lowered sex-drive [73].

2. Bull to Female Ratio (BFR)

Traditional recommendations for bull-to-female ratios (BFRs) in natural breeding herds of 1:20 - 1:30 can underestimate the reproductive capabilities of competent bulls. For example, in a study in which single- and multi-sire breeding systems were compared using Hereford bulls at BFRs of 1:25, 1:44 and 1:60 [74], fertility, libido and mating ability of individual sires was more important than either BFR or single- vs multi-sire breeding systems. Similarly, in northern Australia, there was no difference in reproductive rates between single- and multi-sire herds studied over a period of 18 years [75]. In Colorado, yearling Hereford bulls which had been pre-assessed for BSE and libido, were compared at BFRs of 1:20 and 2:40 with estrus-synchronized crossbred heifers [76]. Overall, bull mating performance and pregnancy rates did not differ between BFRs. Comparison of a variety of single-sire BFRs (1:7 to 1:51), also with estrus-synchronized females, found that BFR was not a limiting factor to fertility, even at the lowest bull ratios [64], although another study suggested that lower fertility may occur when BFRs exceed approximately 1:50 [77]. In northern Australia, no difference was observed in herd fertility when reproductively sound Brahman bulls were used at BFRs of either 1:17 or 1:40 [78]. Two studies conducted in different environments showed that BSE-screened bulls increased herd pregnancy rates at reduced BFRs (1:20 to 1:33) [79,80]. Thus it is apparent that many bulls can handle considerably more females in a generic breeding season than traditional recommendations would suggest. It is also evident that most producers have yet to take full advantage of these findings. For example, USA surveys indicate that cow-calf operations overall use yearling bulls at 1:17.5 and mature bulls at 1:25; figures which have changed little in recent years (USDA-NAHMS 1998). Cow-calf producers in the Rocky Mountain West used a mean BFR of 1:21, with 25% of herds employing a BFR of <1:18 [81].

Several studies indicate that BFR is relatively unimportant when conducting tests for sex drive in young, experienced bulls [39,49] provided group sizes are relatively small. One study obtained better results when bulls were tested individually [65] although inter-male aggression and interference in group tests may have influenced these results. Such interference can occur more often when there is inadequate spacing between stimulus females, when older bulls are being tested or when bulls are tested in groups greater than 2 [27].

3. Social Effects

Social ranking of bulls within groups can influence their sexual activity [7,74,82,83]. Dominance is expressed more strongly and linearly in older bulls (i.e. those 3.5 to 4 years of age or older) and it appears to be more related to seniority than to either age or body weight [82]. It has been suggested that the effect of social interactions among bulls on herd fertility may be greater at lower BFRs than where there are higher levels of breeding stress [82]. Dominance effects among bulls can also influence results obtained in pen tests for bull sex drive [84].

Dominance rank was negatively correlated with sex-drive in one study with yearling bulls [25]. If dominance and sex-drive do indeed represent different traits, then the dominant bull (or bulls) could impair herd fertility both through failure to service females and also by preventing less dominant bulls from serving. Evidence exists for such effects in extensive beef operations [80], where it was also shown that the social dominance ratio of bulls had some relationship with herd fertility. Such effects are probably most evident when older and younger males are combined in the breeding pasture [82], although mixing different bull genotypes in the breeding pasture may apparently cause similar effects [85].

Social effects may, however, also be beneficial for bull sexual behavior. Such an effect was observed in one study where greater sexual activity occurred when young, inexperienced bulls were tested in groups [3-5] than when tested individually [48]. Similarly, yearling bulls of higher serving capacity achieved more services in double-sire tests than when tested alone [4]. The combination of bull prestimulation and competition can positively influence results of sex-drive test procedures [31].

4. Genetic Effects

The evidence for genetic influences upon bull sex-drive is strong. In Scandanavia, monozygous twin bulls raised on differing nutritional regimes displayed greater similarity within pairs in mating behavior and temperament than between pairs [21], suggesting strong genetic influences upon these traits. Paternal half-sibs of Swedish bulls differed significantly in libido with greater variation between sire-son groups than within them [22]. Studies showing that cross-bred bulls generally exhibited higher sex-drive in pen-tests than did their parental pure breds, indicate that genetic effects, in this case heterosis, influence bull sex-drive [38,86]. In Colorado, line of breeding (inbred lines or crosses among inbred lines) was an important source of variation in bull sex-drive, indicating that lines had previously been selected or differentiated on the basis of sexual behavior [23]. Similarly, differences in libido scores were observed between breeding lines and sires-within-lines in young bulls of British breeds [25]. Here, high sex-drive was not synonymous with either superior production traits (average daily gain or final test weight) or high social ranking. Sire strongly influenced serving capacity in young Angus bulls [26]. A number of studies have indicated that measures of traditional breeding soundness criteria, such as scrotal circumference and semen traits, are not significantly correlated with sex-drive estimates in bulls [23,24,37,49] indicating that these are separate traits. An heritability estimate of 0.59±0.16 was obtained for serving capacity in a study of 157 paternal half-sib bull groups in Australia [24]. In this study, the inclusion of bodyweight as a covariate did not alter the result, and serving capacity was not associated with temperament rating.

Breed effects have also been noted in bull sexual behaviour. Bulls of dairy breeds are reputedly more sexually active than those of beef breeds [33] and Bos indicus bulls often display lower, and more variable, levels of libido than do Bos taurus bulls [43,66,86]. In several studies in tropical Australia, Brahman and Brahman crossbred bulls obtained the lowest libido scores, Africander bulls and their crosses achieved the highest, whereas European bred bulls were intermediate [38,86]. In the US, Bos taurus bulls also obtained higher sex drive scores than did Bos indicus bulls [66]. Despite such findings, a comparison of trials in which bulls were placed with estrous synchronized females indicated that Bos indicus derived bulls were as efficient as European breed bulls in detecting, serving and impregnating estrous females, despite a lower service rate [6]. This discrepancy may be part explained by perceptions that Bos indicus bulls tend to be selective and shy breeders, and that they generally do not perform well in pen tests to assess sex-drive [42,66] , even though they can be very active and efficient in detecting of estrous females in the pasture. In Florida, Bos taurus (Angus, Hereford) bulls obtained the highest scores in sex-drive tests than did tropicalized Bos taurus (Senepol, Romosinuano) bulls, with Bos indicus (Brahman, Nellore x Brahman) bulls generally obtaining lowest scores [66]. Here it was suggested that commonly used testing procedures for sex drive may disadvantage Bos indicus bulls. Suggested test modifications for such bulls include use of unrestrained estrous females, and the minimization of distractions during the test [85], although use of restrained estrous females did not provide an advantage in one trial [42].

Alternative Assessments

The indirect determination of bull libido, e.g. via blood hormone levels, is an attractive proposition as it has the potential to reduce or eliminate the time, labor, esthetic or welfare concerns which might occur with current methods of assessing sex-drive. It would also allow assessment of bulls which do not respond well to such testing procedures. However, attempts to link either sporadic or sequential luteinizing hormone (LH) or testosterone (T) levels with bull sex-drive have generally been disappointing [7,27,88] probably because of the episodic nature of hormone release and the inhibiting effects of handling or restraint of the animal. By inducing LH or T release with parenteral administration of gonadotropin releasing hormone (GnRH), some of these difficulties may be circumvented. In one study [51], a significant relationship occurred between induced T levels and bull fertility, while in another [89], positive relationships were obtained with induced LH levels. However, other studies have obtained disappointing results when attempting to relate GnRH induced levels of testosterone or LH with bull sex drive [71,90].