Bull Development

Chapter 5
Bull Development: Sexual Development and Puberty in Bulls


Leonardo F.C. Brito


ABS Global, DeForest, Wisconsin, USA


Introduction


Age at puberty is a major determinant of cattle production efficiency. The ability to breed animals at younger ages reduces generation intervals and increases genetic gains. However, reduced sperm production and poor semen quality due to immaturity are common causes of poor reproductive performance of young bulls and represent a serious loss of superior genetic stock. The ability to collect and freeze semen from younger bulls is also desired to reduce the time required for progeny testing and to accelerate the process of artificial insemination and sire selection. Therefore, an understanding of pubertal changes and the factors that affect sexual development is required in order to promote the successful use of young bulls for reproductive purposes.


Testicular development


Sexual development is associated with marked gonadal growth. Scrotal circumference (SC) is highly correlated with testicular weight (Figure 5.1) and is the most common endpoint evaluated to determine testicular development. The testicular growth curve in bulls shows an initial period of little growth followed by a rapid growth phase and then by a plateau (Figure 5.2). Although the overall pattern of testicular growth is fairly similar in all breeds, the characteristics of the growth curve are greatly affected by genetics. In general, the rapid growth phase is shorter and testicular growth plateaus sooner in bulls from breeds that mature faster (reach puberty earlier) than in bulls from late-maturing breeds, resulting in marked differences in the curve slope. This is especially evident when Bos taurus bulls are compared with Bos indicus bulls, which in general reach puberty later than the former. The asymptotic value of the testicular growth curve, namely adult testicular size (Figure 5.3), also differs considerably among breeds.1–7 These same differences can be observed within breeds between early- and late-maturing bulls (Figure 5.4), emphasizing the effects of genetics on testicular growth.8–10

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Figure 5.1 Regression lines for paired-testes weight (PTW) according to scrotal circumference (SC). Holstein1, measurements obtained from mature Holstein bulls (n = 35); PTW = –1298.5 + (50.2 × SC).116 Holstein2, measurements obtained from Holstein bulls (n = 47) 19–184 months old; PTW = –654.4 + (34 × SC).117 Angus and Hereford SC measurements obtained from Hereford (n = 199) and Angus (n = 136) bulls 11–30 months old; PTW = –722.28 + (36.53 × SC).3 Angus and Angus × Charolais SC measurements obtained from Angus and Angus × Charolais bulls (n = 111) 14–16 months old; PTW = –1274 + (54.04 × SC).

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Figure 5.2 Top: Regression curves for scrotal circumference (SC) according to age in Holstein, Jersey, Nelore, and Guzera bulls. Holstein measurements (n = 9614) obtained from bulls 6–77 months old; SC = –11.75 + [56.7 × (log Age)] – [15.3 × (log Age)2] (ASB Global Inc., unpublished results). Jersey measurements (n = 1038) obtained from bulls 7–75 months old; SC = –0.6814 + [40.26 × (log Age)] – [10.27 × (log Age)2] (ABS Global Inc., unpublished results). Nelore measurements obtained from bulls (n = 532) 7–43 months old; SC = 36.9/1 + [4.22–(0.11 × age)].118 Guzera measurements (n = 7410) obtained from bulls 2–69 months old; SC = 35.96/1 + [2.86–(0.002 × age in days)].119 Bottom: Testicular length and width associations with SC between 3 and 16 months of age in Angus and Angus × Charolais bulls (n = 111) receiving adequate nutrition.

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Figure 5.3 Weighted mean scrotal circumference (SC) reported for 2-year-old bulls of various breeds: Simmental, n = 540; Angus, n = 2310; Polled Hereford, n = 3546; Charolais, n = 1015; Hereford, n = 4369; Brangus, n = 1312; Braford, n = 1210; Limousin, n = 149; Nelore, n = 5903.4, 120, 121

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Figure 5.4 Mean (± SEM) scrotal circumference (SC) according to age (top) and age at puberty (bottom) in early- and late-maturing Nelore bulls (n = 6 per group). Arrows indicate mean age at puberty (ejaculate containing ≥50 × 106 sperm with ≥10% motile sperm; downward arrow indicates early; upward arrow indicates late). Early-maturing bulls had greater body weight (not shown) and SC than late-maturing bulls during the entire experimental period. In addition, early-maturing bulls were lighter and had smaller SC at puberty than late-maturing bulls, indicating that sexual precocity is not related to attainment of a threshold body or testicular development earlier, but that these thresholds are lower in early-maturing bulls. G, A and G × A indicate group, age, and group-by-age effects, respectively. Means with superscripts indicate differences between groups within age (a, P < 0:05; b, P < 0:005; c, P < 0:01).



Adapted from Brito L, Silva A, Unanian M, Dode M, Barbosa R, Kastelic J. Sexual development in early- and late-maturing Bos indicus and Bos indicus × Bos taurus crossbred bulls in Brazil. Theriogenology 2004;62:1198–1217 with permission from Elsevier.


SC is a moderately heritable trait in cattle; yearling heritability estimates are 0.36–0.55 in Angus,11–15 0.28 in Brahman,16 0.40–0.71 in Hereford,13,14,17–23 0.67 in Holstein,24 0.46 in Limousin,25 0.39–0.60 in Nelore,26–29 0.32 in Red Angus,30 and 0.48 in Simmental bulls.13 Therefore, direct selection can have a very significant impact on SC. For example, selection of Santa Gertrudis bulls based on minimum SC over a 10-year period resulted in significant changes in average SC in one herd,31 whereas testicular weight at weaning was greater in the progeny sired by Limousin bulls with high expected progeny difference (EPD) for SC compared with progeny sired by bulls with average or low EPD.32 Several studies have also demonstrated moderate to high phenotypic correlations between SC and growth traits and estimates of the genetic correlations with growth traits are generally positive (Table 5.1). Therefore, either the combination of direct selection for SC and/or indirect selection for growth traits is likely responsible for the general trend of increasing SC over the years in certain breeds (Figure 5.5).


Table 5.1 Genetic correlations (rg) between scrotal circumference and growth traits in bulls.




































































































Breed Growth trait r g Reference
Angus Yearling weight 0.24–0.68 Knights et al.12; Meyer et al.14; Garmyn et al.15
Sperm concentration 0.54
Sperm motility 0.36
Total sperm defects –0.23
Composite Yearling weight 0.40–0.43 Mwansa et al.33
Hereford Weaning weight 0.08–0.86 Meyer et al.14; Neely et al.17; Nelsen et al.18; Bourdon & Brinks19; Crews & Porteous20; Kriese et al.21; Kealey et al.23
Yearling weight 0.30–0.52
Weaning–yearling ADG 0.22–0.35
Sperm concentration 0.77
Sperm motility 0.34
Normal sperm 0.33
Hereford/Simmental Sperm concentration 0.20 Gipson et al.13
Sperm motility 0.11
Total sperm number 0.19
Limousin Weaning weight 0.14 Keeton et al.25
Nelore Weaning weight 0.36 Yokoo et al.26; Boligon et al.27
Yearling weight 0.34
Longissimus muscle area 0.28
Backfat thickness 0.17
Red Angus Yearling intramuscular fat 0.05 McAllister et al.30
Yearling carcass marbling score 0.01
Various breeds Birth–weaning ADG 0.02 Lunstra et al.85; Smith et al.107
Yearling weight 0.10–0.63
Weaning weight 0.56
Weaning–yearling ADG 0.59
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Figure 5.5 Mean scrotal circumference (SC) in registered yearling bulls according to year of birth. Measurements for Angus (unspecified number of bulls) and Limousin (n = 73 757; 1184–5200/year) bulls are adjusted to 365 days of age (sources: North American Limousin Foundation and American Angus Association). Measurements for Charolais (n = 6984; 121–997/year) and Hereford (n = 5553; 360–536/year) bulls are unadjusted measurements obtained between 321 and 421 days of age.



(sources: Canadian Hereford Association and Canadian Charolais Association)


Heritability estimates for SC vary according to age. Studies have demonstrated that heritability estimates increase with age until approximately 1 year of age (or 15–18 months of age in Bos indicus bulls), whereas estimates for 2-year-old bulls are lower.4,14,17,24,26,27,29,33 Therefore, selection based on yearling SC is recommended over selection based on measurements obtained at other ages. Yearling SC is commonly recorded in performance evaluation programs for beef bulls, but age effects are very pronounced around this age since testicular growth is rapid during this stage of development (Figure 5.6). In order to adjust SC measurements to age 365 days, the Beef Improvement Program recommends use of the adjustment factors described in Table 5.2. Correlation coefficients between SC at l year of age and SC and paired-testes weight at 2 years of age in Angus and Hereford and bulls were 0.76 and 0.65, respectively, demonstrating that a bull with relatively small or large testes as a yearling will generally have comparable testes size as a 2 year old.3

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Figure 5.6 Mean scrotal circumference (SC) in yearling bulls. Charolais: n = 246 to 2622/age (Canadian Charolais Association). Chianina, Marchigiana, and Romagnola: n = 455, 415, and 425/age, respectively.122 Hereford: n = 77 to 2510/age (Canadian Hereford Association). Holstein: n = 162 to 1004/age (ABS Global Inc.). Simmental1: n = 129 to 2276/age (Canadian Simmental Association). Simmental2: n = 120 to 2022/age (American Simmental Association). Standard deviations are all between 2 and 3 cm.


Table 5.2 Age adjustment factors for scrotal circumference (SC) at 365 days of age according to breed.




























Breed Age adjustment factor
Angus 0.0374
Charolais 0.0505
Gelbvieh 0.0505
Hereford 0.0425
Limousin 0.0590
Red Angus 0.0324
Simmental 0.0543

365-day SC = actual SC + [(365 – age) × age adjustment factor].108


Attempts to establish guidelines for selection of bulls at weaning based on the likelihood of attainment of certain minimum yearling SC have produced mixed results. In one study, it was recommended that the minimum SC in Angus and Simmental bulls 198–291 days old should be 23 or 25 cm to ensure an SC of 30 or 32 cm at 365 days of age, respectively; the same recommendations for Hereford bulls were 26 and 28 cm.7 In another study, differences between bulls that attained a minimum yearling SC of 34 cm and bulls that did not were observed for adjusted SC at 200 days of age (23.3 vs. 20.5 cm, respectively). Based on these results, it was suggested that SC at weaning could be used to select bulls for breeding and 23 cm was proposed as the minimum SC standard at 200 days.34 However, this study included bulls from several breeds with known differences in patterns of testicular growth and mature size, while using a singular and very strict yearling SC minimum. SC at 240 days of age could be used as a tool to select bulls with a high probability of meeting the minimum requirements for SC at 365 days of age (i.e., Simmental 32 cm; Angus, Charolais, and Red Poll 31 cm; Hereford 30 cm; Limousin 29 cm); sensitivity and specificity analysis for determining cutoff values indicated that the probability of Charolais bulls with SC ≥24 cm, Simmental and Limousin bulls with SC ≥22 cm, and Angus, Hereford and Red Poll bulls with SC ≥21 cm attaining minimum requirements was greater than 80%. However, SC at weaning was not useful as a culling tool, since a large portion of bulls, irrespective of breed, met the minimum requirements at 365 days of age even when SC was below 21 cm at 240 days of age.35


Although the heritability of semen traits is generally low, SC is positively associated with sperm production and semen quality and genetic correlations between SC and semen traits are generally favorable (Table 5.1). This suggests that direct selection for SC would be more effective in bringing about sperm production and semen quality improvement than direct selection pressure on semen traits themselves. In addition, several studies have reported an association between sire SC and daughter puberty. In Brahman and Hereford cattle, genetic correlations between SC and heifer ages at first detected ovulatory estrus, first breeding, and first calving were –0.32, –0.39 and –0.38, respectively.16,36 In another study with beef cattle, favorable relationships between greater sire SC and ages at puberty and at first calving were demonstrated by negative correlation coefficients between the two traits.37 In a population of composite beef cattle, the correlation coefficient among parental breed group means for SC and percentage of pubertal females at 452 days of age was 0.95, whereas the correlation with female age at puberty was –0.91.5 A significantly greater proportion of females had reached puberty at 11 and 13 months of age when sired by Limousin bulls with high SC EPD compared with females sired by bulls with low or average EPD.32


Although sire SC is associated with daughter puberty, evaluation of the genetic correlation between SC and pregnancy rates has produced low estimates that in some cases are not different from zero.28,30,38 A possible explanation for these observations is a nonlinear relationship between the traits. One study in Hereford cattle indicated that the effect of SC breeding values on heifer pregnancy exhibits a threshold relationship. As SC increases in value, there is a diminishing return for improved heifer pregnancy, suggesting that selection for a high SC breeding value may not be an advantage for increased heifer pregnancy over selection for a moderate SC breeding value.22 Although it would seem that the favorable genetic relationship between SC and age at puberty does not completely translate to heifer pregnancy, it is important to note that the experimental design might have confounded some of the referred results, since it is obvious that when the entire group of heifers reach puberty before exposure to breeding, those heifers reaching puberty at younger ages would have no advantage in conception over those reaching puberty at older ages. Moreover, end-of-season pregnancy rates were used in these studies as opposed to per-cycle pregnancy rates and the value of having heifers conceiving early rather than late in the season might have been lost.


Puberty


After spermatogenesis is established, there is a gradual increase in the number of testicular germ cells supported by each Sertoli cell and an increase in the efficiency of the spermatogenesis, i.e., an increase in the number of more advanced germ cells resulting from the division of precursor cells. The yields of different germ cell divisions, low during the onset of spermatogenesis, increases progressively to the adult level.39–41 Testicular histological changes and increasing efficiency of spermatogenesis are accompanied by increasing testicular echogenicity. Testicular ultrasonogram pixel intensity starts to increase approximately 12–16 weeks before puberty, and reaches maximum values right around puberty42 (Figure 5.7). If the initial changes in testicular echogenicity are associated with Sertoli cell differentiation and meiosis is not completed until formation of a functional blood–testis barrier, then 12–16 weeks seems to be the interval required for the gradual increase in the efficiency of spermatogenesis that eventually leads to the appearance of sperm in the ejaculate. That testicular echogenicity does not change significantly after puberty indicates that a certain developmental stage of the testicular parenchyma must be reached before puberty, a conclusion corroborated by the observation that testicular echotexture at puberty did not differ between early- and late-maturing bulls.9 In addition, testicular echogenicity did not change with age in mature bulls,43 suggesting that the composition of testicular parenchyma remained relatively consistent after puberty.

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Figure 5.7 Mean (± SEM) scrotal circumference (SC) and testicular ultrasonogram pixel intensity (TPI) according to age at puberty in Angus and Angus × Charolais bulls (Year 1, n = 37; Year 2, n = 39; Year 3, n = 43; Year 4, n = 33). TPI, determined on a scale of 1 (black) to 255 (white), started to increase 16–12 weeks before puberty and reached maximum values 4 weeks before or at puberty. These results indicate that a certain developmental stage of the testicular parenchyma must be reached before puberty and that the composition of the parenchyma remains consistent after puberty. Overall, TPI was greater (P < 0.0001) in Angus × Charolais than in Angus bulls. TPI means with superscript asterisks indicate overall change (P < 0.05) with age.



Adapted from Brito L, Barth A, Wilde R, Kastelic J. Testicular ultrasonogram pixel intensity during sexual development and its relationship with semen quality, sperm production, and quantitative testicular histology in beef bulls. Theriogenology 2012;78:69–76 with permission from Elsevier.


In general terms, puberty is defined as the process by which a bull becomes capable of reproducing. This process involves development of the gonads and secondary sexual organs, and development of the ability to breed. For research purposes, however, puberty in bulls is usually defined as an event instead of a process. Most researchers define attainment of puberty by the production of an ejaculate containing 50 million or more sperm with 10% or more motile sperm.44 The interval between the first observation of sperm in the ejaculate and puberty as defined by these criteria is approximately 30–40 days in Bos taurus bulls.45,46 Age at puberty determined experimentally can be affected by the age that semen collection attempts are performed, the interval between attempted collections, the method of semen collection (artificial vagina or electroejaculator), the response of the bull to the specific semen collection method, and the experience of the collector(s). Moreover, age at puberty is affected by management, nutrition (see below), and genetics. Table 5.3 describes weight, SC, and age at puberty in different breeds. Although data from large trials comparing bulls of different breeds raised as contemporary groups are scarce, some liberties could be taken to make some generalizations. Dairy bulls usually mature faster and attain puberty earlier than beef bulls. Bulls from continental beef breeds (with the exception of Charolais) usually attain puberty later than bulls from British beef breeds, especially Angus bulls. Bulls from double-muscled breeds are notorious for being late-maturing. Puberty is delayed in bulls from tropically adapted Bos taurus breeds and in nonadapted bulls raised in the tropics. In general, Bos indicus bulls attain puberty at considerably older ages than Bos taurus bulls.


Table 5.3 Age, weight, and scrotal circumference (SC) at puberty (ejaculate with ≥50 million sperm and ≥10% sperm motility) in different breeds.
























































































Breed Age (months)α Weight (kg) SC (cm) References
Angus 10.1 309 30.0 Wolf et al.44
Bos taurus beef crosses 7.8–9.7 272–339 27.9–28.3 Lunstra & Cundiff6; Lunstra et al.45; Casas et al.109
Brahman 15.9–17.0 350–430 28.2–33.0 Chase et al.110; Fields et al.111; Rocha et al.112; Silva-Mena113
Brown Swiss 8.7–10.2 233–295 25.9–27.2 Lunstra et al.45; Jimenez-Severiano46
Charolais 9.4 396 28.8 Barber & Almquist70
Guzera 18.2 310 25.6 Troconiz et al.114
Gyr 17–19.2 315–346 26.2–27.9 Martins et al.10
Hereford 9.6–11.7 261–391 27.9–32.0 Evans et al.8; Wolf et al.44; Lunstra et al.45; Pruitt et al.91
Holstein 9.4–10.9 276–303 28.4 Jimenez-Severiano46; Killian & Amann48
Nelore 14.8–19.7 232–298 21.7–24.3 Brito et al.9; Troconiz et al.114; Freneau et al.115
Red Poll 9.3 258 27.5 Lunstra et al.45
Romosinuano 14.2 340 28.8 Chase et al.110
Simmental 10.6–11.4 328–419 30.6–34.0 Pruitt et al.91

αTransformed from days or weeks from original reports.


There is large variation in age and body weight at puberty across breeds and within breeds. Although on average Bos taurus bulls attain puberty with SC between 28 and 30 cm regardless of the breed, the fact that there is still considerable variation in SC at puberty is sometimes overlooked. Interesting observations have been reported in studies evaluating differences between early- and late-maturing bulls. Bulls that attain puberty earlier were generally heavier and had greater SC than bulls that attained puberty later; however, both weight and SC were smaller at puberty in early-maturing bulls8,9,47 (Figure 5.4). These observations not only indicate that precocious bulls develop faster, but also suggest that sexual precocity is not simply related to earlier attainment of a threshold body or testicular development. In fact, these thresholds seem to be lower in early-maturing bulls, and late-maturing bulls must reach a more advanced stage of body and testicular development before puberty is attained.


Spermatogenesis efficiency reaches adult levels at approximately 12 months of age in Holstein bulls39,48 and 2.5–3.5 years of age in Bos indicus bulls.49 Individual variation in spermatogenesis efficiency is relatively small and is not affected by ejaculation frequency; values between 10 and 14 million sperm per gram of testicular parenchyma have been reported for bulls.1,6,39,48–54 Since spermatogenesis efficiency is somewhat constant among bulls, daily sperm production of a bull is largely dependent on the weight of the testes. Considering testicular weight at different ages, yearling Bos taurus bulls are expected to produce around 4–5 billion sperm per day, whereas adult bulls are expected to produce around 7–9 billion sperm per day. Sperm output (number of sperm in the ejaculate) in bulls ejaculated frequently is essentially the same as sperm production.51 One important difference between young and older bulls is the capacity of the epididymis to store sperm. Evaluation of sperm numbers in the tail of the epididymis in 15- to 17- month-old Holstein bulls demonstrated that sperm available for ejaculation corresponded to approximately 1.5–2 days of sperm production, whereas in 2- to 12-year-old bulls stored sperm numbers corresponded to approximately 3.5–5 days of sperm production.55,56 These observations are especially important for artificial insemination centers and indicate that more frequent semen collection is necessary to maximize sperm harvest from young bulls, whereas semen collection intervals of less than 3 days have smaller effects on increasing sperm harvest from older bulls. Sperm output increases with increased ejaculation interval up to the number of days required for epididymal storage capacity to reach its limit. Sperm that are not ejaculated are eliminated with urine or during masturbation.


Semen quality in peripubertal bulls is poor and a gradual improvement characterized by increase in sperm motility and reduction in morphological sperm abnormalities is observed after puberty. The most prevalent sperm defects observed in peripubertal bulls are proximal cytoplasmic droplets and abnormal sperm heads (approximately 30–60% and 30–40% at puberty, respectively; Figure 5.8).8,47,57 The difference between age at puberty and age at satisfactory semen quality (≥30% sperm motility, ≥70% morphologically normal sperm) was 110 days in Bos indicus bulls9 and 50 days in Bos taurus beef bulls; 10% of the latter did not have satisfactory semen quality by 16 months of age58 (Figure 5.8). In western Canada, the proportions of Bos taurus beef bulls with satisfactory sperm morphology (≥70% morphologically normal sperm) at 11, 12, 13, and 14 months of age were approximately 40, 50, 60, and 70%, respectively.59 Similarly, only 48% of Bos taurus beef bulls 11–13 months old in Sweden had less than 15% proximal cytoplasmic droplets and less than 15% abnormal sperm heads.60 These observations have profound implications on the ability of producers to use yearling bulls and the ability of artificial insemination centers to produce semen for progeny testing at the youngest possible age.

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Figure 5.8 Top: Mean sperm viability and morphology according to age in Angus and Angus × Charolais bulls (n = 39). Bottom: Proportion of pubertal (ejaculate containing ≥50 × 106 sperm with ≥10% motile sperm) and mature (ejaculate containing ≥30% motile and ≥70% morphologically normal sperm) bulls according to age. The interval between puberty and maturity was approximately 50 days.



Adapted from Brito L, Barth A, Wilde R, Kastelic J. Effect of growth rate from 6 to 16 months of age on sexual development and reproductive function in beef bulls. Theriogenology 2012;77:1398–1405 with permission from Elsevier.

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