Appropriate bull selection is an important component of bovine herd improvement, with the aims of introducing desired genetic traits and enhancing herd reproductive performance. Whether both aims are achieved depends on fertility of the bull. The desire to improve beef herds through selection of superior genetics has resulted in the use of bulls younger than 18 to 24 months of age. This use has the benefit of shortening the generation interval (ie, decreasing the time for breeding-based genetic changes to a population) but can result in decreased herd reproductive performance if the bulls are not sufficiently sexually mature. Young bulls are hypothesized to be less reproductively efficient than older bulls owing to inexperience, unknown or decreased libido, and potentially less than desirable semen quantity and quality due to immaturity.1–9
Performance of a BSE before young bulls are sold or used is useful to identify those with adequate semen quality as well as other traits important for breeding soundness. Age at puberty has a significant effect on motility and morphology of spermatozoa in yearling bulls.4,10–13 Ideally, a BSE of yearling bull cohorts should be scheduled when it would allow for the identification of bulls that may be slow in attaining puberty, while at the same time allowing a reasonable percentage of the candidate bulls to pass the BSE. Ideal BSE scheduling can be a challenge because the BSE and sale dates are fixed, but the bulls are born over a range of dates and the age at which a bull is able to pass a BSE differs greatly among individuals. Information regarding the age at which a substantial proportion of young bulls would be able to pass a BSE would be useful to prevent time and resources from being allocated to evaluations conducted during a period when results are poorly predictive of performance in the postsale breeding season. Development of a minimum age guideline could theoretically result in a reduction in the number of reevaluations needed to estimate a young bull's semen quality prior to its first breeding season.
The purpose of the study reported here was to determine the proportion of yearling bulls capable of passing a second or third BSE after failing their initial BSE. A second objective was to evaluate the effect of bull age and breed on the likelihood of failing the initial BSE, with the goal of developing guidelines for the minimum age at which Angus, Simmental, and Charolais bulls could be expected to be of sufficient sexual maturity to pass a BSE. The final objective was to identify factors that could be used to predict likelihood of passing a second or third BSE after failing the initial evaluation.
Materials and Methods
Animals
Yearling bulls from 6 ranches for which a BSE had been performed by a licensed veterinary technician (ST) at the Kansas Artificial Breeding Service Unit from January 1, 2006, through December 31, 2013, were eligible for inclusion in the study. To be included, bulls were required to have had a routine BSE performed prior to sale, and ranch owners were required to be willing to have recheck evaluations performed at the Kansas Artificial Breeding Services Unit if bulls failed the initial BSE. Yearling was defined as an age between 11 and 14 months at the time of initial BSE.
BSE
The technician performing the BSEs did so under the direct supervision of a veterinarian and had 31 years of experience, including training under numerous veterinarians in the evaluation of bull semen and attendance at National Association of Animal Breeders bovine semen workshops. During the BSE, as was typical, the technician generated a spermiogram report by grading spermatozoa motility, classifying the morphological attributes of the spermatozoa, and identifying any other abnormalities in the semen sample. The technician reported all findings to the supervising veterinarian, who examined the bulls and reevaluated all semen samples that failed to meet SFT minimum guidelines for satisfactory classification. The supervising veterinarian then classified each bull as a satisfactory potential breeder, decision deferred, or unsatisfactory potential breeder in accordance with 1993 SFT guidelines14 on the basis of physical examination findings, scrotal circumference, or spermatozoa motility and morphology. The supervising veterinarian determined whether a testicular consistency, hair ring, or persistent frenulum affected the bull classification as a satisfactory potential breeder on a case-by-case basis. All other reproductive system evaluation abnormalities were treated as failure to meet SFT minimum guidelines. If no semen sample was obtained or no penile extension could be achieved after 3 attempts, the bull was classified as decision deferred provided it was not classifiable as unsatisfactory on the basis of physical or reproductive examination findings or scrotal circumference.
Data collection
Data were extracted from the records of each bull for the initial BSE and up to 2 recheck evaluations regarding source ranch, BSE date, birth date, breed, physical examination abnormalities, scrotal circumference, and spermiogram results, including percentages of progressively motile, morphologically normal, and morphologically abnormal spermatozoa.
Bulls were classified as Angus, Charolais, Simmental, or Angus-Simmental cross (50% Angus and 50% Simmental genetics) on the basis of information collected at the initial evaluation. Age at time of BSE was calculated in days by subtracting the birth date from the evaluation date and then rounded to the nearest month (defined as a 30-day period).
Results for each evaluated BSE component were converted into binary data by classification as pass or fail (Appendix). Failure in any 1 component resulted in an overall failure classification. For study purposes, bulls were classified as pass if they met all requirements for satisfactory potential breeder status or as fail if they met requirements for decision-deferred or unsatisfactory potential breeder status.
Statistical analysis
All analyses were performed with statistical software.a Basic descriptive statistics were calculated to summarize included bulls with respect to characteristics and findings at initial BSE and percentages that passed the initial, second, and third BSEs. To determine whether certain factors could predict the probability of bulls passing a subsequent evaluation after failing the initial BSE, a general linear mixed model was constructed. Considered fixed effects included initial evaluation data regarding breed, age, scrotal circumference per day of age, and percentage of morphologically normal spermatozoa. Random effects were included in the model to control for ranch of origin and year of initial BSE. The model was constructed by including all of these potential effects and removing nonsignificant (P > 0.05) effects one at a time in a backward stepwise manner.
To determine whether age at initial BSE or breed was a significant predictor of satisfactory initial BSE classification, a generalized linear mixed model was generated. Considered fixed effects included breed, age, and the interaction between these 2 variables. Random effects were included in the model to control for ranch of origin and year of initial BSE. The model was constructed by including all of these potential effects and removing nonsignificant (P > 0.05) effects one at a time in a backward stepwise manner. The final model included only variables with values of P ≤ 0.05.
Results
Animals
The original data set included 2,805 bulls from the 6 ranches and 3,252 BSE results. Data for bulls with ages ≥ 15 months4 (n = 36) or < 11 months (35) at any BSE or for bulls of breeds represented by < 20 bulls overall (12) were removed prior to analysis. Bulls with missing birth dates, breed, or scrotal circumference data (n = 658) were also removed prior to analysis. Therefore, the final data set included 2,064 bulls and 2,342 BSE results.
Included bulls were classified as Angus (n = 971 [47.0%]), Charolais (588 [28.5%]), Simmental (363 [17.6%]), and Angus-Simmental cross (142 [6.9%). All Charolais were from the same ranch, and the other ranches contributed bulls to at least 2 breed categories (Supplementary Table S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.12.1617). Over half of the included bulls (n = 1,385 [67.1%]) originated from the same ranch. Age at initial BSE was classified as 11 months for 158 (7.7%) bulls, 12 months for 416 (20.2%) bulls, 13 months for 1,196 (57.9%) bulls, and 14 months for 294 (14.2%) bulls (Supplementary Table S2, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.12.1617).
Initial BSE
A total of 1,777 (86.1%) bulls passed the initial BSE and were classified as satisfactory potential breeders; the remaining 287 (13.9%) failed. The SFT classification of 12 of the 287 (4.2%) bulls that failed was unsatisfactory potential breeder; the remaining 275 (95.8%) bulls were classified as decision deferred. The older yearling bulls were more successful at the initial BSE than younger bulls. Proportions of bulls that passed the initial BSE by age category were as follows: 11 months, 114 of 158 (72.2%); 12 months, 345 of 416 (82.9%); 13 months, 1,050 of 1,196 (87.8%); and 14 months, 268 of 294 (91.2%).
The number of bulls that passed each BSE component was as follows: physical examination, 2,033 (98.5%); reproductive examination, 1,946 (94.3%); scrotal circumference, 2,054 (99.5%); penile extension achieved, 2,055 (99.6%); semen sample obtained, 2,011 (97.4%); spermatozoa motility, 1,882 (91.2%); and spermatozoa morphology, 1,816 (88.0%). Of the 287 bulls that failed the initial BSE, 248 (86.4%) failed the spermatozoa morphology component. Scrotal circumference at initial BSE ranged from 26.0 to 45.5 cm.
Physical examination abnormalities in bulls that failed the initial BSE included left hind limb lameness (n = 6), corneal ulceration (5), right forelimb lameness (4), swollen feet or foot rot (3), right hind limb lameness (1), unspecified joint abnormality (1), signs of illness or pyrexia (1), unspecified hernia (1), neck abscess (1), and flank abscess (1). Reproductive examination abnormalities included WBCs in the semen sample (n = 36), persistent frenulum (13), abnormal testicular palpation results (10), penile or preputial warts (9), enlarged seminal vesicles or seminal vesiculitis (8), cryptorchidism (4), penile injury (3), RBCs in the semen sample (2), and bilateral cryptorchidism (1). Some bulls had > 1 reproductive abnormality noted. A persistent frenulum was identified and treated in 7 additional bulls that passed the initial BSE on the basis of satisfactory results in the other SFT categories and the supervising veterinarian's judgment on the reproductive system evaluation. Ten bulls did not meet the minimum scrotal circumference requirement, but only 1 of those 10 failed the BSE because of scrotal circumference alone.
Spermatozoa motility failed to meet minimum SFT guidelines for 182 bulls at initial BSE. Insufficient sample quantity and quality accounted for 48 of these failures. The remaining 134 samples had detectable spermatozoa motility that was below the SFT minimum guidelines. Most (129/134 [96.3%]) bulls with measurable spermatozoa motility below the minimum guideline had spermatozoa morphology that failed to meet minimum guidelines as well. Three of the 134 bulls with poor motility also had reproductive system abnormalities. The minimum requirement for normal spermatozoa morphology was not met for 248 bulls at initial BSE. Insufficient sample quantity and quality to quantify spermatozoa morphological defects accounted for 51 of these failures. The remaining 197 samples had quantifiable normal and abnormal spermatozoan morphology that failed to meet SFT minimum guidelines. The spermatozoa morphological defects were classified as primary or secondary as directed by the SFT guidelines. Percentages of morphologically normal spermatozoa, spermatozoa with primary morphological defects, and spermatozoa with secondary defects were recorded for each bull. For 125 of 2,064 (6.1%) bulls, > 50% of counted spermatozoa had primary morphological defects, and for 50 bulls, 100% of counted spermatozoa had primary defects. For 11 bulls, > 50% of counted spermatozoa had secondary morphological defects.
The probability of bulls passing the initial BSE by age and breed was graphically displayed (Figure 1). A significant (P = 0.009) interaction was identified between age and breed regarding the probability of passing the initial BSE, indicating that the effect of age depended on the breed. Because of this interaction, breed and age were not analyzed individually.
Probabilities of bulls passing an initial BSE by age and breed (Angus [white circles; n = 971]; Charolais [squares; 588]; Simmental [triangles; 363]; and Angus-Simmental cross [black circles; 142]). Error bars represent SD. The interaction between age and breed was significant (P = 0.009).
Citation: Journal of the American Veterinary Medical Association 253, 12; 10.2460/javma.253.12.1617
Subsequent BSEs
None of the 12 bulls classified on initial BSE by the supervising veterinarian as unsatisfactory potential breeders per SFT guidelines were reevaluated. Of the 275 bulls that failed the initial BSE and were decision deferred, 234 (85.1%) received a second BSE between 7 and 67 days after the initial BSE (mean ± SD interval, 24.8 ± 1.2 days). One-hundred twenty of the 234 (51.3%) tested bulls passed the second BSE (Supplementary Table S3, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.12.1617). Of the 114 bulls that failed the second BSE, 7 (6.1%) were classified as unsatisfactory potential breeders and 107 (93.9%) were classified as decision deferred.
Two of the 7 bulls classified as unsatisfactory potential breeders on second BSE and 42 of the bulls classified as decision deferred at that examination received a third BSE 14 to 56 days after the second BSE (mean ± SD interval, 27.7 ± 3.0 days). Twenty-four of the 44 (55%) bulls that failed the second evaluation passed the third BSE; the remaining 20 (45%) bulls failed to meet the criteria for classification as satisfactory potential breeders (Supplementary Table S4, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.12.1617). One of the 2 bulls that was classified as unsatisfactory at the second BSE was classified as satisfactory at the third BSE.
Overall, 1,921 (93.1%) bulls passed the BSE after a maximum of 3 evaluations. The proportion of yearling bulls that were not classified as satisfactory during initial BSE but were later classified as satisfactory was 143 of 287 (49.8%). Generalized linear mixed modeling revealed that none of the evaluated factors were significantly associated with passing a BSE after failing an initial BSE.
Discussion
Overall, 86.1% of yearling bulls in the present study passed an initial BSE and 93.1% passed with repeated testing. Of 234 bulls that failed the initial BSE and were reevaluated, 144 (61.5%) eventually passed 1 of 2 subsequent reevaluations. Breed, age (rounded to the nearest month), scrotal circumference per day of age, and percentage of morphologically normal spermatozoa at initial BSE were not significantly associated with the probability of passing subsequent evaluations. Previous studies3,4,10,12,15–23 have involved investigation of factors that predict puberty or maturity status, but to our knowledge, no studies have been conducted to identify factors that predict the probability of passing subsequent evaluations through data collected at initial BSE.
In the study reported here, older bulls were more likely to pass a BSE than younger bulls, which is consistent with previous reports3,4,24–26 of semen quality in bulls < 16 months of age at a single time point. Spermatozoa motility, percentage of morphologically normal spermatozoa, and percentage of spermatozoa with primary morphological defects in beef bulls in Florida reportedly improved from 12 to 18 months of age in 1 study.12 In another study,13 the percentage of morphologically normal spermatozoa from beef bulls increased with increasing age category (10 to 12, 13 to 18, 19 to 24, and ≥ 25 months). In a third study,17 Angus, Simmental, Hereford, and Limousin yearling bulls (8 to 15 months of age) that produced ≥ 70% morphologically normal spermatozoa were significantly older than bulls of the same breed that produced spermatozoa with unsatisfactory morphology,17 and the probability of failing to produce an adequate number of morphologically normal spermatozoa decreased as age increased. Investigators in that study17 concluded that age at first BSE was more important than scrotal circumference for predicting semen quality in their population of yearling bulls. Age at initial BSE was examined in the present study as a possible predictor of passing reevaluation after failing the initial BSE; however, no such association was identified for the evaluated bull populations.
In the present study, 72.2% of the bulls that were 11 months of age at initial BSE met SFT requirements for classification as satisfactory potential breeders. At 12, 13, and 14 months of age, 82.9%, 87.8%, and 91.2% of bulls, respectively, met these requirements at initial BSE. In research involving 11- to 15-month-old beef bulls in Canada, a mature spermiogram was defined as the production of ≥ 400 × 106 spermatozoa/mL, progressive motility in ≥ 60% of spermatozoa, and normal morphology in ≥ 70 % of spermatozoa.4,27 Only 20% of bulls had a mature spermiogram at 11 months of age in 1 study,4 and these numbers increased to 30%, 51%, 52%, and 61% at 12, 13, 14, and 15 months of age, respectively. Overall, 42% of the bulls met all criteria for a mature spermiogram and only 57% had ≥ 70% morphologically normal sperm.4 Other research involving analysis of BSEs from yearling bulls evaluated at the Western College of Veterinary Medicine showed that most (81% to 100%) bulls will have satisfactory semen quality by 16 months of age.1,28,29
Bulls reach maturity when their testes are fully functional and semen quality has attained adult properties. Semen quality of young bulls is expected to be similar to that of mature bulls by 12 to 16 months of age or 16 weeks after the onset of puberty.1,4,10 Onset of puberty in beef bulls occurs between 8 and 12 months of age, when puberty is defined as the first production of ≥ 50 million spermatozoa with ≥ 10% having progressive motility.19 Young bulls still going through puberty have low spermatozoa motility and a high percentage of morphological defects.4,10–13
Various studies10,27,30 have been conducted to determine age of onset of puberty in various bull breeds. Age of onset in Angus and Hereford bulls reportedly occurs between 9 and 12 months10,27 and in Charolais bulls between 7.5 and 12.5 months.30 Age of onset of puberty in Simmental and Simmental cross bulls has not been reported; however, previous research showed that among 93 Simmental yearling bulls, 35% had satisfactory semen quality at 11 months of age, whereas 56%, 61%, and 83% had satisfactory semen quality at 13, 14, and 15 months of age, respectively.1 Those findings are consistent with those of the present study as well as of previous studies6,10 of morphological spermatozoa defects for yearling bulls, in which older bulls were more likely than younger bulls to have satisfactory semen quality at initial BSE. Percentage of morphologically normal spermatozoa was evaluated in our study as a possible predictor of passing reevaluation after failing the initial BSE, but no significant association between these variables was identified for the evaluated bulls.
In the population represented in the present study, few bulls failed to meet the minimum requirement for scrotal circumference. Data on pre- and postweaning bull management and genetic selection were not available for review, but the bulls were being bred and raised for sale and use as yearling bulls. Owners of ranches that participated in the study were motivated to select for early maturing bulls and to manage the bulls so that optimal body weight and condition would be met by the time of sale. The selection and growth pressure expected to exist in the study population could explain the low number of bulls with small scrotal circumference. Several studies4,11,19,20,31 have shown that scrotal circumference can be used to select for early maturing bulls. In 1 study,17 only 27% of bulls with a scrotal circumference > 30 cm produced < 70 % morphologically normal sperm.17 In the present study, 10 of the 2,064 bulls (0.5%) had a scrotal circumference < 30 cm, 197 (9.5%) had < 70 % morphologically normal spermatozoa, and 51 did not have the semen quality or quantity needed to quantify morphological abnormalities at initial BSE. Previous research has suggested that scrotal circumference may be a more accurate predictor of age at onset of puberty than age or body weight at BSE, regardless of breed.10,11,17 Scrotal circumference per day of age was evaluated as a possible predictor of passing reevaluation after failing the initial BSE and was not significant for the bulls of the present study.
Prior research into the onset of puberty based on breed, age, or scrotal circumference showed that the mean age at onset varied by as much as 62 days among the 6 beef breeds evaluated and by 88 days among bulls within the breed groups evaluated.10 The variation in the onset and duration of puberty and the effects of nutrition and environment on growing bull calves make it difficult to estimate the age at which bulls will have a mature spermiogram. Because of this difficulty, in the authors' experience, it is common to reevaluate bulls that were young at initial BSE to try and separate bulls that failed because of immaturity from those that are sufficiently mature but are unsatisfactory potential breeders.
One objective of the study reported here was to determine whether age or breed plays a role in the probability of failing an initial BSE and then suggest guidelines for the minimum age at which Angus, Simmental, and Charolais bulls from the study population should undergo BSE. Given the significant interaction between age and breed in the study population, we were unable to develop recommendations for the minimum age to test the breeds of beef bulls represented by the study population. The effect of breed on growth and reproductive development was previously examined, revealing significant breed-by-age interactions for yearling beef bulls regarding body, testicular, skeletal, and pelvic growth traits.16 The conclusion was that the breeds of evaluated bulls had different growth patterns between 8 and 20 months of age.16 In the present study, breed was evaluated as a possible predictor of passing reevaluation after failing the initial BSE and was not significant for the evaluated bulls.
In a similar study12 involving reproductive traits and BSE categorization of bulls, investigators concluded that qualitative semen traits improved from 12 to 18 months of age and breed influenced spermatozoa motility and percentages of spermatozoa with normal morphology or primary morphological defects. These 2 studies12,16 also failed to identify an age on the basis of breed that was associated with reproductive maturation for the evaluated bulls. Another study17 involved determination of the proportion of bulls that had values less than the population means for age, scrotal circumference, and percentage of morphologically normal spermatozoa within breed at a single time point. Findings indicated that among yearling bulls, older bulls with larger scrotal circumferences were more likely to produce ≥ 70% morphologically normal spermatozoa than others, but age and scrotal circumference were not significant predictors of semen quality.17 The association between spermatozoa abnormalities and various factors has been evaluated for beef bulls in Alberta, Canada,22 but no significant associations were identified for mean percentage of spermatozoa abnormalities, total numbers of abnormal and normal spermatozoa, bull age, and scrotal circumference. Given the breed and age interactions identified in multiple studies, including the present study, we believe that additional research into body weights, physical examination abnormalities, reproductive examination findings, scrotal circumference, spermatozoa motility, and morphology for beef bulls of single breeds from 11 to 16 or 18 months of age would be better suited to develop recommendations for minimum age for performance of a BSE for various breeds of beef bulls.
A limitation of the present study was the inclusion of only bulls that the participating ranch owners chose to return for reevaluation if the bulls failed the initial BSE. We had no control of which bulls were reevaluated and which bulls were culled without reevaluation, nor were we privy to the reasons behind selection for culling or reevaluation. The statistical inferences made from the available data were also limited by the fact that bulls that were classified as satisfactory potential breeders were not returned for reevaluation alongside the bulls that were classified as unsatisfactory, so each BSE was treated as a separate event rather than evaluation of the risk of passing or failing a BSE over time. Also, detailed data were unavailable regarding the number and type of morphological defects identified for each bull at each evaluation. Furthermore, the study population was limited to a small number of ranches that met the inclusion criteria in a limited geographic area of Kansas, and only results from BSEs performed by a single highly trained and experienced technician were included in the study dataset to avoid interobserver differences in semen evaluation results.
Overall, the present study revealed no significant predictors of the probability of passing subsequent evaluations in yearling bulls of 4 common breed groups in Kansas that failed an initial BSE. The older yearling bulls were more successful at the initial BSE than younger bulls. Age and breed information should be considered when deciding at which age an initial BSE should be scheduled for yearling bull cohorts.
Acknowledgments
The study was conducted at the College of Veterinary Medicine, Kansas State University.
This manuscript represents a portion of a thesis submitted by Dr. Monday to the Kansas State University Department of Clinical Sciences as partial fulfillment of the requirements for a Master of Science degree.
No extrainstitutional funding or support was received for this project. The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| BSE | Breeding soundness evaluation SFT Society for Theriogenology |
Footnotes
SAS, version 9.3, SAS Institute Inc, Cary, NC.
References
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Appendix
Scoring system used for BSE of yearling beef bulls.
| Component | Pass | Fail |
|---|---|---|
| Physical examination for soundness, vision, and health | NAF | Ab |
| Reproductive system examination | NAF | Ab |
| Scrotal circumference | ≥ 30 cm | < 30 cm |
| Penile extension achieved | Yes | No |
| Semen sample obtained | Yes | No |
| Spermatozoa motility | ≥ 30% PM | < 30% PM |
| Spermatozoa morphology | ≥ 70% MN | < 70% MN |
Ab = Abnormality identified. MN = Morphologically normal. NAF = No abnormalities found. PM = Progressively motile.
