However, this reputation for poor reproductive capability raises questions about the relative roles of genetics, environment and management practices. The central question is whether B. indicus cattle are inherently of low genetic fertility or whether their poor reproductive performance is the consequence of a number of external influences, including environment and mismanagement. In this chapter, the latter opinion is supported. The extensive and stressful conditions under which B. indicus cattle are managed have confounded environmental and genetic factors and allowed the myth to develop that they can achieve maximum production with minimal input.

The chapter will first address general physiological aspects of B. indicus bulls before leading into practical approaches for evaluating their andrological status, taking into consideration the genetic, social and management factors that may influence findings and their interpretation.

Physiological Characteristics of Zebu Bulls

Significant physiological particularities have been determined in B. indicus males. The ability of this genus to withstand the environmental conditions prevailing in the tropics has been widely recognized for many decades (Cartwright, 1955; Turner, 1980; Kumi-Diaka et al., 1981), although much of the original focus of study was on their capacity to resist the effects of climate. It is now recognized though that B. indicus cattle possess superior capabilities to withstand other adverse effects on cattle production in tropical areas as well, such as low quality forages, and diseases especially caused by haemoprotozoa and other parasites (Cartwright, 1980).

B. indicus cattle are further recognized for their ability to better utilize low-quality forages and their lower nutritional requirements for maintenance than B. taurus cattle (Turner, 1980; Wildeus and Entwistle, 1984). Rekwot et al. (1994) suggested that B. indicus bulls are able to lower their metabolic rate during the dry season when good quality pastures are scarce. In general, B. indicus cattle exhibit a higher resistance to ticks and fly infestations than B. taurus cattle (Riek, 1962; Turner, 1980; Fordyce et al., 1996) as well. The skin thickness and its local defence mechanisms of the species could explain this feature.

Haematological differences between B. indicus and B. taurus cattle have been reported too. Turner (1980) found higher red blood cell counts and haemoglobin levels in Brahman (B. indicus) than in Hereford (B. taurus) bulls in Florida, which concurred with earlier findings (Evans 1963). This condition, together with their mechanisms of heat loss, may explain the lower body temperatures and respiration rates observed in B. indicus during rest or after walking in a tropical climate (Cartwright, 1955; Turner, 1980; Finch, 1986; Carvalho et al., 1995).

On testicular and scrotal thermoregulation, Turner (1980) reported that the scrotal skin in B. indicus bulls is hairless and less thick than that in B. taurus sires. These features may facilitate heat loss from superficial testicular vessels, and so act in favour of testicular thermoregulation. According to Brito et al. (2004), the ratio of testicular artery length and volume to testicular volume ratios were significantly larger in B. indicus and related crossbreeds than in B. taurus bulls. B. indicus sires also showed smaller testicular artery wall thickness than crossbred and B. taurus bulls (averages 192.5, 229.0 and 290.0 μm, respectively) and arterial to venous distances (averages 330.5, 373.7 and 609.4 μm, respectively) (Brito et al., 2004). Consequently, the proximity between the arterial and venous blood vessels in B. indicus males is more efficient in lowering the temperature of the arterial blood reaching the testicles. These physiological attributes might explain the lower prevalence of testicular degeneration – presumably resulting from environmental heat stress in the tropics – in B. indicus than in B. taurus bulls (Vale Filho et al., 1980; Kumi-Diaka et al., 1981; Wildeus and Entwistle, 1983, 1984; Crabo, 1988; Ohashi et al., 1988; Chacón, 2000).

Puberty and Sexual Maturity

Factors involved in the modulation of puberty and sexual maturity have received scant attention in B. indicus compared with B taurus bulls. Moreover, the available information has been generated from limited bull populations. Although the chain of endocrine and other events associated with puberty attainment are similar in the two species, there is general agreement that B. indicus bulls reach puberty and sexual maturity at a later age than do B. taurus males, even when they are raised under similar conditions (Igboeli and Rakha, 1971a; Fields et al., 1979, 1982; Vale Filho et al., 1980; Wildeus and Entwistle, 1982; Silva-Mena, 1997). Reports on age at puberty and sexual maturity in B. indicus bulls differ according to the breed involved, the conditions of the study (particularly the nutritional management of the experimental animals) and how puberty and sexual maturity achievement were defined. Many studies have employed the definition of puberty of Wolf et al. (1965) as the age at which a bull is first capable of producing an ejaculate containing at least 50 × 10⁶ spermatozoa with a minimum of 10% progressive motility. Others have defined puberty by recognizing histological indicators of the onset of spermatogenesis in preparations of testicular tissue. While the latter method has the potential of achieving greater accuracy than the former, it suffers from the disadvantage of being unable to be repeated in the same animal.

Using Wolf’s definition, the age at puberty in supplemented pasture-raised White Fulani (n = 6) and Sokoto zebu bulls (n = 6) in Nigeria was reported as 15.5 and 17 months respectively (Oyedipe et al., 1981), whereas in similarly raised Brahman bulls (n = 12) in Yucatán, México, the mean age at puberty was reported to be 17 months, with a mean body weight and SC of 374 ± 22.5 kg and 28.6 ± 0.6 cm, respectively (Silva-Mena, 1997). Supplemented hay-fed Brahman males (n = 10), which were monitored from 8 to 20 months of age in Florida, attained puberty at around 15.9 months of age, weighing 432 ± 16 kg and with an SC of 33.4 ± 1.2 cm (Fields et al., 1982). This relatively large testicular size in contrast with a number of comparable studies could be attributed to this being a closed herd that had been selected and managed optimally for some years. In another study in Florida, and in the same breed, Morris et al. (1989) suggested that puberty was attained between 14 and 15 months of age. However, no semen collection was performed in this study, with age at puberty being estimated based on the period of accelerated testicular growth. In tropical Venezuela, Guzerat (n = 159) and Nellore (n = 60) supplemented pasture-raised bulls reached puberty at 18.0 ± 2.0 and 18.5 ± 2.7 months of age, with an SC of 25.6 ± 2.2 versus 23.6 ± 0.2 cm and body weight of 310 ± 42 versus 268.1 ± 12.1 kg, respectively (Trocóniz et al., 1991). Other studies carried out in the same location with Brahman bulls (n = 4) reported puberty at an age of 21.3 months with a mean body weight and SC of 287.3 ± 67.8 kg and 24.9 ± 2.4 cm, respectively (Ocanto et al., 1984). In considering these results and others from different world regions, it is apparent that both genetic and environmental influences can strongly affect the age at puberty in B. indicus males.

Puberty, though, is not synonymous with sexual maturity or even acceptable fertility. For example, in yearling Tabapuâ (n = 246) zebu bulls (a B. indicus × B. Taurus crossbreed developed in Brazil), Corrêa et al. (2006) reported values for sperm motility and total spermatozoa per ejaculate (× 10⁶) ranging from 14.0 to 42.0% and 91 to 315.8, respectively. Despite such values being consistent with evidence of puberty attainment, they would not permit these bulls to pass a BSE or to achieve satisfactory levels of breeding fertility. Those hurdles were not reached in these same bulls until they achieved a mean SC and body weight of 33.5 cm and 490 kg, respectively, which, in some bulls, was not until they were 2 years old.

Studies based on histological analysis of the testis parenchyma and epididymal contents of young zebu males showed that only Sertoli and spermatogenic stem cells were found in the seminiferous tubules of 7-month-old grass-fed Angoni (short horn B. indicus) bulls in Nigeria (Igboeli and Rakha, 1971a). The onset of spermatogenesis was detected at 9 months of age, leading to the presence of first spermatozoa in the cauda epididymis at 11 months of age. Puberty was estimated to have occurred by approximately 14 months old in this breed (Igboeli and Rakha, 1971a). Similar results were found in two different studies by Aire and Akpokodje (1975) and Aponte et al. (2005), in Nigeria and Venezuela, respectively. In the first study, conducted with supplemented pasture fed White Fulani (n = 20), primary spermatocytes were found at 9 months of age and spermatozoa were present in large numbers at 15 months of age in both the seminiferous tubules and all regions of the epididymis. In the second study, conducted with similarly raised Brahman bulls (n = 20), the onset of spermatogenesis was estimated to occur at an average at 9 months of age.

Nutrition plays a significant role in the onset of puberty and attainment of sexual maturity in B. indicus bulls (Igboeli and Rakha, 1971a; Crabo, 1988; Vale Filho et al., 1996). For example, supplemented pasture-fed Boran bulls (n = 27) in Ethiopia reached puberty earlier (16.4 versus 17.8 months, respectively, P < 0.05), were heavier (208.6 ± 6.0 versus 193.5 ± 7.6 kg, respectively) and had larger SC (24.5 ± 0.6 versus 23.3 ± 0.6 cm, respectively) than control animals that were not supplemented (Tegegne et al., 1992). Underfed young B. indicus bulls show impaired body growth, delayed puberty and a retarded development of their endocrine system and reproductive tract (Rekwot et al., 1994). Deficiencies of essential micronutrients, such as zinc, selenium and vitamins A and E can negatively affect gonadotrophin release by the pituitary gland, thus impairing the replication and functionality of Sertoli cells, as well as hormone steroid synthesis by Leydig cells (Dunn and Moss, 1992). Because the critical process of Sertoli cell division occurs during the peri-pubertal period only, nutritional deprivation at this stage can seriously and irreversibly impair the potential reproductive performance of young zebu bulls.

Breeding Management of B. indicus bulls in Tropical Areas

Beef cattle production in tropical regions is largely dependent upon pure or crossbred B. indicus cattle that are extensively managed on natural pasture. Breeding of the herd is carried out by means of natural mating by using one or several bulls per herd. Data from tropical Costa Rica indicate that natural mating accounts for at least around 95% of the cows sired in beef farms. In general, B. indicus bulls are first bred at not earlier than 24 months. Breeding bulls are managed using continuous (i.e. the male mixed with the herd the whole year) or temporal mating seasons with one sire (single sire system) or several sires (multiple sire system). Data from the Andrology Section of the Veterinary School of the Universidad Nacional (UNA) of Costa Rica, based on 1100 BSEs of zebu bulls from the dry Pacific area, showed that 47.6% of the males (n = 524) were in a continuous mating system, and 49.5% of them were in multiple sire systems in which mixed-age or mixed-breed groups were common (Chacón, 2000). Additionally, around 7% of the bulls examined were over 7 years old.

The mean of bulls per group in multiple sire systems in Costa Rica was 4.0 (range 3–11) breeding sires for an average of 101.8 (range 15–450) cows. The mean number of cows in a single sire mating system was 29.3 animals (Chacón, 2000). These data call attention to the fact that, regardless of the system used, there is a bull/cow ratio of approximately 1:25, which is similar to data reported from other tropical countries (McCosker et al., 1989). This management strategy is used by most farmers, as it is believed to represent the maximum breeding capacity of a sire in natural mating, and because it compensates for bull sub-fertility.

Fertility in B. indicus bulls

The reproductive efficiency of breeding herds in tropical regions, where beef cattle production is based upon B. indicus breeds extensively managed on natural pastures, has often been reported to be low compared with those in more temperate areas, where B. taurus cattle predominate.

Fertility is a multifactorial status to which both males and females contribute. Males must produce a fertile ejaculate and be competent in delivering this to the female. Females must be able to produce fertile oocytes and provide a reproductive system compatible with sperm transport, capacitation, fertilization of the ova, and embryo and fetal development.

The fertility of naturally mating B. indicus breeding bulls, when measured by means of their pregnancy or calving rates, must embrace a wide range of decisive factors, which can include climatic stressors, cyclicity and fertility of females, nutritional constraints, sexual behaviour and a number of management considerations that are particularly pertinent for this species. For example, B. indicus bulls tend to spend more time in courtship than do European breeds, and this is possibly associated with females tending to spend less time in oestrus. Observations that Brahman bulls may miss mating opportunities owing to focus on a particular female (Aguilar Chavarria, 2008) have yet to receive scientific validation.

Under natural mating conditions, the fertility of B. indicus bulls differs between studies. Chenoweth and Osborne (1975) studied the performance of Brahman bulls 16–31 months old in Queensland, Australia. They found lower libido scores in this breed associated with its lower pregnancy rate (54.9%) compared with Shorthorn–Hereford (B. taurus) (64.4%) and the Africander crossbred (B. indicus) (79.1%) after breeding with 20 to 35 cows for 7 weeks individually. Although no differences in semen quality were noted between breeds, it is noticeable in this study that Brahman bulls were not selected before the mating period, so they also had the highest prevalence of presumed testicular hypoplasia (11.1% versus 1.4% overall), which could have accounted for these fertility differences. In fact, individually, many Brahman bulls performed as well as the best sires from the other breeds. Moreover, the use of some young Brahman bulls (16 months old) probably influenced the differences found as a result of sexual immaturity and lack of mating experience compared with the other bulls tested.

Crockett et al. (1978) reported the pregnancy records from mature (4 year old) Angus (B. taurus), Hereford and Brahman bulls in Florida, which were naturally mated with groups of 30 heifers for 90 days. Here, breed group affected pregnancy rates, being lower for the Brahman genotype (72%) compared with the other breeds (89.9%). It should be noted, though, that these bulls were selected on the basis of phenotype records as the main criteria.

Silva-Mena et al. (2000) studied the sexual behaviour and pregnancy rates of Brahman and Nellore bulls (n = 15), which were bred individually with groups of 16 oestrus-synchronized heifers in Mexico. The mean pregnancy rate under these conditions was 59.2 ± 5.8%, which was similar to values reported for European breeds by Pexton et al. (1989).

Bull Breeding Soundness Evaluation (BSE)

General background of the BSE in Bos indicus

Many decades of use and refinement have confirmed that the BSE is an essential tool in diagnosing and eliminating bulls of potential low fertility, thereby contributing to the reproductive efficiency of cattle herds. Much of this benefit has been obtained with B. taurus cattle in temperate regions. However, it is evident that even greater benefits are possible if widespread use of the BSE is adopted within B. indicus beef herds managed under extensive conditions in the tropics. This is because beef cattle in the tropics are generally managed either as herds under extensive grazing conditions or as small groups attached to local communities. Both systems are usually distinguished by the absence of a proscribed breeding period or season, as well as by a lack of adequate records for either productive or reproductive parameters. In addition, veterinary assistance is absent or infrequent, with the consequence that there is inadequate identification and elimination of those animals that have undesirable breeding characteristics. Bulls are often managed in multiple sire systems under extensive conditions, rendering it impossible to identify males of questionable fertility by means of their individual performance records. Therefore, bulls with reproductive problems often go unnoticed and are retained in the breeding herd, thus causing considerable economic losses. If such problem bulls are dominant within multiple sire breeding groups, the adverse effects on fertility can be compounded. Lack of a finite breeding period tends to obscure the extent of unsound breeding bulls in the herd as well.

Unfortunately, veterinarians are often not aware of how important a complete bull BSE is under these conditions, and continue to base their evaluations solely on aspects of semen quality and, in particular, on the assessment of sperm mass activity of the collected semen. In general, this practice does not include a complete clinical examination of the sire and, therefore, has led people to wrongly consider a bull BSE as just a ‘semen examination’ (Chacón, 2000). A similar picture emerges from other tropical regions (McCosker et al., 1989).

The tendency to undervalue the importance of the bull in herd reproductive performance is reflected in the relatively minimal attention given to studies in the tropics of the breeding performance of B. indicus bulls and the factors that interfere with their efficiency. An indicator of this imbalance is the ratio of publications concerning reproductive aspects in the male (20%) compared with the female (80%), and the low emphasis given to studying the reproductive aspects of B. indicus (19%) compared with B. taurus males (38%) (Galina and Russell, 1987; Galina and Arthur, 1991). Further, 42% of published research was associated with aspects of artificial insemination (AI) compared with 10% on natural mating (Galina and Russell, 1987).

Thus there is a strong case for promoting much higher acceptance of bull BSEs in extensively managed beef cattle herds where B. indicus type cattle are predominant.

Its performance should both provide relatively accurate information and be economically feasible. The ensuing sections will describe the different components of a thorough and practical andrological examination of B. indicus sires under field farm conditions.

General information and sire’s history

Although semen collection and evaluation are important aspects of the bull BSE, it should be emphasized that other aspects are of equal importance.

Accurate recording of age for B. indicus bulls is important for several reasons. For example, age is positively and significantly correlated with SC and semen quality. Similarly, the breed of the bull should be recorded, as B. indicus genotypes differ in SC and body weight relationships, as discussed later in this chapter. There is also a higher prevalence of venereal diseases and of skeletal and testicular pathologies in aged (i.e. >7 years) bulls. Another consideration with retrained older bulls is the risk of inbreeding – a factor whose effects are probably underestimated in tropical beef cattle stocks as a result of inadequate record keeping. Age of the bulls is further important in terms of relative ranking of the bull breeding team when results of the BSEs conducted on a particular farm are consolidated. Older bulls tend to have a shorter reproductive life expectancy – owing to a number of problems, as discussed above – so they should either be culled, or if particularly valuable, be used for monitored hand mating programmes.

The bull BSE should be based on a compilation of the considerations described above, and also include a history of nutritional and reproductive management, previous illnesses, abrupt weight changes prior to examination and any available information on preceding reproductive performance of the sire. Problems such as lameness, or any systemic disease causing fever, may adversely affect mating ability and spermatogenesis. Any potential existing problems in the cattle population, such as low heat observation, low calving rate or further reproductive problems, such as abortions, should be investigated as well.

Reproductive management

The breeding system employed, i.e. single or multiple sire, bull to female ratio, continuous or seasonal breeding and physiological status of the females (e.g. primiparous, first calf or multiparous and post-partum interval) should be recorded. In multiple sire systems, if the male is subordinated by a dominant bull partner, he is likely to have few chances to access the sexually active group of females. This system has the disadvantage of favouring social dominance, especially when age is not uniform in the group, which is often the case in the tropics (Blockey, 1979; Chenoweth, 1981; McCosker et al., 1989; Rodríguez et al., 1993; Chacón, 2000). Dominance is not necessarily related to bull libido and fertility. In addition, dominant older sires tend to monopolize mating opportunities with females, or at least prevent less dominant animals from accessing females, even though they are more likely to have a higher prevalence of reproductive problems (McCosker et al., 1989; Pérez et al., 1992).

McCosker et al. (1989) reported low conception rates in herds located in tropical Australia in which multiple sire breeding systems used Brahman bulls of mixed ages and where up to 82% of the calving cows were impregnated by the dominant bull. Furthermore, Rodríguez et al. (1993) reported that the dominant zebu (Indu-Brazil) bull was responsible for most (63%) of the bull-related sexual activity in the breeding herd. If this is generally so, the general belief of most farmers in tropical areas of the effectiveness of using a bull/cow ratio of 1:25 is not well founded. In continuous mating systems, many of the cows in the herd could be either pregnant or non-oestrous, thus lowering the ratio even more. Consequently, using a multiple sire breeding system in which the bulls are of mixed ages is often not efficient and can contribute to decreased reproductive outcomes.

The physiological status of the cows is also important, especially in relation to cyclicity and fertility. Early or middle post-partum cows (<5 months) that are still feeding calves have higher probabilities of being non-oestrous, especially if they are not in good body condition. In heifers, genetic or nutritional factors may contribute to lowered cyclicity and pregnancy rates that should not be attributed to deficiencies in the bull(s).

Libido and mating behaviour

The term libido describes the willingness and eagerness of a male to mount and to attempt service of a female, while mating ability describes the physical suitability of the male to complete a service (Blockey, 1979; Chenoweth, 1981). Several methods have been developed to measure libido, mainly in B. taurus bulls, in which the sire’s sexual response is evaluated during exposure to a restrained non-oestrous or oestrous cow for a certain interval (5–10 min). In B. taurus bulls, the libido score is highly correlated (r = 0.98) with the proportion of heifers served during a breeding season and has proved to be highly repeatable in this species (r >0.6) in consecutive trials under corral conditions (Price, 1987). Libido is highly inherited in bulls (heritability, h² = 0.5–0.59) and has been shown to be significantly correlated with sexual activity in the breeding pasture (Chenoweth, 1981; Hernández et al., 1991), although this does not necessarily translate into pregnancy rates. Blockey (1979) reported in Australia that at least 30% of bulls from several breeds with satisfactory semen quality had poor libido. In fact, libido is not significantly correlated with other reproductive traits, such as SC or semen quality.

When standard libido and serving capacity tests are applied to B. indicus bulls, they often achieve low scores in comparison with B. taurus bulls. This is considered to reflect differences in sexual behaviour between the species and not a genetic tendency for low libido in the former group. Given these particular differences, the application and interpretation of the results obtained after applying such tests to zebu sires are fairly difficult. For example, the sexual activity of B. indicus bulls seems to differ if tested under corral or grass conditions, and the repeatability of libido score results is less than that reported for B. taurus. Indu-Brazil bulls undergoing libido evaluations performed fewer services under corral conditions during a 30 min period than they did under grazing conditions (Hernández et al.