Bull selection and use for improved performance in pastoral herds of Tanzania

I P B Kashoma, C Luziga and F O K Mgongo

Department of Veterinary Surgery and Theriogenology, Faculty of Veterinary Medicine,
Sokoine University of Agriculture, P.O.Box 3020, Morogoro, Tanzania
ikashoma@yahoo.co.uk   or   kashoma@suanet.ac.tz

Abstract

Tanzania shorthorn zebu (TSHZ) cattle are extensively reared in pastoral herds under natural multiple-breeding system in Tanzania.  However, no study has been carried out to describe the reproductive performance of TSHZ bulls. The objective of this study was to measure scrotal circumference (SC) and correlate it with age, heart girth (HG), spermatozoa quality and body condition (BC). 303 healthy TSHZ breeding bulls were evaluated. SC measured by using standard scrotal metal. Age was determined by dentition. HG circumference was measured by tape. BC was estimated by visual assessment. Sperm cells were collected by epididymal aspiration procedure and stained with Carbol-fuchsin. One hundred spermatozoa were counted per slide and each classified into normal or abnormal. Three parenchyma samples were taken after slaughter and processed for histological examination by staining with hemotoxylin and eosin. Forty sections of seminiferous tubules per section were evaluated and classified into either normal or abnormal.

Bulls were retrospectively classified into two groups; normal (55.8%) and abnormal (44.2%). The mean SC in normal bulls was 28.9±1.8 cm and positively correlated with age, years (r=0.67, P< 0.01) and HG, cm (r=0.82, P< 0.01). The mean percentages of spermatozoa abnormalities in normal and abnormal bulls were 15.6 ± 2.5 and 39.0 ± 9.1, respectively. Bulls with large testicular lesions had poorer seminal characteristics than bulls with normal testicles and the spermatozoa abnormalities increased with severity of testicular abnormalities (P < 0.01).

This study revealed that large numbers of inferior bulls are used for breeding in pastoral system that partly contributes to poor performance and low genetic improvement that currently exist in pastoral system. Also the study established the average values of SC for normal TSHZ bulls, however further studies should be done to establish the origin and effects of stump-tail spermatozoa abnormalities that had high prevalence in this study. 

Key words: scrotal circumference, spermatozoa abnormalities, Tanzania shorthorn zebu bulls

Introduction

Beef cattle production in Tanzania is dominated by Tanzania shorthorn zebu (Bos indicus) extensively managed on natural pasture under pastoral system. The breeding system is based on natural mating and is characterized by cows mated by using two or several bulls per herd (Mgongo and Kashoma 2007). Under such multiple-breeding system together with lack of record keeping on farms make it difficult to assess the fertility of individual bulls based on the female’s conception rate. Since a subfertile dominant bull may cause irreparable losses of an entire herd under this extensive management conditions, the importance of conducting a soundness examination cannot be over emphasized. The properly performed breeding soundness examination (BSE) involves evaluation of external physical characteristics, internal genital organs, the ability to achieve penile extension and erection, the ability to ejaculate, the scrotal circumference, and the motility and morphologic characteristics of ejaculated spermatozoa (Roberts 1986; Parkinson 2004). Among these, scrotal circumference and spermatozoa morphology are easy to measure under field conditions and are genetically associated with bull’s fertility (Gipson et al 1985; Söderquist et al 1991).

Scrotal circumference is a reliable indicator of onset of puberty and testicular function in bulls because is positively related to sperm quality parameters such as number of sperm, percentage of motile sperm and percentage of morphologically normal sperm (Brito et al 2002; Pant et al 2003). Also SC is highly heritable, positively related to testicular health, and is associated with onset of puberty, fertility, first and second calving dates of related females (Vargas et al 1998; Martínez-Velázquez et al 2003). However, there are many factors that can affect SC measurements. Important factors that affect SC include breed, age, body condition and the season of the year (Kastelic et al 2001; Pedro et al 2005). Hence, it is necessary to know SC variability that exists within a given breed and select bulls of higher-than-average scrotal circumference.

Semen quality parameters such as motility, sperm number and sperm morphology are of value in identifying bulls of low fertility in pastoral herds (Parkinson 2004). Of the component of semen quality, spermatozoa morphology is of utmost importance in zebu bulls extensively reared in the tropics (Chacón 2001). A correlation has been demonstrated between the fertility and the frequencies of some sperm abnormalities particularly those related to sperm head forms, defective acrosomes, and presence of proximal cytoplasmic droplets (Chacón et al 1999). Various techniques have been used to collect semen from bulls, including artificial vagina, electro-ejaculation, transrectal massage of the ampullae, aspiration of sperm from caudal epididymis and testicular biopsy (Roberts 1986; Goovaerts et al 2006). Nevertheless, due to management conditions and also to the hostile behavior of the breeding bulls in pastoral herds, the collection of semen for morphological evaluation may be done by aspiration of sperm cells (semen) from caudal epididymis (Goovaerts et al 2006). Spermatozoa aspirated from the caudal epididymis have been reported to be as fertile as those in the ejaculate (Barth and Oko 1989).

Many studies have been carried out to describe the reproductive performance of female Tanzania shorthorn zebu cattle (Kanuya et al 2006a; Kanuya et al 2006b). However, no comparative studies have been carried out to describe the performance of Tanzania shorthorn zebu breeding bulls extensively reared under multiple breeding systems. The present study was therefore undertaken to measure SC and establish the relationship of SC with spermatozoa morphology, age, heart girth (size) and body condition of Tanzania shorthorn zebu bulls.

Material and methods 

Study area and animals

This study was carried out in Morogoro and Coastal regions of Tanzania over a period of 12 months. Three hundred and three extensively reared, healthy Tanzania shorthorn zebu breeding bulls from the traditional pastoral livestock were examined. The examination included assessment of body condition, estimation of age, measurement of heart girth, assessment of external genital organs, semen collection and evaluation, and testicular tissue collection and histopathological evaluation.

Body condition score, age and heart girth measurements

Body condition scores, a subjective estimate of the overall nutritional condition of bulls was made after visual assessment using a one to nine-point scoring scale as described by Nicholson and Butterwoth (1986). Score 1 represented emaciated, 5 moderate amount of fat cover and 9 very fat. Furthermore, the estimation of age in all bulls was done by visual assessment of eruption and wear of dentition using a standard method described by Goetz (1979).

Heart girth (HG) circumference was measured while the animals were restrained in a crush standing on four legs with head maintained in an upright position as described by Goe et al (2001). A plastic tape marked in centimeters was drawn around each animal directly behind the front legs and the base of the hump. In order to standardize readings, a constant tension of 300g was applied to each measurement. The measurement was repeated three times and average recorded to the nearest half centimetre.

Assessment of external genital organs

The authors performed the detailed assessment of external genital organs of the bulls with animals restrained in a crush or with rope. The assessment included examination of external reproductive organs (prepuce, shape of scrotum), testicular consistency (determined subjectively by palpation; and classified as “normal’, “soft’ and “hard’), ultrasound scanning and measurement of scrotal circumference.  

The ultrasonographic examination of each testis (within the scrotum) was done with a B-mode diagnostic scanner (SonoAce SA 600V, Kretz Technich AG, Zipf, Austria) with a 5-mHz linear-array transducer. Coupling obstetric gel was applied to the transducer, which was aligned at the centre of each testis so as to be oriented vertically (parallel to the long axis of the testis) and reveal the mediastinum as a continuous band across the image. Testicular tissue was then scanned in different planes (transverse and longitudinal) for consistency and abnormalities.

Measurements of the SC were performed by grasping the scrotum from behind and forcing both testes to the bottom until ventral scrotal skin folds were eliminated. The testes were kept firmly in place by holding the neck of the scrotum with one hand. The area of the scrotum with the greatest circumference was then identified for measurement. Measurements were conducted using a graduated scrotal metal tape. The measurement was repeated three times and average recorded to the nearest half centimeter.

Semen collection and evaluation

Sperm cells (epididymal semen) samples were obtained using a modified epididymal aspiration procedure as described by Khorram et al (2001). A site on the bottom aspect of a testicle nearest to the caudal epididymis was shaved and disinfected with methylated spirit. A sterile 18-gauge needle was then threaded half to one centimeter deep into the caudal of the epididymis. In each case a sterile 5 ml syringe was used to aspirate semen by suction. The aspirated semen was placed on a clean microscopic glass slide, diluted with approximately equal amount of normal saline, thoroughly mixed and finally spread over the slide before air drying. The air dried slides were fixed with 0.2% glutaraldehyde solution. Staining was according to Boguth (1951), in brief, the slides were covered with carbol fuschin solution for five minutes, washed with 1% acid-alcohol (1.0 ml glacial acetic acid and 99.0 ml ethyl alcohol 90-95%) solution for five minutes, placed in Methylene blue solution for two minutes and finally washed with absolute alcohol before air drying. The smears were ultimately examined for spermatozoa abnormalities (magnification, X 100) by using a dark phase microscope (Minitube Abfull – und Labortechnik GmbH, Tieferbach, Germany). At least 100 spermatozoa were counted in each sample, and classified as either: normal spermatozoa, spermatozoa with abnormal heads or tails, or spermatozoa with proximal or distal cytoplasmic droplets (values expressed as percentages).

Testicular tissue collection and histopathological evaluation

Immediately after slaughter, the scrotum (containing the testes and epididymis) was excised, wrapped in a plastic bag and transported in a cool box to the laboratory. In the laboratory, the scrotum was excised and testes together with epididymis were exposed. Three parenchyma tissue samples were taken from dorsal, middle and ventral regions and fixed in Bouin’s solution. After 48 hours of fixation, the samples were washed with running water for 6 hours and finally trimmed and preserved in 70% ethyl alcohol at room temperature until processed. Parenchyma tissues processing for histology included imbedding in paraffin, sectioning (7µm thick) mounting on glass slides, and staining with haematoxylin and eosin. Forty tissue sections were examined for pathological changes (magnification, X 100) by using a light microscope. The changes were loss of germinal epithelium, loss of spermatocytes and/ or spermatogonia, vacuolation, presence of pyknotic nuclei, giant cells, and presence of only sustentacular cells in seminiferous tubules. The percentages of germinal epithelial loss (PGEL) described by Veeramachaneni et al (1986) were used to grade tissues either normal (less than 25% testicular tissue loss) or abnormal (more than 25% testicular tissue loss). The abnormal testicular tissues were further graded into five grades, namely, 1 = moderate degeneration, 2 = moderate hypoplasia, 3 = severe degeneration, 4 = severe hypoplasia, and 5 = mixture (at different rates) of degeneration and hypoplasia.

After thorough examinations, bulls were further categorized into two groups namely, normal bulls (healthy, good body condition, free of any clinical congenital or inflammatory diseases in their reproductive organs, histologically normal testicles and low percentage of spermatozoa abnormalities) and abnormal bulls (healthy, good body condition, presence of clinical congenital or inflammatory diseases in their reproductive organs, histologically abnormal testicles and high percentage of spermatozoa abnormalities). In summary, 55.8% of bulls qualified to be satisfactory breeders (normal bulls) and 44.2% unsatisfactory breeders (abnormal bulls).

Statistical analysis

Data were handled in Microsoft excel and analysed using the Statistical Analysis System (SAS 1999) windows program. Means and standard deviations of spermatozoa abnormalities, SC and HG were calculated for every age group. The linear relationship of SC with age was estimated, using a linear regression. Differences of SC attributable to age were tested, using 2-way analysis of variance, with age and heart girth as main effects. The effect of age on spermatozoa abnormalities was tested using 2-way analysis of variance, with age and BCS as main effects. The relationship of spermatozoa abnormalities with SC was tested, using a linear regression.  The relationship between different pathologic variables and SC was determined, using simple correlations. A probability value of ≤ 0.05 was considered statistically significant.

Results 

Detailed data on mean scrotal circumference and heart girth according to age in normal bulls are summarized in Table 1.

Table 2 summarizes the percentage of spermatozoa abnormalities in Tanzania shorthorn zebu bulls.

Table 3 illustrates the effects of testicular conditions on spermatozoa abnormalities in TSZ bulls observed in this study.

Scrotal circumference, body condition score, age, heart girth measurement and spermatozoa abnormality

The SC and mean percentages of spermatozoa abnormalities in bulls with normal testicles in this study ranged between 24 - 33 centimeters and 13.1 - 18.1%., respectively. The age, body condition scores and heart girth in all bulls ranged between 1.5 to above 4 years, 4 to 8 scores and 115 to 175 centimeters, respectively

Ultrasound images

A longitudinal images of normal testes showed moderate echogenicity scattered uniformly throughout the testicular parenchyma with mediastinum appeared as a high echogenic line in the midline. The transverse image of the testes showed a mediastinum as hyperechogenic spot in the middle. Regards to abnormal testicles, the ultrasonographic images was white (more echodense) and the intensity increased with severity of pathology in the testes. However, the hyperchogenicity was not correlated to the different types of testicular pathology such as hypoplasia and degeneration.

Relationship between scrotal circumference, age and heart girth

Scrotal circumference (SC) measurements varied with age groups and heart girth. SC increased gradually with advancement in age of the bull up to 4 years of age (p < 0.01), and thereafter increased marginally with little change. Linear regression analysis shown that SC increases with age (r = 0.67; P<0.01) and heart girth circumference (r = 0.61; P<0.01). Nevertheless, body condition had little influence on SC within same age group. Testicular pathology was a significant factor that caused significant variations in scrotal circumference because there was a difference in scrotal circumference between normal and abnormal bulls when age, heart girth and body condition score were similar.

Relationship between scrotal circumference and spermatozoa quality

Bulls with normal parenchyma tissues (normal bulls) had larger scrotal circumference compared to their counterparts with abnormal parenchyma tissues (abnormal bulls). Furthermore, normal bulls have few primary spermatozoa abnormalities such as stump-tail, Dag defects and pear shaped head. However, each of these abnormalities accounted for less than 2% of total abnormalities and did not contribute significantly to total spermatozoa abnormalities of any age group. Regarding to secondary spermatozoa abnormalities, normal bulls had few abnormalities in all age groups compared to their age mates of abnormal group. The mostly observed secondary spermatozoa abnormalities in abnormal bulls were loose head and bent tails.

In abnormal bulls, the total spermatozoa abnormalities were observed in high amount (39.0±9.1; mean and standard deviation). The commonly observed primary spermatozoa abnormalities were stump tail (57.5%; 54 out of 94 bulls), Dag defect (24%; 23 out of 94 bulls) and decapitated sperm heads (26%; 25 out of 94 bulls). Regards to secondary spermatozoa abnormalities, loose heads and bent tail were commonly observed in all age groups while proximal and distal cytoplasmic droplets was higher (4%) in younger bulls (below 2.0 years old), moderate (2%) in midle aged bulls (2.0 to 2.5 years old) and lower (1%) in mature and older bulls (above 2 years old)

Relationship between scrotal circumference and testicular pathology

Pathologic changes representing six grades, namely, moderate degeneration, moderate hypoplasia, severe degeneration, severe hypoplasia and mixture of degeneration and hypoplasia were observed. Bulls with high percentages of germinal epithelial loss (severe degeneration or hypoplasia) had small SC as well as no spermatozoa (azoospermia).  However, when the testicular histopathologic grades were correlated to spermatozoa abnormalities, a negative Pearson’s correlation was revealed (r=-0.16; P<0.19; n=303). But no correlation between testicular histopathologic grades with age (r=0) was observed

Discussion 

Age of bulls in this study ranged from 1.5 to above 4 years. This is the age range for young bulls to be recruited for breeding in the traditional livestock management system (Mpiri et al 1988). Accordingly, this study covered an age group, which is repeatedly used for breeding and therefore represents a large population of breeding TSH zebu bulls.

Scrotal circumference in bulls with normal testicles in this study ranged between 24 and 34 centimeters. The SC measurements were positively correlated with age (r=0.69; P<0.01; n=169). The increase in SC with age was gradual until bulls were 4 years. The increase was greater in the young than in the old. That is, there was a large variation in SC in young bulls causing a significant variation than in mature bulls. This finding is consistent with many other publications that report SC increases with age and that young bulls have a great potential of changing SC size (Brito et al 2002; MacGowan et al 2002). Similarly, scrotal circumference in this study is positively correlated with heart girth (r=0.77; P<0.01; n=169) and body condition score (r=0.33; P<0.01; n=169). Many researchers have reported similar correlations (coefficient correlations ranged from 0.45 to 0.78; P< 0.01) (MacGowan et al 2002; Sosa et al 2002). 

Scrotal circumference varies with breeds; breeds with small body size have small SC as compared with age mates of large body size (Kastelic et al 2001). This variation was also reflected by TSH zebu bulls in which SC of 26.3 – 29.7 centimeters for 2 – 3 year old bulls is obviously smaller than that of 31.7 – 34.7 centimeters reported for other zebu bulls of the same age group (Coulter 1986). Furthermore, testicular pathology is another factor that causes significant variations in scrotal circumference between bulls within age groups (Madrid et al 1988). Similar findings were observed in this study where bulls with normal testes had larger scrotal circumference as compared to their counterparts with abnormal testes. Similarly, testicular histopathologic examination of bulls with abnormal testicles revealed an increased number of abnormalities in seminiferous tubules such as loss of germinal epithelium, spermatocytes and/ or spermatogonia, vacuolation, presence of pyknotic nuclei, giant cells, and presence of only sustentacular cells in seminiferous tubules. Seminiferous epithelium has been reported to be sensitive to a variety of physical, chemical, endocrine, and pathologic disturbances resulting in degeneration of germinal cells and vacuolation of seminiferous epithelium (Roberts 1986). Similarly, the testicular pathological defects probably caused the observed decrease in scrotal circumference in bulls with abnormal testicles since the loss of germinal epithelium normally results in decreased scrotal circumference as observed by Veeramachaneni et al (1986).

Diagnostic ultrasound appears to offer an exceptionally fine tool for evaluating testicular structure, which is not available by any other means (Pechman and Eilts 1987; Abdel-Razek and Ali 2005). Ultrasound permits a non-invasive evaluation of internal structure of scrotum and testis with its fibrous tunics, as well as parenchyma and mediastinum and at the same time follows their changes. In this study, testicular parenchyma showed changes in enchogenicity of its ultrasonic image during pathological conditions. This is attributed to cellular proliferation and fluid production (Aravindakshan et al 2000).

The association of poor quality semen and bulls with abnormal testes was also observed in this study. Of the 303 bulls studied, 134 with abnormal testicles had the poorest semen quality as compared with their age mates with normal testicles (39.0 ± 9.1 versus15.6 ± 2.5). These spermatozoa abnormalities could be caused by testicular pathology such as hypoplasia and degeneration or low concentration of circulating testosterone (Barth and Oko 1989). Similarly, bulls with abnormal testes have many primary spermatozoa abnormalities such as decapitated sperm head, Dag defects and pear shaped as compared to their age mates with normal testicles. The spermatozoa abnormalities contributed significantly to total spermatozoa abnormalities of any age group. Dag defect development in the epididymis is believed to be due to exposure to abnormal epididymal secretion (Barth and Oko1989) and is commonly associated with disturbances to scrotal/ testicular thermoregulation in bulls (Kastelic et al 2001).

On the other hand, stump-tail abnormality which accounted for more than 2% in more than 49% of bulls examined was an important observation. Stump-tail abnormalities are indicative of abnormal spermatogenesis and are rarely found in large numbers of bulls (Stolla et al 1996). This fact is incomparable to our observation since there were high prevalence and large number of bulls having the defect in their spermatozoa. However, further studies should be conducted to establish if the stump – tail abnormality is an inherited defect in Tanzania shorthorn zebu and to estimate its effects on bull’s fertility.

Conclusion 

• The results in this study showed that the scrotal circumference measurements in TSHZ bulls range from 24 to 33 centimeters. The SC positively correlates with age, heart girth and body condition.

  
  

• The study also showed that percentage of spermatozoa abnormalities in bulls with normal testicles ranges from 13.1% to 18.1%.  However, bulls with abnormal testicles had high percentages of spermatozoa abnormalities. Nevertheless, further studies have to be conducted so as to establish the causes and effects of stump – tail abnormality observed in high amount in TSH bulls studied.

Acknowledgements 

This study was supported financially by Sokoine University of Agriculture Postgraduate Fund through NORAD project. Thanks are due to Germany Academic Exchange Programme, (DAAD) for donation of equipment.

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Received 12 July 2009; Accepted 31 August 2009; Published 1 January 2010

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