Br. vet.]. (1975), 131, 146
DEVELOPMENT OF PUBERTY IN THE WHITE FULANI (BOS INDICUS) BULL CALF T.
A. AIRE* AND].
u.
AKPOKOD]Et
*Department if Veterinary Anatomy and Physiology, t Department if Veterinary Medicine and Surgery, University
if Ibadan, Nigeria
SUMMARY
The development of puberty was studied in 20 White Fulani (Bos indicus) bull calves by employing histological analyses of the testes and epididymis of the calves. Primary spermatocytes were first seen at 36 weeks of age and the seminiferous cords were canalized at 44 weeks of age. Spermatozoa were first observed in the seminiferous tubules at 48 weeks of age. From 60 weeks of age, spermatozoa were present in large numbers in both the seminiferous tubules and all parts of the epididymis. The discussion included the few works done on puberty in the zebu breeds of cattle. INTRODUCTION
The study of development and attainment of puberty in bulls is important because of their relation to practical management of bull calves. Testicular development in certain breeds of bulls has been studied by various investigators (Phillips & Andrews, 1936; Fossland, 1954; Santamarina & Reece, 1957; Hay, Lindner & Mann, 1961). Fossland (1954), first saw spermatozoa in the lumina of seminiferous tubules of] ersey bull calves at 9 months of age and in the tenth month in Holstein-Friesian bull calves. Hay, Lindner & Mann (1961), studying the Friesian breed observed the first appearance of spermatozoa in the seminiferous tubules at 9 months of age. Santamarina & Reece (1957) stated that normal development of the testis depended more on the stage of development of the individual animal than on breed differences. Igboeli & Rakha (197 I) observed that it was generally assumed that cattle indigenous to the tropics grew slowly and attained puberty later than the taurine or European breeds. Environmental factors and/or genetic constitution have been implicated. Only Godinho (1970) and Igboeli & Rakha (1971) appear to have worked on puberty in two zebu breeds of cattle. Godinho's method of investigation was on evaluation of semen collected at different ages from the Brazilian Gir (Zebu) animal by electroejaculation. Igboeli & Rakha (1971) did a histological and hormonal assessment of puberty in the Angoni (Short Horn Zebu) bull calves. The purpose of this paper is to report the findings of an investigation on the sexual development of the White Fulani (Bas indicus) bull calf.
PUBERTY IN WHITE FULANI BULL CALF
147
MATERIALS AND METHODS
Twenty bull calves born and managed in the University of Ibadan Teaching and Research Farm were used in this investigation. The calves were weaned from their dams 3 days after birth and were bucket-fed on whole milk daily for 3 weeks. There was then, a gradual substitution to skim milk from which they were weaned at 4 months of age. Grass and concentrates were subsequently fed to the calves till they were castrated. The routine deworming and vaccination programmes of the farm were carried out. Two calves of the required age were unilaterally and openly castrated. The testes were freed from the tunica vaginalis propria and the epididymis, and weighed. Tissue for histology was taken from the central portion of each testis and from the three parts of the epididymis. All tissues were fixed in Bouin's fluid and formal-saline solution, and processed in the usual paraffin procedure. The tissues were then sectioned at 5 pm thick and stained with haematoxylin and eosin. The remaining testis in each calf was removed and treated similarly 2 weeks or a month later. The histological slides were analysed and the stages of development of the tissues were noted. The diameter of twenty round seminiferous tubules in each testis tissue was measured by using a calibrated eye-piece micrometer.
RESULTS
There was a pOSItIve correlation between live bodyweight and testicular weight, r = 0.71 (P 0·10), and between testicular weight and seminiferous tubular diameter, r = 0.96 (P 0·005). There was a clear parallelism between the testis weight and the seminiferous tubule diameter (Fig. I). At 4 weeks of age, the seminiferous cords had not developed canals and they were lined by supporting cells, and the central matrix contained varying numbers of gonocytes. The seminiferous cords were separated from one another by extensive masses of connective tissue. Similar findings were observed in testes of calves from 6 weeks to 16 weeks of age. The seminiferous tubular diameters (Fig. I and Table I) did not show any marked differences between 4 weeks and 16 weeks of age. From 20 weeks of age, there was generally an obvious increase in the tubular diameter, and a reduction in the amount of intertubular connective tissue with age. The gonocytes were now migrating toward the periphery of the sex cords (Fig. 2). Early, and a few late, stages of primary spermatocytes were seen in the seminiferous cords at 36 weeks of age. Canalization of the seminiferous cords was first observed at 44 weeks of age, and the intertubular connective tissue had virtually disappeared (Fig. 3). Also, from 44 weeks of age the increase in testis weight and seminiferous tubular diameter became very rapid. At this age, early and late stages of primary spermatocytes were observed in the tubules. Indeed, round spermatids were also evident in a few tubules in one of the calves of this age (Fig. 3). At 48 weeks of age, one of the bull calves had mature spermatozoa in about 60 per cent of its tubules. The other calf of the same age had spermatogenic stages up to sperma-
148
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TABLE I AGE, LIVE BODYWEIGHT, TESTIS WEIGHT AND SEMINIFEROUS TUBULE DIAMETER OF WHITE FULAN I BULL CALVES
Age (weeks)
Live bodyweight (kg)
Testis weight (g)
4 6 12 14 16 20 24 28 32 36 40
30'5 35'0 39'0 4 0 '0
2'5 3'0 3'2 5'7
86'0 79'S 29'2 115'0
12,6 7,8 14'1 21,8
121,6 153'3 165'8 17 6 '0 188'0 180'5
18'4 33 '8 57'8 68,S 80'5 9 2'1
44
48 56 60 64
Sem, tubule diameter (microns) 43'8 40 '8 45'0 45'0 40 '8 63'0 60'0 66,8 72 '3 90 '0 78 '6 12 7'8 15 1,8 17 1'0 192 '3 18 7'8
PUBERTY IN WHITE FULANI BULL CALF
Fig.
Fig. 3
2.
Twenty-week-old testis showing well-formed non-canalized tubules. x
149
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Fig. 4
Fig. 3. Forty-four-week-old testis showing canalized seminiferous tubules and primary spermatocytes at various stages of development. A few spermatids are also evident in one of the tubules. X 312. Fig. 4. Sixty-week-old testis showing mature spermatozoa. X 312.
tids only. Spermatozoa were present in most of the tubules of 56-week-old bull calves. At 60 and 64 weeks of age, mature spermatozoa were present in all tubules and in all three parts of the epididymis (Fig. 4). DISCUSSION
Primary spermatocytes were first seen in the seminiferous tubules of IO-week-old (70-71 days) calves in the work of Santamarina & Reece (1957). These spermatogenic elements were, however, first seen in this investigation at 36 weeks of age. Santamarina & Reece (1957) also stated that the seminiferous tubules acquired lumina at 4 months of age. We first observed canalization of the cords at 40 weeks (10 months) of age. This age is also three months later than in the Angoni bull calves studied by Igboeli & Rakha (197 I ). The a ppearance of primary spermatocytes in the tubules when tubular diameter was go fLm is in complete agreement with the observation by Hay, et at. (1961). They stated that one of the most characteristic changes in the bull testis associated with sexual maturation is an increase in the diameter of the seminiferous tubules. Thus the diameter could be used as a means of measuring testicular function and development. The rapid increase in the tubular diameter and the
BRITISH VETERINARY JOURNAL, 131, 2
associated spermatogenic elements from 32 weeks of age (Fig. 1) lend support to this observation. Spermatozoa were first seen in the lumina of 9-month-old Jerseys and 10month-old Holstein-Friesian bull calves (Fossland, 1954), and 9-month-old Friesian (Hay, et at., 1961). Spermatozoa were first seen in the tubules of 48week-old (12 months) White Fulani bull calves, and these became numerous and were present in all three parts of the epididymis as from 60 weeks (15 months). Igboeli & Rakha (1971) first observed spermatozoa in the epididymis of 13-month-old Angoni bull calves. This means that the White Fulani bull calf attains puberty at a much later age than the taurine breeds, and slightly later than the Angoni (Short Horn Zebu) bulls. The findings here agree with those of Godinho (1970), who stated that spermatozoa were seen only in animals over 60 weeks of age when he electroejaculated Brazilian Gir (Zebu) bull calves. Many reasons could be advanced for the relatively late sexual maturity in the zebu breeds of cattle, but perhaps the most relevant is the observation made by Courott; Kibler, Bergman & Turner; and Watson, Sapsford & McCance (all quoted by Ortavant, et at., 1969), that initiation of spermatogenesis is dependent more on the development of the animal than on its age. The White Fulani, like most other Zebu breeds, is a slow-growing breed of cattle and this probably explains why it attains puberty much later than the taurine breeds which are fast-growing animals. More work needs to be done on puberty in this and other Zebu breeds of cattle, and it is necessary to determine the reproductive capacity and potentials of the Zebu bull because of its importance in the livestock industry of many tropical countries. ACKNOWLEDGEMENT
We are grateful to Mr W . Ibok who helped during the collection of material and to the workers of the University of Ibadan Teaching and Research Farm dairy for their assistance and patience. REFERENCES
FOSSLAND, R. G. (1954),], Dairy Sci. 37,669. GODINHO, H. P. (1970). Arq. Esc. Vet. xxn, 165. HAY, M. F., LINDNER, H. R. & MANN, T. (1961). Proc. Roy. Soc., B. 154,433. IGBOELI, G. & RAKHA, A. M. (1971).]. Anim. Sci. 33, 647. ORTAVANT, R., COUROT, M. & HOCHEREAU, M. T. (1969). In Reproduction in Domestic Animals, ed. H. H. Cole & P. T. Cupps, 2nd edn. New York: Academic Press. PHILLIPS, R. W. & ANDREWS, F. N. (1936). Bull. Mass. Agr. Exp. St. No. 331. SANTAMARINA, E. & REECE, R. P. (1957). Am.]. Vet. Res. 18,261. (Accepted for publication 9 April 1974)
Le developpeDlent de la puberte chez Ie tauri110n White Fulani (Bos indicus) (Aire et Akpokodje)
ResUDle. On etudia Ie developpement de la puberte chez 20 taurillons White Fulani
(Bos indicus) en utilisant des analyses histologiques des testicules et des epididymes des veaux. On
PUBERTY IN WHITE FULANI BULL CALF observa les spermatocytes primaires pour la premiere fois a l'age de 36 semaines et les tubes seminiferes furent canalizes a I'age de 44 semaines. On enregistra la presence de spermatozoldes dans les tubules seminiferes pour la premiere fois a l'age de 48 semaines. A partir d e la 60 erne semaine, les spermatozoides se trouverent en nombre important a la fois d ans les tubules seminiferes et dans toutes les regions de I'epididyme. La discussion mit en jeu les quelques travaux sur la puberte chez les diiferentes races de zebus. Entwicklung der Pubertat bei White Fulani (Bos indicus) StierkaIbern (Aire und Akpokodje) ZusaDlUlenfassung. Die Entwicklung der Pubertat wurde b ei 20 White Fulani (bos indicus) Stierkalbern studiert mit Hilfe von histologischen Untersuchungen d es Testikel und Nebenhoden. Primaire Spermatozyten wurden zuerst in der 36.Woche gesehen und die Cordae seminiferae wurden durchlassig in der 44.Woche. Spermatozoen wurden in d en ductus seminiferi zum ersten Mal in d er 48.Woche beobachtet. Von der 60.Woche an waren grosse Mengen von Spermatozoen sowohl in den ductus seminiferi wie in allen Teilen d er Epididymis. Die wenigen Arbeiten i.iber die Pubertat bei Zuberindern werden erwahnt. Desarrollo de la pubertad en el ternero Fulani Blanco (Bos indicus) (Aire y Akpokodje) Resumen. Se estudi6 el desarrollo de la pubertad en 20 terneros Fulani Blancos (bos indicus) empleando analises histol6gicos de los testiculos y epididimo de los terneros. Los espermatocitos primarios se observaron por primera vez a las 36 semanas de edad y los conductos seminiferos se canalizaron a las 44 semanas de edad. Los espermatozoos se observaron por primera vez en los tubulos seminiferous a las 48 semanas de edad. A partir de las 60 semanas de edad, los espermatozoos se hallaron presentes en grandes cantidades tanto en los tubulos seminiferos como en todas las partes del epididimo. La discusi6n incluy6 las pocas obras que se han realizado sobre la pubertad en el cebu.