Short communication Testis developments and puberty in the male Tokara (Japanese native) goat

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1 Animal Reproduction Science 64 (2000) Short communication Testis developments and puberty in the male Tokara (Japanese native) goat S. Nishimura a,, K. Okano b, K. Yasukouchi c, T. Gotoh a, S. Tabata a, H. Iwamoto a a Department of Animal Science, Faculty of Agriculture, Graduate School, Kyushu University, Fukuoka , Japan b Department of Plant Resources, Faculty of Agriculture, Graduate School, Kyushu University, Fukuoka , Japan c University Farm, Fuculty of Agriculture, Kyushu University, Fukuoka , Japan Received 18 April 2000; received in revised form 1 August 2000; accepted 1 August 2000 Abstract In male Tokara (Japanese native) goats, testis development and the onset of puberty were studied histologically and observing sexual behaviour. Testes weight increased from 36 ± 5.4(S.E.) g (n = 5) at 3 months of age to 126±6.3g(n = 6) at 12 months. The degree of the testis development differed among kids at 3 months of age and only one of four had produced spermatozoa in the testis. Large number of spermatozoa were always present in seminiferous tubules and epididymal ducts from 4 months of age. The diameter of seminiferous tubules increased from 133 ± 9.9 m(n = 4) at 3 months to 198 ± 1.0 m (n = 3) at 6 months with little increase thereafter. Mounting and pelvic thrusts onto a teaser doe started at from 9 to 14 weeks of age. Ejaculated semen contained sperm with good motility for the first time from 17 weeks. The male Tokara goat reaches puberty at around 4 months of age but testis development continues to 12 months Elsevier Science B.V. All rights reserved. Keywords: Goat; Male reproduction; Puberty; Testis; Sexual behaviour 1. Introduction Detailed information about the onset of puberty and sexual maturation are needed for good reproductive management of domestic animals. Most breeds of goat are seasonal breeders but the age of puberty in male differ among them (Yao and Eaton, 1954; Louw and Corresponding author. Tel.: ; fax: address: shotaro@agr.kyushu-u.ac.jp (S. Nishimura) /00/$ see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S (00)

2 128 S. Nishimura et al. / Animal Reproduction Science 64 (2000) Joubert, 1964; Elwishy and Elsawaf, 1971; Madani and Rahal, 1988; Chakraborty et al., 1989; Bilaspuri and Singh, 1992; Deveson et al., 1992; Ahmad and Noakes, 1996; Abi Saab et al., 1997) as determined by the first appearance of the spermatozoa in ejaculated semen. The Tokara goat is a small Japanese native breed which has been breeding in the Tokara islands which are located on the southwest side of Japan and which provides for local meat demands. It is an aseasonal breeder and is potentially useful as an experimental animal for studying small ruminants (Manda, 1986). However, there is no information about sexual maturity in male. In this study, testis developments and onset of puberty in the male were evaluated by measuring age-related histological changes occuring in the testis as well as associated changes in sexual behaviour. 2. Materials and methods 2.1. Animals Twenty-seven male Tokara goats bred in Kyushu University Farm, Fukuoka, Japan were used. Testes from 23 of them were used for the histological studies; the remaining four males were used for observational studies of sexual behaviour. The goats were weaned at 3 months of age and reared in a pen of similarly aged contemporaries Histological methods Each testis and epididymis was taken by castration or slaughter under deep anesthesia with sodium pentobarbitone from animals at 3, 4, 6, 9, 12 and 24 months of age (Table 1). After measuring organ weight, the tissue of testis and epididymal tail were excised and fixed with Bouin s fixative or 10% formalin and embedded in paraplast. Thin sections of 5 min thickness were cut and stained with hematoxylin and eosin. Seminiferous tubule sections (n = 50) in each animal were randomly selected on the photomicrographs taken from the preparations and tubule size determined by measuring the maximum width perpendicular to the long axis. One-way analysis of variance was used for the comparison among means. The significance of differences was determined by the Tukey s multiple range test. Significance was determined at P<0.05. Table 1 Body weight, testes weight and its relative weight to the body weight in the male Tokara goats Age (months) No. of animals Body wt. (kg) a Testes wt. (g) a,b Testes wt./body wt. (%) a ± 0.45 a 36 ± 5.4 a 0.39 ± a ± 0.43 ab 62 ± 9.8 ab 0.58 ± b ± 0.74 bc 86 ± 6.8 b 0.54 ± ab ± 1.51 cd 82 ± 5.6 b 0.47 ± ab ± 1.47 d 126 ± 6.3 c 0.56 ± b ± 1.88 e 127 ± 8.2 c 0.42 ± ab a Mean ± standard error; means with same letters are not significantly different among ages (P <0.05). b Including the weight of the epididymis.

3 S. Nishimura et al. / Animal Reproduction Science 64 (2000) Observations of sexual behaviour To estimate the onset of sexual behaviours, the four male kids born from 6 to 14 December 1998 were given an easy access to estrous teaser doe for 15 min every week from 8 weeks of age. Estrus was induced in the teaser doe following an injection of prostaglandin F2a (Cayman Chemical Company, USA). The behavioural interactions were observed as nosing, nudging, pawing, bleating, flehmen, mounting, penile erection, and pelvic thrusts. Semen was collected by artificial vagina at copulation and the presence of sperm confirmed by light microscope. 3. Results 3.1. Development of the testis There was no significant difference between left and right sides in testis weight (including epididymis). Testes weight increased from 36 g at 3 months of age to 126 g at 12 months (Table 1). The percentage weight of testes on body weight increased from 0.39% at 3 months to 0.58% at 4 months and maintained a similar percentage to 12 months. It decreased to 0.42% at 24 months (Table 1). The histological structure of testes and epididymides differed among the four kids castrated at 3 months of age. The lumen of the seminiferous tubules with a germinal epithelium of two to three cell layers was small and did not contain spermatids in the kid of the smallest body weight (8.7 kg) (Fig. 1A). No spermatozoa were observed in the epididymal ducts of this animal. In contrast, the germinal epithelium was composed of five to six cell layers with spermatids in the testes of the kid of the largest body weight (10.4 kg) (Fig. 1B) and there were numerous spermatozoa in lumen of the seminiferous tubules and epididymal ducts. The other two kids had some seminiferous tubules with some spermatids, but the epididymal ducts had no spermatozoa. The seminiferous tubule diameter at this age averaged 133 ± 9.9(S.E.) m in diameter (n = 4). There were numerous spermatozoa in the lumen of seminiferous tubules and epididymal ducts in testes from kids aged 4 months or more (Fig. 1C). Mitosis and meiosis were observed frequently in the germinal layer of seminiferous tubules with an average diameter of 149 ± 8.5 m(n = 3). After 6 months of age, the seminiferous tubules and epididymal ducts were filled with spermatozoa (Fig. 1D). Diameters of the seminiferous tubules were 198 ± 1.0 m at6 months (n = 3), 207 ± 4.1 m at 9 months (n = 3), 197 ± 8.3 m at 12 months (n = 4) and 218 ± 5.9 m at 24 months (n = 3), indicating little increase from 6 months of age Sexual behaviours Onset of a range of sexual behaviours in the four male kids was observed as shown in Table 2. It was at 8 to 9 weeks of age that each one of the kids displayed a special interest in the teaser doe by nosing for the first time. Direct behaviours such as penile erection, mounting and pelvic thrusts appeared over the range of 9 to 14 weeks of age. Other behaviours such as nudging, pawing, licking and flehmen were also observed intermittently.

4 130 S. Nishimura et al. / Animal Reproduction Science 64 (2000) Fig. 1. Light micrographs of the testis in the male Tokara goats at 3 months (A and B), 4 months (C) and 6 months (D) of age. At 3 months of age, one kid had no spermatozoa in the seminiferous tubules (A), but many spermatozoa (arrowheads) were observed in the tubules in other kid (B). After 4 months of age (C and D), seminiferous tubules developed larger and many spermatozoa (arrowheads) were seen constantly. Bar indicates 50 m. A few spermatozoa with low motility were seen in the small ejaculate volumes collected from the kids at 15 to 16 weeks of age. Semen of measurable volume (about 0.6 ml) was ejaculated for the first time at 17 weeks of age. It showed pale greenish-yellow color and contained numerous sperm with good motility. The teaser does conceived as a result of pairing with kids at 18 weeks of age. Table 2 Age at the initial display of selected features of sexual behaviours in four male Tokara goats a Sexual behaviour Age (weeks) Nosing 8 9 (4) Nudging 11 (2) Pawing (3) Licking (2) Bleating with low pitch 9 14 (3) Flehmen 8 15 (3) Mounting 9 14 (4) Penile erection 8 13 (4) Pelvic thrusts 9 14 (4) a The age indicates the earliest and the latest case. Parentheses indicate the number of kids which exhibited the behaviour.

5 S. Nishimura et al. / Animal Reproduction Science 64 (2000) Discussion The total testis and epididymis weights of adult red Sokoto goats was 0.34% (Nwoha, 1995) or 0.56% of body weight at years old (Daudu, 1984). In Toggenburgs and its crossbreds, the testes weight represents 0.66% of body weight at 120 days and 0.50% at 210 days (Yao and Eaton, 1954). The testes and epididymis weight was in 0.58% of body weight at 4 months of age and 0.42% at 24 months in our Tokara goats, reflecting a relatively small testis size. Although the average testes weight of the Tokara goat increased until 12 months of age, the diameter of the seminiferous tubules attained mature size at 6 months of age. This suggests that the development of the testis in this breed of goat is complete by 12 months of age. Maximum testis weight of Tokara goats was not achieved until 12 months of age but this development was mainly by increasing its volume after 4 months of age, since the diameter of the seminiferous tubules had reached maximum dimensions by 6 months. The increase of 40 g in the testis weight from 86 g at 6 months to 126 g at 12 months (Table 1) was too large to be based solely on increased volume of semen and fluids. Even though semen ejaculation and sexual behaviour were observed by 4 months, another 8 months were needed for complete testis development. In conclusion, male Tokara goat may acquire some reproductive ability by 4 months of age but development of the testis continues to 12 months. For establishing planned breeding system of this breed, separation of male kid from its mother or other does should occur at 3 months. References Abi Saab, S., Sleiman, F.T., Nassar, K.H., Chemaly, I., El-Skaff, R., Implications of high and low protein levels on puberty and sexual maturity of growing male goat kids. Small Rum. Res. 25, Ahmad, N., Noakes, D.E., Sexual maturity in British breeds of goat kids. Br. Vet. J. 152, Bilaspuri, G.S., Singh, K., Developmental changes in body weight and testicular characteristics in Malabari goat kids. Theriogenology 37, Chakraborty, P.K., Stuart, L.D., Brown, J.L., Puberty in the male Nubian goat: Serum concentrations of LH, FSH and testosterone from birth through puberty and semen characteristics at sexual maturity. Anim. Reprod. Sci. 20, Daudu, C.S., Spermatozoa output, testicular sperm reserve and epididymal storage capacity of the Red Sokoto goats indigenous to northern Nigeria. Theriogenology 21, Deveson, S., Forsyth, I.A., Arendt, J., Reterdation of pubertal development by prenatal long days in goat kids born in autumn. J. Reprod. Fert. 95, Elwishy, A.B., Elsawaf, S.A., Development of sexual activity in male Damascus goats. Indian J. Anim. Sci. 41, Louw, D.F.J., Joubert, D.M., Puberty in the male Dorper sheep and Boer goat. S. Afr. J. Agric. Sci. 7, Madani, M.O.K., Rahal, M.S., Puberty in Libyan male goats. Anim. Reprod. Sci. 17, Manda, M., Availability of Tokara goats for laboratory animals. Exp. Herbivora (Jpn) 11, Nwoha, P.U., A comparative study of the correlation of weights of the body, testis, and epididymis in the goat, ram, bat and rat. Acta Anat. Nippon. 70, Yao, T.S., Eaton, O.N., Postnatal growth and histological development of reproductive organs in male goats. Am. J. Anat. 95,