Skip to main content
SpringerLink
Log in

Seasonal changes in the spermatogenic epithelium of adult Japanese macaques (Macaca fuscata fuscata)

  • Published:
Primates Aims and scope Submit manuscript

Abstract

A histological study was undertaken to clarify seasonal changes in the spermatogenic epithelium of Japanese macaques. Testicular tissue samples were excised by biopsies from five adult laboratory-maintained males in mating and non-mating seasons. The samples were fixed with Bouin's solution, embedded in paraffin, and stained with PAS and hematoxylin. Microscopic observations on cross-sections of seminiferous tubules revealed that the seminiferous epithelium in the mating season was thicker than in the non-mating season. PAS-stained granules were found in some of the dark A-type spermatogonia, which significantly increased in the non-mating season. Spermatids of the steps preceding the appearance of the acrosomic cap in stages I to III were observed significantly more often than those in the step coinciding with the formation of the acrosomic cap in stage IV. In stage I, the ratio of mature spermatids or spermatozoa to immature spermatids in the mating season was higher than that in the non-mating season. These findings suggest that spermiogenesis, as well as spermatocytogenesis, is inhibited in the non-mating season.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ashley, D. J. B., 1990.Evans' Histological Appearances of Tumors. Churchill Livingstone, Edinburgh.

    Google Scholar 

  • Cavicchia, J. C. &A. Dym, 1978. Ultrastructural characteristics of monkey spermatogonia and preleptotene spermatocytes.Biol. Reprod., 18: 219–228.

    Article  CAS  PubMed  Google Scholar 

  • Clermont, Y., 1963. The cycle of the seminiferous epithelium in man.Amer. J. Anat., 112: 35–51.

    Article  CAS  PubMed  Google Scholar 

  • ————, 1966. Spermatogenesis in man: a study of the spermatogonial population.Fetil. Steril., 17: 705–721.

    CAS  Google Scholar 

  • ————, 1969. Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops).Amer. J. Anat., 126: 57–72.

    Article  CAS  PubMed  Google Scholar 

  • ———— &M. Antar, 1973. Duration of the cycle of the seminiferous epithelium and the spermatogonial renewal in the monkeyMacaca arctoides.Amer. J. Anat., 136: 153–166.

    Article  CAS  PubMed  Google Scholar 

  • ———— &P. Leblond, 1955. Spermiogenesis of man, monkey, ram and other mammals as shown by the “periodic acid-Schiff” technique.Amer. J. Anat., 96: 229–253.

    Article  CAS  PubMed  Google Scholar 

  • ———— & ————, 1959. Differentiation and renewal of spermatogonia in the monkey,Macacus rhesus.Amer. J. Anat., 104: 237–274.

    Article  CAS  PubMed  Google Scholar 

  • Conaway, C. H., 1969. Annual testis cycle of the green monkey (Cercopithecus aethiops) on St. Kitts, West Indies.J. Mammal., 50: 833–835.

    Google Scholar 

  • Dixson, A. F., 1987a. Observations on the evolution of the genitalia and copulatory behavior in male primates.J. Zool. London, 213: 423–443.

    Google Scholar 

  • ————, 1987b. Baculum length and copulatory behavior in primates.Amer. J. Primatol., 13: 51–60.

    Article  Google Scholar 

  • Du Mond, F. V. &T. C. Hutchinson, 1967. Squirrel monkey reproduction: the “fatted” male phenomenon and seasonal spermatogenesis.Science, 158: 1067–1070.

    PubMed  Google Scholar 

  • Dym, M. &U. C. Cavicchia, 1978. Functional morphology of the testis.Biol. Reprod., 18: 1–15.

    Article  CAS  PubMed  Google Scholar 

  • Fa, J. E., 1989. The genusMacaca: a review of taxonomy and evolution.Mammal Rev., 19: 45–81.

    Google Scholar 

  • Fooden, J., 1976. Provisional classification and key to living species of macaques (Primates:Macaca).Folia Primatol., 25: 225–236.

    CAS  PubMed  Google Scholar 

  • Glick, B. B., 1979. Testicular size, testosterone level, and body weight in maleMacaca radiata.Folia Primatol., 32: 268–289.

    Google Scholar 

  • Gondos, B. &A. Zemjanis, 1970. Fine structure of spermatogonia and intercellular bridges inMacaca nemestrina.J. Morphol., 131: 431–446.

    Article  CAS  PubMed  Google Scholar 

  • Harvey, P. H. &A. H. Harcourt, 1984. Sperm competition, testes size, and breeding system in primates. In:Sperm Competition and the Evolution of Animal Mating System,R. L. Smith (ed.), Academic Press, Orlando, pp. 589–600.

    Google Scholar 

  • Heller, C. G. &V. Clermont, 1963. Spermatogenesis in man: an estimate of its duration.Science, 140: 184–186.

    CAS  PubMed  Google Scholar 

  • Lancaster, J. B. &I. B. Lee, 1965. The annual reproductive cycle in monkeys and apes. In:Primate Behaviour, Vol. 1, I. deVore (ed.), Holt, Rinehart, & Winston, New York, pp. 486–513.

    Google Scholar 

  • Lincoln, G. A., 1992. Biology of seasonal breeding in deer. In:The Biology of Deer,R. D. Brown (ed.), Springer-Verlag, New York, pp. 565–574.

    Google Scholar 

  • Matsubayashi, K. &T. Enomoto, 1983. Longitudinal studies on annual changes in plasma testosterone, body weight and spermatogenesis in adult Japanese monkeys (Macaca fuscata fuscata) under laboratory conditions.Primates, 24: 521–529.

    CAS  Google Scholar 

  • ———— &K. Mochizuki, 1982. Growth of male reproductive organs with observation of their seasonal morphologic changes in the Japanese monkey (Macaca fuscata).Jap. J. Vet. Sci., 44(6): 891–902.

    CAS  Google Scholar 

  • ————,G. Watanabe, K. Taya, Y. Katakai, S. Sasamoto, J. Suzuki, &M. Nozaki, 1991. Seasonal changes in plasma concentrations of immunoreactive inhibin and testicular activity in male Japanese monkeys.Biol. Reprod., 44: 822–826.

    Article  CAS  PubMed  Google Scholar 

  • Nagato, Y., T. Enomoto, &K. Matsubayashi, 1994. Observation on the cycle of the seminiferous epithelium in the Japanese macaque (Macaca fuscata) using semithin sections.Primates, 35: 455–464.

    Google Scholar 

  • Nigi, H., 1975. Sexual maturity of male Japanese monkeys (Macaca fuscata) in Shiga A troop.Physiol. Ecology, 16: 47–53. (in Japanese)

    Google Scholar 

  • Plant, T. M., D. Zumpe, M. Sauls, &P. Michael, 1974. An annual rhythm in the plasma testosterone of adult male rhesus monkeys maintained in the laboratory.J. Endocrin., 62: 403–404.

    CAS  Google Scholar 

  • Short, R. V., 1979. Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes.Adv. Study Behav., 9: 131–158.

    Google Scholar 

  • Tiba, T., 1981. Jahreszeirliche schwankungen der spermatogenese des Japanischen makaken (Macaca fuscata) in gefangenschaft, insbesondere im vergleich mit freilebendern gruppen.Z. Saugetierekunde, 46: 352–363.

    Google Scholar 

  • ————, &I. Kita, 1990. Undifferentiated spermatogonia and their role in the seasonally fluctuating spermatogenesis in ferretMustela putorius furo (Mammalia).Zool. Anz., 224: 140–155.

    Google Scholar 

  • ———— & ————, 1991. Undifferentiated spermatogonia and their role in the seasonally fluctuating spermatogenesis in the mink,Mustela Vison.Anat. Histol. Embryol., 20: 118–128.

    CAS  PubMed  Google Scholar 

  • ———— &H. Nigi. 1975. Unregelmässig aufgebaute zellgemeinschaften des samenepithels beim free-ranging Japanischen makak (Macaca fuscata) in der paarungszeit.Primates, 16: 379–398.

    Article  Google Scholar 

  • ———— & ————, 1980. Jahreszeitliche schwankung in der spermatogenese beim “free-ranging” Japanischen makak (Macaca fuscata).Zool. Anz., 204: 371–387.

    Google Scholar 

  • Uehara, S., 1975. The importance of the temperate forest elements among woody food plants utilized by Japanese monkeys and its possible historical meaning for the establishment of the monkey's range. In:Contemporary Primatology,S. Kondo,M. Kawai, &A. Ehara (eds.), S. Karger, Basel, pp. 392–400.

    Google Scholar 

  • Verrell, P. A., 1992. Primate penile morphologies and social systems: further evidence for an association.Folia Primatol., 59: 114–120.

    CAS  PubMed  Google Scholar 

  • Wickings, E. J. &E. Nieschlag, 1980. Seasonality in endocrine and exocrine testicular function of the adult rhesus monkey (Macaca mulatta) maintained in a controlled laboratory environment.Int. J. Androl., 3: 87–104.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Morphology, Tokai University School of Medicine, Bohseidai, Isehara, 259-11, Kanagawa, Japan

    Tomoo Enomoto, Yasukazu Nagato & Mayumi Nakano

  2. Primate Research Institute, Kyoto University, Inuyama, 484, Aichi, Japan

    Kiyoaki Matsubayashi

Authors
  1. Tomoo Enomoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kiyoaki Matsubayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasukazu Nagato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mayumi Nakano
    View author publications

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Enomoto, T., Matsubayashi, K., Nagato, Y. et al. Seasonal changes in the spermatogenic epithelium of adult Japanese macaques (Macaca fuscata fuscata). Primates 35, 465–472 (1994). https://doi.org/10.1007/BF02381955

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02381955

Key Words

Search

Navigation