Skip to main content

Plasma insulin-like growth factor-I, testosterone and morphological changes in the growth of captive agile gibbons (Hylobates agilis) from birth to adolescence

Primates volume 44, pages 273–280 (2003)Cite this article

Abstract

We examined growth changes in concentrations of plasma insulin-like growth factor-1 (IGF-1) and testosterone, and somatometric parameters in two captive male agile gibbons from birth to about 4 years of age, to examine the evolution of growth patterns in primates. Plasma IGF-1 concentrations in agile gibbons generally increased with age with values ranging from 200 to 1,100 ng/ml. The growth profiles in plasma IGF-1 in the gibbons were similar to those reported for chimpanzees. The highest concentrations of plasma testosterone (230 and 296 ng/dl) were observed within the first 0.3 years from birth, then the concentrations rapidly decreased and fluctuated below 100 ng/dl. Continuously higher IGF-1 concentrations were observed after 2.6 and 3.5 years of age. The profiles of plasma testosterone in these gibbons also resembled those of other primates including humans. However, their plasma testosterone levels in both neonate and adult stages (60 ng/dl) were lower than those reported for macaques and chimpanzees of respective stages. The obtained growth profiles of plasma IGF-1 and testosterone suggest that the adolescent phase starts around 2.6 or 3.5 years of age in male agile gibbons. The growth trend in many morphological parameters including body weight showed a linear increase without a significant growth spurt at approximately the onset of puberty. Head length and first digit length had reached a plateau during the study period. Brachial index, which indicates the relative length of forearm to upper arm, significantly increased gradually through the growth period. This result indicates that forearm becomes relatively longer than the upper arm with growth, which may be an evolutionary adaptation for brachiation.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1A–D.
Fig. 2A–F.
Fig. 3A, B.

References

  • Araki K, Samekawa T, Furukawa N, Mochizuki Y, Nishi H (1989) Breeding and hand-rearing the white-handed gibbon, Hylobates lar, and the concolor gibbon, hylobates concolor at Takarazuka Zool and Bot Gardens. (in Japanese) J Jpn Assoc Zool Gardens Aquariums 31:41–46

  • Ashley-Montagu MF (1960) A handbook of anthropometry. Thomas, Springfied

  • Bogin B (1999) Evolutionary perspective on human growth. Annu Rev Anthropol 28:109–153

    Article  CAS  PubMed  Google Scholar 

  • Coelho J, A.M. (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to 8 years of age. In: Nonhuman primate models for human growth and development. Liss, New York, pp 125–159

  • Copeland KC, Kuehl TJ, Castracane VD (1982) Pubertal endocrinology of the baboon: elevated somatomedin-C/insulin-like growth factor I at puberty. J Clin Endocrinol Metab 55:1198–1201

    CAS  PubMed  Google Scholar 

  • Copeland KC, Johnson DM, Kuehl TJ, Castracane VD (1984) Estrogen stimulates growth hormone and somatomedin-C in castrate and intact female baboons. J Clin Endocrinol Metab 58:698–703

    CAS  PubMed  Google Scholar 

  • Copeland KC, Eichberg JW, Parker CR Jr , Bartke A (1985) Puberty in the chimpanzee: somatomedin-C and its relationship to somatic growth and steroid hormone concentrations. J Clin Endocrinol Metab 60:1154–1985

    CAS  PubMed  Google Scholar 

  • Forest MG, Sizonenko PC, Cathiard AM, Bertrand J (1974) Hypophyso-gonadal function in humans during the first year of life. 1. Evidence for testicular activity in early infancy. J Clin Endocrinol Metab 53:819–828

    CAS  Google Scholar 

  • Geissmann T (1991) Reassessment of age of sexual maturity in gibbons (Hylobates spp.). Am J Primatol 23:11–22

    Google Scholar 

  • Hamada Y (1994) Standard growth patterns and variations in growth patterns of the Japanese monkeys (Macaca fuscata) based on an analysis by the spline function method. Anthropol Sci 102 [Suppl]: 57–76

    Google Scholar 

  • Humbel RE (1984) Insulin-like growth factors, somatomedins, and multiplication stimulation activity: chemistry. In: Li Ch (ed.) Hormonal proteins and peptides. Academic Press, Orlando, pp 57–79

  • Iwamoto M (1971) Morphological studies of Macaca fuscata (VI): somatometry. Primates 12:151–174

    Google Scholar 

  • Jungers WL (1984) Scaling of the hominoid locomotor skeleton with special reference to lesser apes. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N (eds) The lesser apes. Edinburgh University Press, Edinburgh, pp 146–169

  • Katharina MM, Ida MM, Niels ES (2000) A possible role for reproductive hormones in newborn boys: progressive hypogonadism without the postnatal testosterone peak. J Clin Endocrinol Metab 85:4905–4907

    PubMed  Google Scholar 

  • Kimura K (1979) Growth. (in Japanese) Yuzankaku Shuppan, Tokyo

  • Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60

    Google Scholar 

  • Linke K (1988) Beobachtungen zur Entwicklung von 3 Gibbons bei einer Handaufzucht und 2 kombinierten Aufzuchten. Zool Garten N F Jena 58:229–250

    Google Scholar 

  • Marson J, Meuris S, Cooper RW, Jouannet P (1991) Puberty in the male chimpanzee: time-related variations in luteinizing hormone, follicle-stimulating hormone, and testosterone. Biol Reprod 44:456–460

    CAS  PubMed  Google Scholar 

  • Martin CR (1985) Endocrine Physiology. Oxford University Press, New York

  • Martin R, Saller K (1957) Lehrbuch der Anthropologie. Fischer, Stuttgart

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

    CAS  Google Scholar 

  • Meusy-Dessolle N, Dang DC (1985) Plasma concentrations of testosterone, dihydrotestosterone, Δ4−androstenedione, dehydroepiandrosterone and oestradiol-17 β in the crab-eating monkey (Macaca fascicularis) from birth to adulthood. J Reprod Fertil 74:347–359

    CAS  PubMed  Google Scholar 

  • Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, London

  • Nigi H, Tiba T, Yamamoto S, Floescheim Y, Ohsawa N (1980) Sexual maturation and seasonal changes in reproductive phenomena of male Japanese monkeys (Macaca fuscata) at Takasakiyama. Primates 21:230–240

    Google Scholar 

  • Plant TM (1985) A study of the role of the postnatal testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey (Macaca mulatta). Endocrinology 116:1341–1350

    CAS  PubMed  Google Scholar 

  • Plant TM, Zorub DS (1982) The role of nongonadal restraint of gonadotropin secretion in the delay of the onset of puberty in the rhesus monkey (Macaca mulatta). J Anim Sci 55:43–55

    PubMed  Google Scholar 

  • Roonwall ML, Mohnot SM (1977) Primates of South Asia: ecology, sociobiology and behavior. Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Sanayama K, Cho M, Ushihisa H, Sato K, Nishioka T, Sasaki N, Niimi H, Nakashima H (1984) Measurement of somatomedin-C in plasma by radioimmunoassay; basic evaluation and clinical applications (in Japanese). Clin Endocrinol 32:567–571

    CAS  Google Scholar 

  • Sawina NW, Orpachowa WR (1981) Haltung und Zucht von Weisshandgibbons (Hylobates lar L., 1771) im Leningrader Zoo. Zool Garten N F Jena 51:343–352

    Google Scholar 

  • Shohoji T, Sasaki H (1985) An aspect of growth analysis of weight in Savannah baboon. Growth 49:500–509

    CAS  PubMed  Google Scholar 

  • Smith BH (1992) Life history and the evolution of human maturation. Evol Anthropol 1:134–142

    Google Scholar 

  • Smith BH, Crummett TL, Brandt KL (1994) Ages of eruption of Primate teeth: a compendium for aging individuals and comparing life histories. Yearb Phys Anthropol 37:177–231

    Google Scholar 

  • Suzuki J, Ohkura S, Hayakawa S, Hamada Y (2000) Time series analysis of plasma insulin-like growth factor-I and gonadal steroids in adolescent Japanese macaques (Macaca fuscata). J Reprod Dev 46:157–166

    Article  CAS  Google Scholar 

  • Suzuki J, Ishida T, Ohkura S, Udono T, Hayasaka I, Arsaithamkul V (2001) Plasma IGF-1 levels in the great and lesser apes. In: The 18th Congress of the International Primatological Society, pp 485

  • Tachibana K, Suwa K, Yokoya S, Hizuka N, Tanaka T, Hibi I, Fujieda K, Miyachi Y, Irie M (1993) Clinical evaluation of the total IGF-I assay kit (Sm-C [Scitech Research]) (in Japanese). Clin Endocrinol 41:915–923

    Google Scholar 

  • Tachibana K, Suwa K, Yokoya S, Hizuka N, Tanaka T, Hibi I, Fujieda K, Miyachi Y, Irie M (1994) Clinical evaluation of the total somatomedin-C (total IGF-I) assay kit (in Japanese). Clin Endocrinol 42:73–79

    Google Scholar 

  • Watts ES (1985) Adolescent growth and development of monkeys, apes and humans. In: Watts ES (ed) Nonhuman primate models for human growth and development. Liss, New York, pp 41–65

  • Watts ES, Gavan JA (1982) Postnatal growth of nonhuman primates: the problem of the adolescent spurt. Hum Biol 54:53–70

    CAS  PubMed  Google Scholar 

  • Wilson ME (1986) Gonadal steroids influence serum somatomedin-C concentrations in prepubertal female rhesus monkeys. Endocrinology 119:666–671

    CAS  PubMed  Google Scholar 

  • Wilson ME, Schwartz SM, Walker ML, Gordon TP (1984) Oestradiol and somatomedin-C influence body weight patterns in premenarchial rhesus monkeys housed outdoors. J Endocrinol 102:311–317

    CAS  PubMed  Google Scholar 

  • Winter JS, Faiman C, Hobson WC, Prasad AV, Reyes FI (1975) Pituitary-gonadal relations in infancy. I. Patterns of serum gonadotropin concentrations from birth to four years of age in man and chimpanzee. J Clin Endocrinol Metab 40:545–551

    CAS  PubMed  Google Scholar 

  • Yoshida T (1994) Comparison between non-human primates and humans. II. Characterization of growth patterns (in Japanese). Hum Sci 7:52-77

    Google Scholar 

Download references

Acknowledgements

We would like to thank the staff of the Center for Human Evolution Modeling Research, Primate Research Institute of Kyoto University, for their assistance throughout the study. We are also grateful to Prof. S. Sri Kantha, of the Center, for his valuable criticism, and to Ms. Y. Suzuki for her technical assistance.

Author information

Affiliations

  1. Center for Human Evolution Modeling Research, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan

    Juri Suzuki, Akino Kato, Norihiko Maeda & Chihiro Hashimoto

  2. Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, Aichi, Japan

    Makiko Uchikoshi, Toshiaki Mizutani, Chisato Doke & Tetsuro Matsuzawa

Authors
  1. Juri Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akino Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Norihiko Maeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chihiro Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Makiko Uchikoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Toshiaki Mizutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chisato Doke
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tetsuro Matsuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juri Suzuki.

About this article

Cite this article

Suzuki, J., Kato, A., Maeda, N. et al. Plasma insulin-like growth factor-I, testosterone and morphological changes in the growth of captive agile gibbons (Hylobates agilis) from birth to adolescence. Primates 44, 273–280 (2003). https://doi.org/10.1007/s10329-003-0044-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-003-0044-x

Keywords

  • Gibbon
  • Growth
  • Insulin-like growth factor-1
  • Somatometry
  • Testosterone