Skip to main content
Log in

Testosterone levels among Aché hunter-gatherer men

A functional interpretation of population variation among adult males

  • Published:
Human Nature Aims and scope Submit manuscript

Abstract

Salivary testosterone levels were measured in a population of New World indigenous adult hunter-gatherer males in order to compare circulating levels of free unbound bioactive steroid with those previously reported among Boston and nonwestern males. The study population consisted of adult Aché hunter-gatherer males (n=45) living in eastern Paraguay. Morning and evening salivary testosterone levels (TsalA.M.; TsalP.M.) among the Aché were considerably lower than western values (Boston) and even lower than other previously reported nonwestern populations (Efe, Lese, Nepalese). No association was observed between height, weight, or age and salivary testosterone levels within the Aché group, although older men (ages>40) were poorly represented in the study sample. Nevertheless, a mild correlation was observed between Aché TsalA.M. levels and BMI (r=0.133,p=0.0725). Comparison of Aché values with those for other populations confirms the prevalence of significant interpopulational variation in testosterone levels among adult males. Interpopulational variation in male testosterone is not as great, however, as has been documented for ovarian steroids among females, nor is it likely that such variation reflects differences in male fecundity. Nevertheless, such interpopulational variation in salivary testosterone levels may have a functional significance in the regulation of protein anabolism in skeletal muscle, thereby affecting the overall energy budget of the organism. It is suggested that relative suppression of average testosterone may be adaptive under conditions of chronic energy shortage.

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

Access this article

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

  • Adamopoulos, D., D. M. Lawrence, N. Kapolla, L. Kontogeorgos, and H. H. McGarrigle 1984 Hormone Levels in the Reproductive System of Normospermic Men and Patients with Oligospermia and Varicocele.Journal of Clinical Endocrinology and Metabolism 59:447–452.

    Google Scholar 

  • Adlercreutz, H. 1990 Western Diet and Western Diseases: Some Hormonal and Biochemical Mechanisms and Association.Scandinavian Journal of Clinical and Laboratory Investigation 50:3–23.

    Google Scholar 

  • Ayers, J. W., Y. Komesu, T. Romani, and R. Ansbacher 1985 Anthropomorphic, Hormonal, and Psychologic Correlates of Semen Quality in Endurance-Trained Male Athletes.Fertility and Sterility 43:917–921.

    Google Scholar 

  • Aynsley-Green, A., M. Zachmann, and A. Prader 1976 Interrelation of the Therapeutic Effects of Growth Hormone and Testosterone on Growth in Hypopituitarism.Journal of Pediatrics 89:992–999.

    Article  Google Scholar 

  • Bambino, T. H., and A. J. W. Hsueh 1981 Direct Inhibitory Effect of Glucocorticoids upon Testicular Luteinizing Hormone Receptor and Steroidogenesis in vivo and in vitro.Endocrinology 108:2142–2148.

    Google Scholar 

  • Beall, C. M., C. M. Worthman, J. Stallings, K. P. Strohl, G. M. Brittenham, and M. Barragan 1992 Salivary Testosterone Concentration of Aymara Men Native to 3600 m.Annals of Human Biology 19:67–78.

    Article  Google Scholar 

  • Bentley, G. R., A. M. Harrigan, B. Campbell, and P. T. Ellison 1993 Seasonal Effects on Salivary Testosterone Levels among Lese Males of the Ituri Forest, Zaire.American Journal of Human Biology 5:711–717.

    Article  Google Scholar 

  • Bergink, E. W., J. A. A. Geelen, and E. W. Turpijn 1985 Metabolism and Receptor Binding of Nandrolone and Testosterone under in vitro and in vivo Conditions.Acta Endocrinologica 110:31–37.

    Google Scholar 

  • Burris, A. S., R. V. Clark, D. J. Vantman, and R. J. Sherins 1988 A Low Sperm Concentration Does not Preclude Fertility in Men with Isolated Hypogonadotropic Hypogonadism after Gonadotropin Therapy.Fertility and Sterility 50(2):343–347.

    Google Scholar 

  • Butler, G. E., R. F. Walker, R. V. Walker, P. Teague, D. Riad-Fahmy, and S. G. Ratcliffe 1989 Salivary Testosterone Levels and the Progress of Puberty in the Normal Boy.Clinical Endocrinology 30:587–596.

    Google Scholar 

  • Butler, G. E., R. E. Sellar, R. F. Walker, M. Hendry, C. J. Kelnar, and F. C. Wu 1992 Oral Testosterone Undecanoate in the Management of Delayed Puberty in Boys: Pharmacokinetics and Effects on Sexual Maturation and Growth.Journal of Clinical Endocrinology and Metabolism 75:37–44.

    Article  Google Scholar 

  • Campbell, K. 1994 Blood, Urine, Saliva and Dip-Sticks: Experiences in Africa, New Guinea, and Boston. InHuman Reproductive Ecology: Interactions of Environment, Fertility, and Behavior, K. Campbell and J. W. Wood, eds. Pp. 312–330. Annals of the New York Academy of Sciences, Vol. 709.

  • Catz, D. S., L. M. Fischer, M. C. Moschella, M. L. Tobias, and D. B. Kelley 1992 Sexually Dimorphic Expression of a Laryngeal-Specific, Androgen-Regulated Myosin Heavy Chain Gene duringXenopus laevis Development.Developmental Biology 154:366–376.

    Article  Google Scholar 

  • Christiansen, K. 1991a Androgen and Estrogen Levels in Namibian Kavango Men.Homo 42:43–62.

    Google Scholar 

  • 1991b Serum and Saliva Sex Hormone Levels in !Kung San Men.American Journal of Physical Anthropology 86:37–44.

    Article  Google Scholar 

  • 1991c Sex Hormone Levels, Diet and Alcohol Consumption in Namibian Kavango Men.Homo 42:43–62.

    Google Scholar 

  • Cumming, D. C., M. E. Quigley, and S. S. C. Yen 1983 Acute Suppression of Circulating Testosterone Levels by Cortisol in Men.Journal of Clinical Endocrinology and Metabolism 57:671–673.

    Google Scholar 

  • Davidson, J. M., J. J. Chen, L. Crapo, G. D. Gray, W. J. Greenleaf, and J. A. Catania 1983 Hormonal Changes and Sexual Function in Aging Men.Journal of Clinical Endocrinology and Metabolism 57:71–77.

    Google Scholar 

  • Deslypere, J. P., and A. Vermeulen 1984 Leydig Cell Function in Normal Men: Effect of Age, Life-Style, Residence, Diet, and Activity.Journal of Clinical Endocrinology and Metabolism 59:955–962.

    Google Scholar 

  • Dorlochter, M., S. H. Astrow, and A. A. Herrera 1994 Effects of Testosterone on a Sexually Dimorphic Frog Muscle: Repeated in vivo Observations and Androgen Receptor Distribution.Journal of Neurobiology 25:897–916.

    Article  Google Scholar 

  • Eaton, S. B., M. C. Pike, R. V. Short, N. C. Lee, J. Trussell, R. A. Hatcher, J. W. Wood, C. M. Worthman, N. G. Blurton Jones, M. J. Konner, K. R. Hill, R. Bailey, and A. M. Hurtado 1994 Women’s Reproductive Cancers in Evolutionary Context.Quarterly Review of Biology 69:353–367.

    Article  Google Scholar 

  • Elia, M. 1992a Energy Expenditure in the Whole Body. InEnergy Metabolism: Tissue Determinants and Cellular Corollaries, J. M. Kinney and H. N. Tucker, eds. Pp. 19–59. New York: Raven Press.

    Google Scholar 

  • 1992b Organ and Tissue Contribution to Metabolic Rate. InEnergy Metabolism: Tissue Determinants and Cellular Corollaries, J. M. Kinney and H. N. Tucker, eds. Pp. 61–79. New York: Raven Press.

    Google Scholar 

  • Ellison, P. T. 1988 Human Salivary Steroids: Methodological Considerations and Applications in Physical Anthropology.Yearbook of Physical Anthropology 31:115–142.

    Article  Google Scholar 

  • 1990 Human Ovarian Function and Reproductive Ecology: New Hypotheses.American Anthropologist 92:933–952.

    Article  Google Scholar 

  • 1994 Advances in Reproductive Ecology.Annual Review of Anthropology 23:255–275.

    Article  Google Scholar 

  • Ellison, P. T., and C. Lager 1986 Moderate Recreational Running is Associated with Lowered Salivary Progesterone Profiles in Women.American Journal of Obstetrics and Gynecology 154:1000–1003.

    Google Scholar 

  • Ellison, P. T., and C. Panter-Brick 1995 Salivary Testosterone Levels among Tamang and Kami Males of Central Nepal.International Journal of Andrology, in press.

  • Ellison, P. T., S. F. Lipson, and M. D. Meredith 1989 Salivary Testosterone Levels in Males from the Ituri Forest of Zaire.American Journal of Human Biology 1:21–24.

    Article  Google Scholar 

  • Ellison, P. T., C. Panter-Brick, S. F. Lipson, and M. T. O’Rourke 1993 The Ecological Context of Human Ovarian Function.Human Reproduction 8:2248–2258.

    Google Scholar 

  • Ellison, P. T., N. R. Peacock, and C. Lager 1986 Salivary Progesterone and Luteal Function in Two Low-Fertility Populations of Northeast Zaire.Human Biology 58:473–483.

    Google Scholar 

  • 1989 Ecology and Ovarian Function among Lese Women of the Ituri Forest, Zaire.American Journal of Physical Anthropology 78:519–526.

    Article  Google Scholar 

  • Forbes, G. B. 1985 The Effect of Anabolic Steroids on Lean Body Mass: The Dose Response Curve.Metabolism 34:571–573.

    Article  Google Scholar 

  • Galard, R., M. Antolin, R. Catalan, P. Magana, S. Schwartz, and J. M. Castellanos 1987 Salivary Testosterone Levels in Infertile Men.International Journal of Andrology 10:597–601.

    Google Scholar 

  • Glass, R. H. 1991 Infertility. InReproductive Endocrinology: Physiology, Pathophysiology, and Clinical Management, S. Samuel, C. Yen, and R. B. Jaffe, eds. Pp. 689–709. Philadelphia: W. B. Saunders.

    Google Scholar 

  • Griggs, R. C., W. Kingston, R. F. Jozefowicz, B. E. Herr, G. Forbes, and D. Halliday 1989 Effect of Testosterone on Muscle Mass and Muscle Protein Synthesis.Journal of Applied Physiology 66:498–503.

    Google Scholar 

  • Guerra-García, R., A. Velásquez, and J. Coyotupa 1969 A Test of Endocrine Gonadal Function in Men: Urinary Testosterone after the Injection of HCG, Part II. A Different Response of the High Altitude Native.Journal of Clinical Endocrinology 29:179–182.

    Google Scholar 

  • Handelsman, D. J., A. J. Conway, L. M. Boylan, D. K. Yue, and J. R. Turtle 1985 Testicular Function and Glycemic Control in Diabetic Men. A Controlled Study.Andrologia 17:488–496.

    Article  Google Scholar 

  • Hawkes, K., H. Kaplan, K. Hill, and M. Hurtado 1987 Aché at the Settlement: Contrasts between Farming and Foraging.Human Ecology 15:133–161.

    Article  Google Scholar 

  • Hayes R. B., F. H. de Jong, J. Raatgever, J. Bogdanovicz, F. H. Schroeder, P. van der Maas, K. Oishi, and O. Yoshida 1992 Physical Characteristics and Factors Related to Sexual Development and Behaviour and the Risk for Prostatic Cancer.European Journal of Cancer Prevention 1:239–245.

    Article  Google Scholar 

  • Henriksson, J. 1992 Energy Metabolism in Muscle: Its Possible Role in the Adaptation to Energy Deficiency. InEnergy Metabolism: Tissue Determinants and Cellular Corollaries, J. M. Kinney and H. N. Tucker, eds. Pp. 345–365. New York: Raven Press.

    Google Scholar 

  • Hill, K., and K. Hawkes 1983 Neotropical Hunting among the Aché of Eastern Paraguay. InAdaptive Responses of Native Amazonians, R. B. Hames and W. T. Vickers, eds. Pp. 139–188. New York: Academic Press.

    Google Scholar 

  • Hill, K., K. Hawkes, M. Hurtado, and H. Kaplan 1984 Seasonal Variance in the Diet of Ache Hunter-Gatherers in Eastern Paraguay.Human Ecology 12:101–135.

    Article  Google Scholar 

  • Hill, K. R., and A. M. Hurtado 1995Aché Life History: The Ecology and Demography of a Foraging People. New York: Aldine de Gruyter.

    Google Scholar 

  • Isselbacher, K. J., ed. 1994Harrison’s Principles of Internal Medicine, thirteenth edition. New York: McGraw-Hill, Health Professions Division.

    Google Scholar 

  • Jasienska, G., and P. T. Ellison 1993 Heavy Workload Impairs Ovarian Function in Polish Peasant Women.American Journal of Physical Anthropology Supplement 16:117–118.

    Google Scholar 

  • Johnson, L. 1989 Evaluation of the Human Testis and Its Age-Related Dysfunction.Progress in Clinical Biological Research 302:35–60.

    Google Scholar 

  • Johnson, L., J. S. Grumbles, A. Bagheri, and C. S. Petty 1990 Increased Germ Cell Degeneration during Postprophase of Meiosis Is Related to Increased Serum Follicle-Stimulating Hormone Concentrations and Reduced Daily Sperm Production in Aged Men.Biology of Reproduction 42:281–287.

    Article  Google Scholar 

  • Kent, J. D., S. R. Kimball, and L. S. Jefferson 1991 Effect of Diabetes and Insulin Treatment of Diabetic Rats on Total RNA, poly(A) + RNA, and mRNA in Skeletal Muscle.American Journal of Physiology 260:C409–416.

    Google Scholar 

  • Kinney, J. M., and H. N. Tucker, eds. 1992Energy Metabolism: Tissue Determinants and Cellular Corollaries. New York: Raven Press.

    Google Scholar 

  • Knussmann, R., and A. Sperwien 1988 Relations between Anthropometric Characteristics and Androgen Hormone Levels in Healthy Young Men.Annals of Human Biology 15:131–142.

    Article  Google Scholar 

  • Korenchevsky, V. 1961Physiological and Pathological Aging. New York: Hafner.

    Google Scholar 

  • Krieg, M., R. Nass, and S. Tunn 1993 Effect of Aging on Endogenous Level of 5alpha-dihydrotestosterone, Testosterone, Estradiol, and Estrone in Epithelium and Stroma of Normal and Hyperplastic Human Prostate.Journal of Clinical Endocrinology and Metabolism 77:375–381.

    Article  Google Scholar 

  • Kuoppasalmi, K., H. Näveri, S. Rehunen, and M. Härkönen 1976 Effect of Strenuous Anaerobic Running Exercise on Plasma Growth Hormone, Cortisol, Luteinizing Hormone, Testosterone, Androstenedione, Estrone and Estradiol.Journal of Steroid Biochemistry 7:823–829.

    Article  Google Scholar 

  • Kuoppasalmi, K., H. Näveri, M. Härkönen, and H. Adlercreutz 1980 Plasma Cortisol, Androstenedione, Testosterone and Luteinizing Hormone in Running Exercise of Different Intensities.Scandinavian Journal of Clinical Laboratory Investigation 40:403–409.

    Google Scholar 

  • Lenton, E. A., C. H. Gelsthorp, and R. Harper 1988 Measurement of Progesterone in Saliva: Assessment of the Normal Fertile Range using Spontaneous Conception Cycles.Clinical Endocrinology 38:637–646.

    Google Scholar 

  • Lincoln, G. A. 1971 The Seasonal Reproductive Changes in the Red Deer Stag(Cervus elaphus).Journal of Zoology, London 163:105–123.

    Article  Google Scholar 

  • Lipson, S. F., and P. T. Ellison 1989 Development of the Protocols for the Application of Salivary Steroid Analyses to Field Conditions.American Journal of Human Biology 1:249–255.

    Article  Google Scholar 

  • Loucks, A. B., and S. M. Horvath 1984 Exercise-Induced Stress Responses of Amenorrheic and Eumenorrheic Runners.Journal of Clinical Endocrinology and Metabolism 59:1109–1120.

    Google Scholar 

  • Luisi, M. F., F. Franchi, S. Bianchi, G. Gravina, and A. Podesta 1987 Radio-Immunoassay of Salivary Progesterone for Monitoring Ovarian Function in Female Infertility.Annales de Biologie Clinique 45: 449–452.

    Google Scholar 

  • Max, S. R., and J. Toop 1983 Androgens Enhance in vivo 2-Deoxyglucose Uptake by Rat Striated Muscle.Endocrinology 113:119–126.

    Google Scholar 

  • Morville, R., P. C. Pesquies, C. Y. Guezennec, B. D. Serrurier, and M. Guignard 1979 Plasma Variations in Testicular and Adrenal Androgens during Prolonged Physical Exercise in Man.Annales d’Endocrinologie 40:501–510.

    Google Scholar 

  • Navarro, M. A., J. L. Bonnin, and C. M. Villabona 1986 Salivary Testosterone: Relationship to Total and Free Serum Testosterone.Clinical Chemistry 32:237.

    Google Scholar 

  • Navarro, M. A., J. M. Gomez, C. M. Villabona, and R. Bonnin 1987 Salivary Testosterone: A Good Measure to Reflect Free Testosterone.Archives of Internal Medicine 147:1189.

    Article  Google Scholar 

  • Panter-Brick, C., D. S. Lotstein, and P. T. Ellison 1993 Seasonality of Reproductive Function and Weight Loss in Rural Nepali Women.Human Reproduction 8:684–690.

    Google Scholar 

  • Papadimas, J., and S. Mantalenakis 1983 Hormone Profile in Infertile Men.Archives of Andrology 11:73–80.

    Google Scholar 

  • Pestell, R. G., D. M. Hurley, and R. Vandongen 1989 Biochemical and Hormonal Changes during a 1000 km Ultramarathon.Clinical and Experimental Pharmacology and Physiology 16:353–361.

    Article  Google Scholar 

  • Powers, M. L., and J. R. Florini 1975 A Direct Effect of Testosterone on Muscle Cells in Tissue Culture.Endocrinology 97:1043–1047.

    Google Scholar 

  • Pusateri, D. J., W. T. Roth, J. K. Ross, and T. D. Shultz 1990 Dietary and Hormonal Evaluation of Men at Different Risks for Prostate Cancer: Plasma and Fecal Hormone-Nutrient Interrelationships.American Journal of Clinical Nutrition 51:371–377.

    Google Scholar 

  • Ravussin, E., and R. Rising 1992 Daily Energy Expenditure in Humans: Measurements in a Respiratory Chamber and by Doubly Labeled Water. InEnergy Metabolism: Tissue Determinants and Cellular Corollaries, J. M. Kinney and H. N. Tucker, eds. Pp. 81–96. New York: Raven Press.

    Google Scholar 

  • Read, G. F. 1993 Status Report on Measurement of Salivary Estrogens and Androgens.Annals of the New York Academy of Sciences 694:146–160.

    Article  Google Scholar 

  • Regnier, M., and A. A. Herrera 1993 Differential Sensitivity to Androgens within a Sexually Dimorphic Muscle of Male Frogs(Xenopus laevis).Journal of Neurobiology 24:1215–1228.

    Article  Google Scholar 

  • Remes, K., K. Kuoppasalmi, and H. Adlercreutz 1979 Effect of Long-Term Physical Training on Plasma Testosterone, Androstenedione, Luteinizing Hormone and Sex Hormone-Binding Globulin Capacity.Scandinavian Journal of Clinical Laboratory Investigation 39:743–749.

    Google Scholar 

  • Roberts, A. C., R. D. McClure, R. I. Weiner, and G. A. Brooks 1993 Overtraining Affects Male Reproductive Status.Fertility and Sterility 60:686–692.

    Google Scholar 

  • Ross, R. K., L. Bernstein, R. A. Lobo, H. Shimizu, F. Z. Stanczyk, M. C. Pike, and B. E. Henderson 1992 5-Alpha-Reductase Activity and Risk of Prostate Cancer among Japanese and US White and Black Males.Lancet 339:887–889.

    Article  Google Scholar 

  • Sawhney, R. C., P. C. Chhabra, A. S. Malhotra, T. Singh, S. S. Riar, and R. M. Rai 1985 Hormone Profiles at High Altitude in Man.Andrologia 17:178–184.

    Article  Google Scholar 

  • Schurmeyer, T., and E. Nieschlag 1982 Salivary and Serum Testosterone under Physiological and Pharmacological Conditions. InImmunoassays of Steroids in Saliva, G. F. Read, ed. Pp. 203–209. Cardiff, Wales: Alpha Omega.

    Google Scholar 

  • Semple, C. G., C. E. Gray, and G. H. Beastall 1988 Androgen Levels in Men with Diabetes Mellitus.Diabetic Medicine 5:122–125.

    Article  Google Scholar 

  • Skolnick, A. A. 1992 Is “Male Menopause” Real or Just an Excuse?Journal of the American Medical Association 268:2486.

    Article  Google Scholar 

  • Tanner, J. M. 1978Fetus into Man: Physical Growth from Conception to Maturity. Harvard University Press.

  • Tanner, J. M., R. H. Whitehouse, P. C. R. Hughes, and B. S. Carter 1976 Relative Importance of Growth Hormone and Sex Steroids for the Growth at Puberty of Trunk Length, Limb Length, and Muscle Width in Growth Hormone-Deficient Children.Journal of Pediatrics 89:1000–1008.

    Article  Google Scholar 

  • Van der Walt, L. A., E. N. Wilmsen, and T. Jenkins 1978 Unusual Sex Hormone Patterns among Desert-Dwelling Hunter-Gatherers.Journal of Clinical Endocrinology and Metabolism 46:658–663.

    Google Scholar 

  • Walker, R. F., D. W. Wilson, P. L. Truron, G. F. Read, G. Richards, S. M. Walker, and D. Riad-Fahmy 1985 Characterization of Profiles of Salivary Progesterone Concentrations during the Luteal Phase of Fertile and Subfertile Women.Journal of Endocrinology 104:441–448.

    Article  Google Scholar 

  • Walker, R. F., D. W. Wilson, G. F. Read, and D. Riad-Fahmy 1980 Assessment of Testicular Function by the Immunoassay of Testosterone in Saliva.International Journal of Andrology 3:105.

    Article  Google Scholar 

  • Walker, R. F., I. A. Hughes, D. Riad-Fahmy, and G. F. Read 1978 Assessment of Ovarian Function by Salivary Progesterone.Lancet 2:585.

    Article  Google Scholar 

  • Wheeler, G. D., S. R. Wall, A. N. Belcastro, and D. C. Cumming 1984 Reduced Serum Testosterone and Prolactin Levels in Male Distance Runners.Journal of the American Medical Association 252:514–516.

    Article  Google Scholar 

  • Winkler, E. M., and K. Christiansen 1991 Anthropometric-Hormonal Correlation Patterns in San and Kavango Males.Annals of Human Biology 18(4):341–355.

    Article  Google Scholar 

  • Worthman, C. M., and M. J. Konner 1987 Testosterone Levels Change with Subsistence Hunting Effort in !Kung San Men.Psychoneuroendocrinology 12(6):449–458.

    Article  Google Scholar 

  • Young, N. R., H. W. G. Baker, G. Liu, and E. Seeman 1993 Body Composition and Muscle Strength in Healthy Men Receiving Testosterone Enanthate for Contraception.Journal of Clinical Endocrinology and Metabolism 77:1028–1032.

    Article  Google Scholar 

  • Zorn, J. R., P. G. McDonough, C. Nessman, Y. Janssens, and L. Cedard 1984 Salivary Progesterone as an Index of the Luteal Function.Fertility and Sterility 41:248–253.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard G. Bribiescas.

Additional information

This research was funded by the National Science Foundation, the Mellon Foundation, Sigma Xi, and Harvard University.

The author is a doctoral candidate in biological anthropology at Harvard University. He received his B.A. in anthropology and psychology from UCLA in 1988 and his M.A. in anthropology from Harvard in 1994. His research interests include male reproductive ecology, male hormone function, foraging societies, evolutionary biology, and behavioral evolution.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bribiescas, R.G. Testosterone levels among Aché hunter-gatherer men. Human Nature 7, 163–188 (1996). https://doi.org/10.1007/BF02692109

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02692109

Key words

Navigation