Letter | Published:

Barium distributions in teeth reveal early-life dietary transitions in primates

Nature volume 498, pages 216219 (13 June 2013) | Download Citation


Early-life dietary transitions reflect fundamental aspects of primate evolution and are important determinants of health in contemporary human populations1,2. Weaning is critical to developmental and reproductive rates; early weaning can have detrimental health effects but enables shorter inter-birth intervals, which influences population growth3. Uncovering early-life dietary history in fossils is hampered by the absence of prospectively validated biomarkers that are not modified during fossilization4. Here we show that large dietary shifts in early life manifest as compositional variations in dental tissues. Teeth from human children and captive macaques, with prospectively recorded diet histories, demonstrate that barium (Ba) distributions accurately reflect dietary transitions from the introduction of mother’s milk through the weaning process. We also document dietary transitions in a Middle Palaeolithic juvenile Neanderthal, which shows a pattern of exclusive breastfeeding for seven months, followed by seven months of supplementation. After this point, Ba levels in enamel returned to baseline prenatal levels, indicating an abrupt cessation of breastfeeding at 1.2 years of age. Integration of Ba spatial distributions and histological mapping of tooth formation enables novel studies of the evolution of human life history, dietary ontogeny in wild primates, and human health investigations through accurate reconstructions of breastfeeding history.

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  1. 1.

    et al. Breastfeeding and maternal and infant health outcomes in developed countries. Evidence Report/Technology Assessment No. 153 (AHRQ, 2007)

  2. 2.

    Life history, maintenance, and the early origins of immune function. Am. J. Hum. Biol. 17, 81–94 (2005)

  3. 3.

    Weaning behaviour in human evolution. Semin. Cell Dev. Biol. 21, 453–461 (2010)

  4. 4.

    & New visions of dental tissue research: Tooth development, chemistry, and structure. Evol. Anthropol. 17, 213–226 (2008)

  5. 5.

    & Relationship between subsistence and age at weaning in “preindustrial” societies. Hum. Nature 12, 47–87 (2001)

  6. 6.

    , & Growth, weaning and maternal investment from a comparative perspective. J. Zool. (Lond.) 225, 99–114 (1991)

  7. 7.

    Comparison of infant feeding patterns reported for nonindustrial populations with current recommendations. J. Nutr. 131, 2707–2715 (2001)

  8. 8.

    , & Rhesus macaque milk: Magnitude, sources, and consequences of individual variation over lactation. Am. J. Phys. Anthropol. 138, 148–157 (2009)

  9. 9.

    , , & Tracking dietary transitions in weanling baboons (Papio hamadryas anubis) using strontium/calcium ratios in enamel. Folia Primatol. (Basel) 79, 197–212 (2008)

  10. 10.

    , & Concentrations of trace elements in sera of newborns, young infants, and adults. Biol. Trace Elem. Res. 68, 121–135 (1999)

  11. 11.

    & Enamel diagenesis at South African Australopith sites: Implications for paleoecological reconstruction with trace elements. Geochim. Cosmochim. Acta 70, 1644–1654 (2006)

  12. 12.

    , & Trace element concentrations in teeth – a modern Idaho baseline with implications for archeometry, forensics, and palaeontology. J. Archaeol. Sci. 40, 1689–1699 (2013)

  13. 13.

    , , , & Rapid dental development in a Middle Paleolithic Belgian Neanderthal. Proc. Natl Acad. Sci. USA 104, 20220–20225 (2007)

  14. 14.

    Cellular and chemical events during enamel maturation. Crit. Rev. Oral Biol. Med. 9, 128–161 (1998)

  15. 15.

    , , & Dentin: structure, composition and mineralization. Front. Biosci. 3, 711–735 (2011)

  16. 16.

    , & Altered states: effects of diagenesis on fossil tooth chemistry. Geochim. Cosmochim. Acta 63, 2737–2747 (1999)

  17. 17.

    & The effect of tissue structure and soil chemistry on trace element uptake in fossils. Geochim. Cosmochim. Acta 74, 3213–3231 (2010)

  18. 18.

    , , & Evidence for dietary change but not landscape use in South African early hominins. Nature 489, 558–560 (2012)

  19. 19.

    et al. Extraction and sequencing of human and Neanderthal mature enamel proteins using MALDI-TOF/TOF MS. J. Archaeol. Sci. 36, 1758–1763 (2009)

  20. 20.

    et al. Revisiting Neandertal diversity with a 100,000 year old mtDNA sequence. Curr. Biol. 16, R400–R402 (2006)

  21. 21.

    , , & Unlocking evidence of early diet from tooth enamel. Proc. Natl Acad. Sci. USA 105, 6834–6839 (2008)

  22. 22.

    , , , & Recall of age of weaning and other breastfeeding variables. Int. Breastfeed. J. 1, 4 (2006)

  23. 23.

    & Trace element diffusivities in bone rule out simple diffusive uptake during fossilization but explain in vivo uptake and release. Proc. Natl Acad. Sci. USA 110, 419–424 (2013)

  24. 24.

    A test of diet versus diagenesis at Ventana Cave, Arizona. J. Archaeol. Sci. 19, 23–37 (1992)

  25. 25.

    et al. First molar eruption, weaning, and life history in living wild chimpanzees. Proc. Natl Acad. Sci. USA 110, 2787–2791 (2013)

  26. 26.

    Dental wear in immature Late Pleistocene European hominines. J. Archaeol. Sci. 24, 677–700 (1997)

  27. 27.

    , & The Effect of time in the U.S. on the duration of breastfeeding in women of Mexican descent. Matern. Child Health J. 11, 119–125 (2007)

  28. 28.

    Observational study of behavior: Sampling methods. Behaviour 49, 227–266 (1974)

  29. 29.

    , , & Elemental bio-imaging of trace elements in teeth using laser ablation-inductively coupled plasma-mass spectrometry. J. Dent. 39, 397–403 (2011)

  30. 30.

    Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological Profile for Barium (US Department of Health and Human Services, Public Health Service, 2007)

  31. 31.

    et al. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ. Health Perspect. 112, 1116–1124 (2004)

  32. 32.

    , , , & Improving acquisition times of elemental bio-imaging for quadrupole-based LA-ICP-MS. J. Anal. At. Spectrom. 27, 159–164 (2012)

  33. 33.

    , & Test of multielement analysis of bone samples using instrumental neutron activation analysis (INAA) and anti-Compton spectrometry. J. Radioanal. Nucl. Chem. 224, 103–107 (1997)

  34. 34.

    , , & The effect of age and gender on Al, B, Ba, Ca, Cu, Fe, K, Li, Mg, Mn, Na, P, S, Sr, V, and Zn contents in rib bone of healthy humans. Biol. Trace Elem. Res. 129, 107–115 (2009)

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L. Reynard, N. Tuross and F. Bidlack provided comments on this project. C. Amarasiriwardena and N. Lupoli provided expertise in macaque milk analysis. Fossil samples were provided by M. Toussaint, R. Gruen and M.-H. Moncell. The CHAMACOS study is funded by the US Environmental Protection Agency (RD 83171001 and RD 82670901 to B.E.) and the US National Institutes of Environmental Health Sciences (PO1 ES009605 to B.E.). Support for macaque data collection was provided by NSF BCS-0921978 (K.H.); milk samples were made possible through the ARMMS program (Archive of Rhesus Macaque Milk Samples). Histological study of the Scladina Neanderthal was funded by the Max Planck Institute for Evolutionary Anthropology. R.J.-B. is supported by Australian Research Council Discovery Grant (DP120101752) and SCU postdoctoral Fellowship grant. P.D. was supported by Australian Research Council Project Grant (LP100200254) that draws collaborative funding from Agilent Technologies and Kennelec Scientific. M.A. is supported by a National Institute of Environmental Health Sciences grant 4R00ES019597-03. C.A. and M.A. are supported by NHMRC grant APP1028372.

Author information

Author notes

    • Christine Austin
    •  & Tanya M. Smith

    These authors contributed equally to this work.


  1. Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA

    • Christine Austin
    •  & Manish Arora
  2. Environmental and Occupational Medicine and Epidemiology, Harvard School of Public Health, Boston, Massachusetts 02115, USA

    • Christine Austin
    •  & Manish Arora
  3. Institute of Dental Research, Westmead Millennium Institute, Westmead Hospital, and Oral Pathology and Oral Medicine, Faculty of Dentistry, University of Sydney, Sydney, New South Wales 2145, Australia

    • Christine Austin
    •  & Manish Arora
  4. Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Tanya M. Smith
    •  & Katie Hinde
  5. Center for Environmental Research and Children’s Health, School of Public Health, University of California, Berkeley, California 94720, USA

    • Asa Bradman
    •  & Brenda Eskenazi
  6. California National Primate Research Center, Davis, California 95616, USA

    • Katie Hinde
  7. Southern Cross GeoScience, Southern Cross University, Lismore, New South Wales 2480, Australia

    • Renaud Joannes-Boyau
  8. Elemental Bio-imaging Facility, University of Technology Sydney, Sydney, New South Wales 2007, Australia

    • David Bishop
    • , Dominic J. Hare
    •  & Philip Doble
  9. The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria 3010, Australia

    • Dominic J. Hare


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C.A., T.M.S. and M.A. designed the study, undertook the elemental and histological analysis, and wrote the manuscript. A.B. and B.E. designed and analysed the human study. K.H. designed the macaque lactation study and collected samples. R.J.-B. analysed the Payre Neanderthal tooth in the Supplementary Information and assessed diagenetic alteration. C.A., D.J.H., D.B. and P.D. undertook elemental imaging of tooth samples. All authors contributed to the interpretation of the results, in addition to editing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Manish Arora.

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    Supplementary Information

    This file contains Supplementary Figures 1-10, Supplementary Tables 1-5, a Supplementary Discussion, Supplementary Methods and additional references.

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