The Science of Nature

, 104:47 | Cite as

Oxygen isotope fractionation between bird bone phosphate and drinking water

  • Romain AmiotEmail author
  • Delphine Angst
  • Serge Legendre
  • Eric Buffetaut
  • François Fourel
  • Jan Adolfssen
  • Aurore André
  • Ana Voica Bojar
  • Aurore Canoville
  • Abel Barral
  • Jean Goedert
  • Stanislaw Halas
  • Nao Kusuhashi
  • Ekaterina Pestchevitskaya
  • Kevin Rey
  • Aurélien Royer
  • Antônio Álamo Feitosa Saraiva
  • Bérengère Savary-Sismondini
  • Jean-Luc Siméon
  • Alexandra Touzeau
  • Zhonghe Zhou
  • Christophe Lécuyer
Original Paper


Oxygen isotope compositions of bone phosphate (δ18Op) were measured in broiler chickens reared in 21 farms worldwide characterized by contrasted latitudes and local climates. These sedentary birds were raised during an approximately 3 to 4-month period, and local precipitation was the ultimate source of their drinking water. This sampling strategy allowed the relationship to be determined between the bone phosphate δ18Op values (from 9.8 to 22.5‰ V-SMOW) and the local rainfall δ18Ow values estimated from nearby IAEA/WMO stations (from −16.0 to −1.0‰ V-SMOW). Linear least square fitting of data provided the following isotopic fractionation equation: δ18Ow = 1.119 (±0.040) δ18Op − 24.222 (±0.644); R 2 = 0.98. The δ18Op–δ18Ow couples of five extant mallard ducks, a common buzzard, a European herring gull, a common ostrich, and a greater rhea fall within the predicted range of the equation, indicating that the relationship established for extant chickens can also be applied to birds of various ecologies and body masses. Applied to published oxygen isotope compositions of Miocene and Pliocene penguins from Peru, this new equation computes estimates of local seawater similar to those previously calculated. Applied to the basal bird Confuciusornis from the Early Cretaceous of Northeastern China, our equation gives a slightly higher δ18Ow value compared to the previously estimated one, possibly as a result of lower body temperature. These data indicate that caution should be exercised when the relationship estimated for modern birds is applied to their basal counterparts that likely had a metabolism intermediate between that of their theropod dinosaur ancestors and that of advanced ornithurines.


Bird Phosphate Oxygen isotope Fractionation equation 



Dr. Stanislaw Halas, co-author of this study, passed away the 3rd may 2017. Our thoughts are with his family and colleagues during these difficult times. The authors would like to thank V. Paulet, P. Touzeau, M. Mathis, D. Viscaïno, I. Buffetaut, J. Barnoud, M. and W. Halverson, G. and C. von Hahn, A. and O. von Lilienfeld, S. and G. Caillard, J., and J. and P. Angst for providing chicken bones and D. Berthet from the Musée des Confluences, Lyon, France, for providing the bone samples of Buteo buteo (50.001696), Larus argentatus (50.001682), and Anas platyrhynchos (50.001681). We also would like to thank the five anonymous reviewers for their constructive comments that greatly helped to improve the manuscript. This study was supported by the CNRS PICS project no. PIC07193, the National Basic Research Program of China grant 2012CB821900 (RA), and the Institut Universitaire de France (CL).

Supplementary material

114_2017_1468_MOESM1_ESM.xlsx (20 kb)
ESM 1 (XLSX 19 kb)


  1. Amiot R, Lécuyer C, Buffetaut E et al (2004) Latitudinal temperature gradient during the Cretaceous Upper Campanian-Middle Maastrichtian: δ18O record of continental vertebrates. Earth Planet Sci Lett 226:255–272. doi: 10.1016/j.epsl.2004.07.015 CrossRefGoogle Scholar
  2. Amiot R, Lécuyer C, Escarguel G et al (2007) Oxygen isotope fractionation between crocodilian phosphate and water. Palaeogeogr Palaeoclimatol Palaeoecol 243:412–420. doi: 10.1016/j.palaeo.2006.08.013 CrossRefGoogle Scholar
  3. Amiot R, Göhlich UB, Lécuyer C et al (2008) Oxygen isotope compositions of phosphate from Middle Miocene-Early Pliocene marine vertebrates of Peru. Palaeogeogr Palaeoclimatol Palaeoecol 264:85–92. doi: 10.1016/j.palaeo.2008.04.001 CrossRefGoogle Scholar
  4. Amiot R, Buffetaut E, Lécuyer C et al (2010) Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology 38:139–142. doi: 10.1130/G30402.1 CrossRefGoogle Scholar
  5. Amiot R, Wang X, Zhou Z et al (2011) Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates. Proc Natl Acad Sci 108:5179–5183. doi: 10.1073/pnas.1011369108 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Amiot R, Wang X, Zhou Z et al (2015) Environment and ecology of East Asian dinosaurs during the Early Cretaceous inferred from stable oxygen and carbon isotopes in apatite. J Asian Earth Sci 98:358–370CrossRefGoogle Scholar
  7. Barkan E, Luz B (2005) High precision measurements of 17O/16O and 18O/16O ratios in H2O. Rapid Commun Mass Spectrom 19:3737–3742. doi: 10.1002/rcm.2250 CrossRefPubMedGoogle Scholar
  8. Barrick RE, Fischer AG, Showers WJ (1999) Oxygen isotopes from turtle bone: applications for terrestrial paleoclimates? PALAIOS 14:186–191. doi: 10.2307/3515374 CrossRefGoogle Scholar
  9. Bojar A-V, Guja O, Pelc A et al (2015) Bison bonasus skull from the Bihor Mountains, Romania: isotopic and morphological investigations. The Holocene 25:1134–1143. doi: 10.1177/0959683615580202 CrossRefGoogle Scholar
  10. Bojar A-V, Halas S, Bojar H-P, Chmiel S (2017) Stable isotope hydrology of precipitation and groundwater of a region with high continentality, South Carpathians, Romania. Carpathian J Earth Environ Sci 12:513–524Google Scholar
  11. Bowen GJ, Revenaugh J (2003) Interpolating the isotopic composition of modern meteoric precipitation. Water Resour Res 39:1299. doi: 10.1029/2003WR002086 CrossRefGoogle Scholar
  12. Brudevold F, Soremark R (1967) Chemistry of the mineral phase of enamel. In: Mills A (ed) Structural and chemical organization of teeth, vol 2. Elsevier, Amsterdam, pp 247–277Google Scholar
  13. Bryant DJ, Luz B, Froelich PN (1994) Oxygen isotopic composition of fossil horse tooth phosphate as a record of continental paleoclimate. Palaeogeogr Palaeoclimatol Palaeoecol 107:303–316. doi: 10.1016/0031-0182(94)90102-3 CrossRefGoogle Scholar
  14. Chenery C, Mueldner G, Evans J et al (2010) Strontium and stable isotope evidence for diet and mobility in Roman Gloucester, UK. J Archaeol Sci 37:150–163. doi: 10.1016/j.jas.2009.09.025 CrossRefGoogle Scholar
  15. Chinsamy A, Chiappe LM, Dodson P (1994) Growth rings in Mesozoic birds. Nature 368:196–197. doi: 10.1038/368196a0 CrossRefGoogle Scholar
  16. Chinsamy A, Chiappe LM, Dodson P (1995) Mesozoic avian bone microstructure: physiological implications. Paleobiology 21:561–574. doi: 10.1017/S0094837300013543 CrossRefGoogle Scholar
  17. Coplen TB, Huang R (2000) Stable hydrogen and oxygen isotope ratios for selected sites of the National Oceanic and Atmospheric Administration’s Atmospheric Integrated Research Monitoring Network (AIRMoN). US Geological Survey, RestonGoogle Scholar
  18. Cormie AB, Luz B, Schwarcz HP (1994) Relationship between the hydrogen and oxygen isotopes of deer bone and their use in the estimation of relative humidity. Geochim Cosmochim Acta 58:3439–3449. doi: 10.1016/0016-7037(94)90097-3 CrossRefGoogle Scholar
  19. Crowson RA, Showers WJ, Wright EK, Hoering TC (1991) Preparation of phosphate samples for oxygen isotope analysis. Anal Chem 63:2397–2400. doi: 10.1021/ac00020a038 CrossRefGoogle Scholar
  20. D’Angela D, Longinelli A (1990) Oxygen isotopes in living mammal’s bone phosphate: further results. Chem Geol Isot Geosci Sect 86:75–82. doi: 10.1016/0168-9622(90)90007-Y CrossRefGoogle Scholar
  21. Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468. doi: 10.1111/j.2153-3490.1964.tb00181.x CrossRefGoogle Scholar
  22. de Ricqlès A, Padian K, Horner JR et al (2003) Osteohistology of Confuciusornis sanctus (Theropoda: Aves). J Vertebr Paleontol 23:373–386. doi: 10.1671/0272-4634(2003)023[0373:OOCSTA]2.0.CO;2 CrossRefGoogle Scholar
  23. Dean JR, Eastwood WJ, Roberts N et al (2015) Tracking the hydro-climatic signal from lake to sediment: a field study from central Turkey. J Hydrol 529:608–621. doi: 10.1016/j.jhydrol.2014.11.004 CrossRefGoogle Scholar
  24. Fourel F, Martineau F, Lécuyer C et al (2011) 18O/16O ratio measurements of inorganic and organic materials by elemental analysis–pyrolysis–isotope ratio mass spectrometry continuous-flow techniques. Rapid Commun Mass Spectrom 25:2691–2696. doi: 10.1002/rcm.5056 CrossRefPubMedGoogle Scholar
  25. Halas S, Skrzypek G, Meier-Augenstein W et al (2011) Inter-laboratory calibration of new silver orthophosphate comparison materials for the stable oxygen isotope analysis of phosphates. Rapid Commun Mass Spectrom 25:579–584. doi: 10.1002/rcm.4892 CrossRefPubMedGoogle Scholar
  26. Hou L-H, Zhou Z, Gu Y, Zhang H (1995) Confuciusornis sanctus, a new Late Jurassic sauriurine bird from China. Chin Sci Bull 40:1545–1551Google Scholar
  27. IAEA/WMO (2016) Global network of isotopes in precipitation. The GNIP Database. Accessible at:
  28. Kadono H, Besch EL (1978) Telemetry measured body temperature of domestic fowl at various ambient temperatures. Poult Sci 57:1075–1080. doi: 10.3382/ps.0571075 CrossRefPubMedGoogle Scholar
  29. Kennedy CD, Bowen GJ, Ehleringer JR (2011) Temporal variation of oxygen isotope ratios (δ18O) in drinking water: implications for specifying location of origin with human scalp hair. Forensic Sci Int 208:156–166. doi: 10.1016/j.forsciint.2010.11.021 CrossRefPubMedGoogle Scholar
  30. Kohn MJ (1996) Predicting animal δ18O: accounting for diet and physiological adaptation. Geochim Cosmochim Acta 60:4811–4829. doi: 10.1016/S0016-7037(96)00240-2 CrossRefGoogle Scholar
  31. Kohn MJ, Schoeninger MJ, Valley JW (1996) Herbivore tooth oxygen isotope compositions: effects of diet and physiology. Geochim Cosmochim Acta 60:3889–3896. doi: 10.1016/0016-7037(96)00248-7 CrossRefGoogle Scholar
  32. Kolodny Y, Luz B, Navon O (1983) Oxygen isotope variations in phosphate of biogenic apatites, I. Fish bone apatite—rechecking the rules of the game. Earth Planet Sci Lett 64:398–404. doi: 10.1016/0012-821X(83)90100-0 CrossRefGoogle Scholar
  33. Kolodny Y, Luz B, Sander M, Clemens WA (1996) Dinosaur bones: fossils or pseudomorphs? The pitfalls of physiology reconstruction from apatitic fossils. Palaeogeogr Palaeoclimatol Palaeoecol 126:161–171CrossRefGoogle Scholar
  34. Lazzerini N, Lécuyer C, Amiot R et al (2016) Oxygen isotope fractionation between bird eggshell calcite and body water: application to fossil eggs from Lanzarote (Canary Islands). Sci Nat 103:81. doi: 10.1007/s00114-016-1404-x CrossRefGoogle Scholar
  35. Lécuyer C, Grandjean P, O’Neil JR et al (1993) Thermal excursions in the ocean at the Cretaceous-tertiary boundary(northern Morocco): δ18O record of phosphatic fish debris. Palaeogeogr Palaeoclimatol Palaeoecol 105:235–243. doi: 10.1016/0031-0182(93)90085-W CrossRefGoogle Scholar
  36. Lécuyer C, Grandjean P, Mazin J-M, de Buffrénil V (1999) Oxygen isotope compositions of reptile bones and teeth: a potential record of terrestrial and marine paleo-environments. In: Hoch E, Brantsen AK (eds). Copenhagen University, Geologisk Museum, Denmark, p 33Google Scholar
  37. Lécuyer C, Amiot R, Touzeau A, Trotter J (2013) Calibration of the phosphate δ18O thermometer with carbonate–water oxygen isotope fractionation equations. Chem Geol 347:217–226. doi: 10.1016/j.chemgeo.2013.03.008 CrossRefGoogle Scholar
  38. Longinelli A (1984) Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research? Geochim Cosmochim Acta 48:385–390. doi: 10.1016/0016-7037(84)90259-X CrossRefGoogle Scholar
  39. Longinelli A, Nuti S (1973) Revised phosphate-water isotopic temperature scale. Earth Planet Sci Lett 19:373–376. doi: 10.1016/0012-821X(73)90088-5 CrossRefGoogle Scholar
  40. Luz B, Kolodny Y, Horowitz M (1984) Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water. Geochim Cosmochim Acta 48:1689–1693. doi: 10.1016/0016-7037(84)90338-7 CrossRefGoogle Scholar
  41. Matsubaya O, Kawaraya H (2014) Hydrogen and oxygen isotopic characteristics of precipitation in coastal areas of Japan determined by observations for 23 years at Akita and for 1-2 years at other several localities. Geochem J 48:397–408. doi: 10.2343/geochemj.2.0314 CrossRefGoogle Scholar
  42. Padian K, de Ricqlès AJ, Horner JR (2001) Dinosaurian growth rates and bird origins. Nature 412:405–408. doi: 10.1038/35086500 CrossRefPubMedGoogle Scholar
  43. Pesti GM, Amato SV, Minear LR (1985) Water consumption of broiler chickens under commercial conditions. Poult Sci 64:803–808. doi: 10.3382/ps.0640803 CrossRefPubMedGoogle Scholar
  44. Prinzinger R, Pressmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol A Physiol 99:499–506. doi: 10.1016/0300-9629(91)90122-S CrossRefGoogle Scholar
  45. Rey K, Amiot R, Fourel F et al (2016) Global climate perturbations during the Permo-Triassic mass extinctions recorded by continental tetrapods from South Africa. Gondwana Res 37:384–396. doi: 10.1016/ CrossRefGoogle Scholar
  46. de Ricqlès A, Padian K, Horner JR et al (2003) Osteohistology of Confuciusornis sanctus (Theropoda: Aves). J Vertebr Paleontol 23:373–386. doi: 10.1671/0272-4634(2003)023[0373:OOCSTA]2.0.CO;2 CrossRefGoogle Scholar
  47. Rink WJ, Schwarcz HP (1995) Tests for diagenesis in tooth enamel: ESR dating signals and carbonate contents. J Archaeol Sci 22:251–255CrossRefGoogle Scholar
  48. Royer A, Lécuyer C, Montuire S et al (2013) What does the oxygen isotope composition of rodent teeth record? Earth Planet Sci Lett 361:258–271. doi: 10.1016/j.epsl.2012.09.058 CrossRefGoogle Scholar
  49. Senter P (2006) Scapular orientation in theropods and basal birds, and the origin of flapping flight. Acta Palaeontol Pol 51:305–313Google Scholar
  50. Stanton-Thomas KJ, Carlson SJ (2004) Microscale δ18O and δ13C isotopic analysis of an ontogenetic series of the hadrosaurid dinosaur Edmontosaurus: implications for physiology and ecology. Palaeogeogr Palaeoclimatol Palaeoecol 206:257–287. doi: 10.1016/j.palaeo.2004.01.007 CrossRefGoogle Scholar
  51. Suarez CA, González LA, Ludvigson GA et al (2014) Multi-taxa isotopic investigation of paleohydrology in the Lower Cretaceous Cedar Mountain Formation, Eastern Utah, USA: deciphering effects of the Nevadaplano Plateau on regional climate. J Sediment Res 84:975–987. doi: 10.2110/jsr.2014.76 CrossRefGoogle Scholar
  52. Tarnowski CP, Ignelzi MA, Morris MD (2002) Mineralization of developing mouse calvaria as revealed by Raman microspectroscopy. J Bone Miner Res 17:1118–1126CrossRefPubMedGoogle Scholar
  53. Tütken T (2014) Isotope compositions (C, O, Sr, Nd) of vertebrate fossils from the Middle Eocene oil shale of Messel, Germany: implications for their taphonomy and palaeoenvironment. Palaeogeogr Palaeoclimatol Palaeoecol 416:92–109CrossRefGoogle Scholar
  54. Van Kampen M, Mitchell BW, Siegel HS (1979) Thermoneutral zone of chickens as determined by measuring heat production, respiration rate, and electromyographic and electroencephalographic activity in light and dark environments and changing ambient temperatures. J Agric Sci 92:219–226. doi: 10.1017/S0021859600060664 CrossRefGoogle Scholar
  55. Vennemann TW, Hegner E, Cliff G, Benz GW (2001) Isotopic composition of recent shark teeth as a proxy for environmental conditions. Geochim Cosmochim Acta 65:1583–1599CrossRefGoogle Scholar
  56. Wang M, Wang X, Wang Y, Zhou Z (2016) A new basal bird from China with implications for morphological diversity in early birds. Sci Rep. doi: 10.1038/srep19700
  57. West GC (1965) Shivering and heat production in wild birds. Physiol Zool 38:111–120CrossRefGoogle Scholar
  58. Withers PC, Forbes RB, Hedrick MS (1987) Metabolic, water and thermal relations of the Chilean tinamou. Condor 89:424–426. doi: 10.2307/1368498 CrossRefGoogle Scholar
  59. Yates EB, Hamlin SN, McCann LH (1990) Geohydrology, water quality, and water budgets of Golden Gate Park and the Lake Merced area in the western part of San Francisco, California. US Geological Survey, SacramentoGoogle Scholar
  60. Yoshida N, Miyazaki N (1991) Oxygen isotope correlation of cetacean bone phosphate with environmental water. J Geophys Res Oceans 96:815–820. doi: 10.1029/90JC01580 CrossRefGoogle Scholar
  61. Zazzo A, Lécuyer C, Mariotti A (2004a) Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions. Geochim Cosmochim Acta 68:1–12CrossRefGoogle Scholar
  62. Zazzo A, Lécuyer C, Sheppard SMF et al (2004b) Diagenesis and the reconstruction of paleoenvironments: a method to restore original δ18O values of carbonate and phosphate from fossil tooth enamel. Geochim Cosmochim Acta 68:2245–2258. doi: 10.1016/j.gca.2003.11.009 CrossRefGoogle Scholar
  63. Zhang F, Hou L, Ouyang L (1998) Osteological microstructure of Confuciusornis: preliminary report. Vertebr Pal Asiat 36:126–135Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Romain Amiot
    • 1
    Email author
  • Delphine Angst
    • 2
  • Serge Legendre
    • 1
  • Eric Buffetaut
    • 3
  • François Fourel
    • 4
  • Jan Adolfssen
    • 5
  • Aurore André
    • 6
  • Ana Voica Bojar
    • 7
  • Aurore Canoville
    • 8
  • Abel Barral
    • 1
  • Jean Goedert
    • 1
  • Stanislaw Halas
    • 9
  • Nao Kusuhashi
    • 10
  • Ekaterina Pestchevitskaya
    • 11
  • Kevin Rey
    • 12
  • Aurélien Royer
    • 13
  • Antônio Álamo Feitosa Saraiva
    • 14
  • Bérengère Savary-Sismondini
    • 15
  • Jean-Luc Siméon
    • 16
  • Alexandra Touzeau
    • 17
  • Zhonghe Zhou
    • 18
  • Christophe Lécuyer
    • 1
    • 19
  1. 1.UMR 5276, Laboratoire de Géologie de Lyon, Terre, Planètes et Environnement, Université Claude Bernard Lyon 1/CNRS/École Normale Supérieure de LyonVilleurbanne CedexFrance
  2. 2.Palaeobiology Research Group, Biological Sciences DepartmentUniversity of Cape TownRhodes GiftSouth Africa
  3. 3.Centre National de la Recherche Scientifique, UMR 8538, Laboratoire de Géologie de l’Ecole Normale SupérieureParis Cedex 05France
  4. 4.CNRS UMR 5023 Laboratoire d’Ecologie des Hydrosystèmes Naturels et AnthropisésUniversité ClaudeBernard Lyon 1Villeurbanne CedexFrance
  5. 5.Ministry of Mineral Resources, GreenlandNuukGreenland
  6. 6.Départements Biologie-Biochimie et Sciences de la TerreUniversité de Reims Champagne-Ardenne, CREAReimsFrance
  7. 7.Department of Geography and Geology, Department of MineralogySalzburg UniversitySalzburgAustria
  8. 8.Paleontology Research Lab, North Carolina Museum of Natural Sciences; Department of Biological SciencesNorth Carolina State UniversityRaleighUSA
  9. 9.Mass Spectrometry Laboratory, UMCSLublinPoland
  10. 10.Department of Earth’s Evolution and Environment, Graduate School of Science and EngineeringEhime UniversityEhimeJapan
  11. 11.A.A. Trofimuk Institute of Petroleum Geology and GeophysicsSiberian Branch of the Russian Academy of SciencesNovosibirskRussia
  12. 12.Evolutionary Studies Institute and School of GeosciencesUniversity of the WitwatersrandJohannesburgSouth Africa
  13. 13.Université de Bordeaux, CNRS UMR 5199 PACEAPessac CedexFrance
  14. 14.Laboratório de PaleontologiaUniversidade Regional do CaririCratoBrazil
  15. 15.Fortis Petroleum Corporation ASStavangerNorway
  16. 16.SIMEON TechnologiesToulouseFrance
  17. 17.LSCE—UMR CEA-CNRS-UVSQ-Université Paris SaclayGif-sur-YvetteFrance
  18. 18.Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and PaleoanthropologyChinese Academy of SciencesBeijingChina
  19. 19.Institut Universitaire de FranceParisFrance

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