The Science of Nature

, 103:81 | Cite as

Oxygen isotope fractionation between bird eggshell calcite and body water: application to fossil eggs from Lanzarote (Canary Islands)

  • Nicolas Lazzerini
  • Christophe Lécuyer
  • Romain Amiot
  • Delphine Angst
  • Eric Buffetaut
  • François Fourel
  • Valérie Daux
  • Juan Francisco Betancort
  • Jean-Pierre Flandrois
  • Antonio Sánchez Marco
  • Alejandro Lomoschitz
Original Paper

Abstract

Oxygen and carbon isotope compositions of fossil bird eggshell calcite (δ18Ocalc and δ13Ccalc) are regularly used to reconstruct paleoenvironmental conditions. However, the interpretation of δ18Ocalc values of fossil eggshells has been limited to qualitative variations in local climatic conditions as oxygen isotope fractionations between calcite, body fluids, and drinking water have not been determined yet. For this purpose, eggshell, albumen water, and drinking water of extant birds have been analyzed for their oxygen and carbon isotope compositions. Relative enrichments in 18O relative to 16O between body fluids and drinking water of +1.6 ± 0.9 ‰ for semi-aquatic birds and of +4.4 ± 1.9 ‰ for terrestrial birds are observed. Surprisingly, no significant dependence to body temperature on the oxygen isotope fractionation between eggshell calcite and body fluids is observed, suggesting that bird eggshells precipitate out of equilibrium. Two empirical equations relating the δ18Ocalc value of eggshell calcite to the δ18Ow value of ingested water have been established for terrestrial and semi-aquatic birds. These equations have been applied to fossil eggshells from Lanzarote in order to infer the ecologies of the Pleistocene marine bird Puffinus sp. and of the enigmatic giant birds from the Pliocene. Both δ13Ccalc and δ18Ocalc values of Puffinus eggshells point to a semi-aquatic marine bird ingesting mostly seawater, whereas low δ13Ccalc and high δ18Ocalc values of eggshells from the Pliocene giant bird suggest a terrestrial lifestyle. This set of equations can help to quantitatively estimate the origin of waters ingested by extinct birds as well as to infer either local environmental or climatic conditions.

Keywords

Bird Eggshell Oxygen and carbon isotopes Paleoecology Lanzarote 

References

  1. Amiot R, Buffetaut E, Lécuyer C, et al. (2010) Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology 38:139–142CrossRefGoogle Scholar
  2. 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 98:358–370. doi:10.1016/j.jseaes.2014.11.032 CrossRefGoogle Scholar
  3. Anderson TF, Arthur MA (1983) Stable isotopes of oxygen and carbon and their application to sedimentologic and paleoenvironmental problems. In: Stable isotopes in sedimentary geology. SEPM (Society for Sedimentary Geology), pp 1–151Google Scholar
  4. Angst D, Amiot R, Buffetaut E, et al. (2015) Diet and climatic context of giant birds inferred from δ13Cc and δ18Oc values of Late Palaeocene and Early Eocene eggshells from southern France. Palaeogeogr Palaeoclimatol Palaeoecol 435:210–221. doi:10.1016/j.palaeo.2015.06.011 CrossRefGoogle Scholar
  5. Angst D, Lécuyer C, Amiot R, et al. (2014) Isotopic and anatomical evidence of an herbivorous diet in the Early Tertiary giant bird Gastornis. Implications for the structure of Paleocene terrestrial ecosystems. Naturwissenschaften 101:313–322. doi:10.1007/s00114-014-1158-2 CrossRefPubMedGoogle Scholar
  6. Bicudo JEP, Buttemer WA, Chappell MA, et al. (2010) Ecological and environmental physiology of birds. Oxford University Press, Oxford 317ppCrossRefGoogle Scholar
  7. Bowen GJ (2009) The online isotopes in precipitation calculator, version 2.2. Available from:<http://www.waterisotopes.org.
  8. Bowen GJ, Revenaugh J (2003) Interpolating the isotopic composition of modern meteoric precipitation. Water Resour Res 39:1299. doi:10.1029/2003WR002086 CrossRefGoogle Scholar
  9. Bowen GJ, Wilkinson B (2002) Spatial distribution of δ18O in meteoric precipitation. Geology 30:315–318CrossRefGoogle Scholar
  10. Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. doi:10.1007/s00442-004-1813-y CrossRefPubMedGoogle Scholar
  11. Cerling TE, Harris JM, Hart JA, et al. (2008) Stable isotope ecology of the common hippopotamus. J Zool 276:204–212CrossRefGoogle Scholar
  12. Clarke A, O’Connor MI (2014) Diet and body temperature in mammals and birds. Glob Ecol Biogeogr 23:1000–1008. doi:10.1111/geb.12185 CrossRefGoogle Scholar
  13. Clementz MT, Goswami A, Gingerich PD, Koch PL (2006) Isotopic records from early whales and sea cows: contrasting patterns of ecological transition. J Vertebr Paleontol 26:355–370. doi:10.1671/0272-4634(2006)26[355:IRFEWA]2.0.CO;2 CrossRefGoogle Scholar
  14. Clementz MT, Holroyd PA, Koch PL (2008) Identifying aquatic habits of herbivorous mammals through stable isotope analysis. PALAIOS 23:574–585CrossRefGoogle Scholar
  15. Coplen TB, Kendall C, Hopple J (1983) Comparison of stable isotope reference samples. Nature 302:236–238CrossRefGoogle Scholar
  16. Dansgaard W (1964) Stable isotopes in precipitation. Tellus A 16:438–468CrossRefGoogle Scholar
  17. Dawson WR (1982) Evaporative losses of water by birds. Comp Biochem Physiol A Physiol 71:495–509CrossRefGoogle Scholar
  18. Erben HK, Hoefs J, Wedepohl KH (1979) Paleobiological and isotopic studies of eggshells from a declining dinosaur species. Paleobiology 5:380–414CrossRefGoogle Scholar
  19. Fertuck HC, Newstead JD (1970) Fine structural observations on magnum mucosa in quail and hen oviducts. Z Zellforsch Mikrosk Anat 103:447–459CrossRefPubMedGoogle Scholar
  20. Feuerbacher I, Prinzinger R (1981) The effects of the male sex-hormone testosterone on body temperature and energy metabolism in male Japanese quail (Coturnix coturnix japonica). Comp Biochem Physiol A Physiol 70:247–250CrossRefGoogle Scholar
  21. Folinsbee RE, Fritz P, Krouse HR, Robblee AR (1970) Carbon-13 and oxygen-18 in dinosaur, crocodile, and bird eggshells indicate environmental conditions. Science 168:1353–1355CrossRefPubMedGoogle Scholar
  22. Fricke HC, O’Neil JR (1999) The correlation between 18O/16O ratios of meteoric water and surface temperature: its use in investigating terrestrial climate change over geologic time. Earth Planet Sci Lett 170:181–196CrossRefGoogle Scholar
  23. Garcia-Talavera F (1990) Aves gigantes en el Mioceno de Famara (Lanzarote). Rev Acad Canar Cienc Folia Canar Acad Sci 2:71–79Google Scholar
  24. Gardner JL, Peters A, Kearney MR, et al. (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291. doi:10.1016/j.tree.2011.03.005 CrossRefPubMedGoogle Scholar
  25. Guillette LJ Jr, Cree A, Rooney AA (1995) Biology of stress: interactions with reproduction, immunology and intermediary metabolism. In: Warwick C, Frye FL, Murphy JB (eds) Health and welfare of captive reptiles. Springer, Dordrecht, pp. 32–81CrossRefGoogle Scholar
  26. Hadley NF (1980) Surface waxes and integumentary permeability: lipids deposited on or associated with the surface of terrestrial plants and animals help protect them from a lethal rate of desiccation. Am Sci 68:546–553Google Scholar
  27. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9ppGoogle Scholar
  28. Hoffman TC, Walsberg GE, DeNardo DF (2007) Cloacal evaporation: an important and previously undescribed mechanism for avian thermoregulation. J Exp Biol 210:741–749CrossRefPubMedGoogle Scholar
  29. IAEA/WMO (2015) Global network of isotopes in precipitation. The GNIP Database. Accessible at: http://www-naweb.iaea.org/napc/ih/index.html.
  30. Imai T, Azuma Y (2015) The oldest known avian eggshell, Plagioolithus fukuiensis, from the Lower Cretaceous (upper Barremian) Kitadani Formation, Fukui, Japan. Hist Biol 27:1090–1097. doi:10.1080/08912963.2014.934232 CrossRefGoogle Scholar
  31. Johnson BJ, Fogel ML, Miller GH (1998) Stable isotopes in modern ostrich eggshell: a calibration for paleoenvironmental applications in semi-arid regions of southern Africa. Geochim Cosmochim Acta 62:2451–2461CrossRefGoogle Scholar
  32. Kim S-T, O’Neil JR (1997) Equilibrium and nonequilibrium oxygen isotope effects in synthetic carbonates. Geochim Cosmochim Acta 61:3461–3475CrossRefGoogle Scholar
  33. Koch PL (2007) Isotopic study of the biology of modern and fossil vertebrates. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science, Second edn. Blackwell Publishing, Malden, pp. 99–154CrossRefGoogle Scholar
  34. Kohn MJ (1996) Predicting animal δ18O: accounting for diet and physiological adaptation. Geochim Cosmochim Acta 60:4811–4829CrossRefGoogle Scholar
  35. Lasiewski RC, Dawson WR (1967) A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13–23. doi:10.2307/1366368 CrossRefGoogle Scholar
  36. Luz B, Kolodny Y (1985) Oxygen isotope variations in phosphate of biogenic apatites, IV. Mammal teeth and bones. Earth Planet Sci Lett 75:29–36. doi:10.1016/0012-821X(85)90047-0 CrossRefGoogle Scholar
  37. Mackenzie GJ, Schaffner FC, Swart PK (2015) The stable isotopic composition of carbonate (C & O) and the organic matrix (C & N) in waterbird eggshells from South Florida: insights into feeding ecology, timing of egg formation, and geographic range. Hydrobiologia 743:89–108. doi:10.1007/s10750-014-2015-1 CrossRefGoogle Scholar
  38. Maurer G, Portugal SJ, Boomer I, Cassey P (2011) Avian embryonic development does not change the stable isotope composition of the calcite eggshell. Reprod Fertil Dev 23:339–345. doi:10.1071/RD10138 1031-3613/11/020339 CrossRefPubMedGoogle Scholar
  39. McMinn M, Jaume D (1990) Puffinus olsoni n. sp.: nova espècie de baldritja recentment extingida provinent de depòsits espeleològics de Fuerteventura i Lanzarote (Illes Canàries, Atlàntic Oriental). Endins Publicació Espeleol 63–72.Google Scholar
  40. McNab BK (1966) An analysis of the body temperatures of birds. Condor 68:47–55. doi:10.2307/1365174 CrossRefGoogle Scholar
  41. Mikhailov KE (1991) Classification of fossil eggshells of amniotic vertebrates. Acta Palaeontol Pol 36:193–238Google Scholar
  42. Mikhailov KE (1997) Fossil and recent eggshell in amniotic vertebrates: fine structure, comparative morphology and classification. Spec Pap Palaeontol 56:1–80Google Scholar
  43. Nys Y, Gautron J, Garcia-Ruiz JM, Hincke MT (2004) Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. Comptes Rendus Palevol 3:549–562. doi:10.1016/j.crpv.2004.08.002 CrossRefGoogle Scholar
  44. Pokrovskaya OB, Litvin KE, Pokrovsky BG (2011) The isotope composition of carbon and oxygen in eggshell of barnacle goose Branta leucopsis. In: Doklady Biological Sciences. Springer, pp 124–127.Google Scholar
  45. Prinzinger R, Pressmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol A Physiol 99:499–506CrossRefGoogle Scholar
  46. Rothe P (1964) Fossile Strausseneier auf Lanzarote. Nat Mus 94:175–187Google Scholar
  47. Rozanski K, Araguás-Araguás L, Gonfiantini R (1993) Isotopic patterns in modern global precipitation. Clim Change Cont Isot Rec 78:1–36. doi:10.1029/GM078p0001 Google Scholar
  48. Sanchez Marco A (2010) New data and an overview of the past avifaunas from the Canary Islands. Ardeola 57:13–40Google Scholar
  49. Sarkar A, Bhattacharya SK, Mohabey DM (1991) Stable-isotope analyses of dinosaur eggshells: paleoenvironmental implications. Geology 19:1068–1071. doi:10.1130/0091-7613(1991)019<1068:SIAODE>2.3.CO;2 CrossRefGoogle Scholar
  50. Sauer EF, Rothe P (1972) Ratite eggshells from Lanzarote, Canary Islands. Science 176:43–45CrossRefGoogle Scholar
  51. Schaffner FC, Swart PK (1991) Influence of diet and environmental water on the carbon and oxygen isotopic signatures of seabird eggshell carbonate. Bull Mar Sci 48:23–38Google Scholar
  52. Sokal RR, Rohlf FJ (2009) Introduction to biostatistics, 2nd edn. Dover Publications Incorp, Mineola, New YorkGoogle Scholar
  53. Swart PK, Price RM, Greer L (2001) The relationship between stable isotopic variations (O, H, and C) and salinity in waters and corals from environments in South Florida: implications for reading the paleoenvironmental record. Bull Am Paleontol 17–30.Google Scholar
  54. Turekian KK, Steele JH, Thorpe SA (2009) Climate & oceans: a derivative of the encyclopedia of ocean sciences, 1st edn. Academic Press, AmsterdamGoogle Scholar
  55. 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
  56. Tütken T, Vennemann TW, Janz H, Heizmann EPJ (2006) Palaeoenvironment and palaeoclimate of the Middle Miocene lake in the Steinheim basin, SW Germany: a reconstruction from C, O, and Sr isotopes of fossil remains. Palaeogeogr Palaeoclimatol Palaeoecol 241:457–491. doi:10.1016/j.palaeo.2006.04.007 CrossRefGoogle Scholar
  57. Tyler C (1969) A study of the egg shells of the Gaviiformes, Procellariiformes, Podicipitiformes and Pelecaniformes. J Zool 158:395–412CrossRefGoogle Scholar
  58. Von Schirnding Y, Van Der Merwe NJ, Vogel JC (1982) Influence of diet and age on carbon isotope ratios in ostrich eggshell. Archaeometry 24:3–20CrossRefGoogle Scholar
  59. Walker CA, Wragg GM, Harrison CJ (1990) A new shearwater from the Pleistocene of the Canary Islands and its bearing on the evolution of certain Puffinus shearwaters. Hist Biol 3:203–224CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Nicolas Lazzerini
    • 1
  • Christophe Lécuyer
    • 1
    • 2
  • Romain Amiot
    • 1
  • Delphine Angst
    • 3
  • Eric Buffetaut
    • 4
  • François Fourel
    • 1
  • Valérie Daux
    • 5
  • Juan Francisco Betancort
    • 6
  • Jean-Pierre Flandrois
    • 7
  • Antonio Sánchez Marco
    • 8
  • Alejandro Lomoschitz
    • 9
  1. 1.UMR 5276, Laboratoire de Géologie de Lyon, Terre, Planètes et EnvironnementUniversité Claude BernardVilleurbanne CedexFrance
  2. 2.Institut Universitaire de FranceParisFrance
  3. 3.Paleaobiology Research Group, Biological Sciences DepartmentUniversity of Cape TownCape TownSouth Africa
  4. 4.Centre National de la Recherche Scientifique, UMR 8538, Laboratoire de Géologie de l’Ecole Normale SupérieureParis cedex 05France
  5. 5.Laboratoire des Sciences du Climat et de l’Environnement/IPSL, UMR CEA/CNRS 1572Gif/Yvette CedexFrance
  6. 6.Departamento de BiologíaUniversidad de Las Palmas de Gran Canaria (ULPGC)Las Palmas de Gran CanariaSpain
  7. 7.CNRS, UMR5558, Laboratoire de Biométrie et Biologie ÉvolutiveUniversity Lyon, Université Lyon 1VilleurbanneFrance
  8. 8.Institut Català de Paleontologia Miquel CrusafontBarcelonaSpain
  9. 9.Instituto de Oceanografía y Cambio GlobalUniversidad de Las Palmas de Gran CanariaLas Palmas de Gran CanariaSpain

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