Stable isotope time-series in mammalian teeth: In situ δ18O from the innermost enamel layer

Geochimica et Cosmochimica Acta

Volumn 124, Issue , 2014, Pages 223-236

  Blumenthal, Scott A ^a,b   Cerling, Thure E ^c   Chritz, Kendra L ^c   Bromage, Timothy G ^d   Kozdon, Reinhard ^e   Valley, John W ^e  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b New York Consortium in Evolutionary Primatology NYCEP   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON ISOTOPE; ENAMEL; FOSSIL ASSEMBLAGE; FOSSIL RECORD; HERBIVORE; MAMMAL; MINERALIZATION; OXYGEN ISOTOPE; PALEOENVIRONMENT; SCANNING ELECTRON MICROSCOPY; STABLE ISOTOPE; TIME SERIES;

ANIMALIA; MAMMALIA; RODENTIA; UNGULATA;

EID: 84887005978     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2013.09.032     Document Type: Article

References (92)

1. Allan J.H. Investigations into the mineralization pattern of human dental enamel. J. Dent. Res. 1959, 38:1096-1107.
2. Allan J.H. Maturation of enamel. Structural and Chemical Organization of Teeth 1967, 467-494. Academic Press, New York. A. Miles (Ed.).
3. Aubert M., Williams I.S., Boljkovac K., Moffat I. In situ oxygen isotope micro-analysis of faunal material and human teeth using a SHRIMP II: a new tool for palaeo-ecology and archaeology. J. Archaeol. Sci. 2012, 39:3184-3194.
4. Ayliffe L.K., Chivas A., Leakey M.G. The retention of primary oxygen isotope compositions of fossil elephant skeletal phopshate. Geochim. Cosmochim. Acta 1994, 58:5291-5298.
5. Balasse M. Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling. Int. J. Osteoarchaeol. 2002, 12:155-165.
6. Balasse M. Potential biases in sampling design and interpretation of intra-tooth isotope analysis. Int. J. Osteoarchaeol. 2003, 13:3-10.
7. Balasse M., Ambrose S.H., Smith A.B., Price T.D. The seasonal mobility model for prehistoric herders in the south-western Cape of South Africa assessed by isotopic analysis of sheep tooth enamel. J. Archaeol. Sci. 2002, 29:917-932.
8. Balasse M., Smith A.B., Ambrose S.H., Leigh S. Determining sheep birth seasonality by analysis of tooth enamel oxygen isotope ratios: the Late Stone Age site of Kasteelberg (South Africa). J. Archaeol. Sci. 2003, 30:205-215.
9. 18O) for winter feeding on seaweed by Neolithic sheep of Scotland. J. Zool. 2005, 270:170-176.
10. Balasse M., Obein G., Ughetto-Monfrin J., Mainland I. Investigating seasonality and season of birth in past herds: a reference set of sheep enamel stable oxygen isotope ratios. Archaeometry 2011, 54:349-368.
11. 18O of Bison priscus teeth. Earth Planet. Sci. Lett. 2009, 283:133-143.
12. Bloebaum R.D., Skedros J.G., Vajda E.G., Bachus K.N., Constantz B.R. Determining mineral content variations in bone using backscattered electron imaging. Quatern. Res. 1997, 20:485-490.
13. Boyde A. Development of the structure of the enamel of the incisor teeth in the three classical subordinal groups of the Rodentia. Development, Function and Evolution of Teeth 1978, 43-58. Academic Press, London. P.M. Butler, K.A. Joysey (Eds.).
14. Boyde A., Jones S.J. Backscattered electron imaging of dental tissues. Anat. Embryol. 1983, 168:211-226.
15. Boyde A., Davy K.W.M., Jones S.J. Standards for mineral quantification of human bone by analysis of backscattered electron images. Scanning 1995, 17(5 Suppl.):V6-V7.
16. Britton K., Grimes V., Dau J., Richards M.P. Reconstructing faunal migrations using intra-tooth sampling and strontium and oxygen isotope analyses: a case study of modern caribou (Rangifer tarandus granti). J. Archaeol. Sci. 2009, 36:1163-1172.
17. Brookman T.H., Ambrose S.H. Seasonal variation in kangaroo tooth enamel oxygen and carbon isotopes in Australia. Quatern. Res. 2012, 78:256-265.
18. Bryant J.D., Froelich P.N. A model of oxygen isotope fractionation in body water of large mammals. Geochim. Cosmochim. Acta 1995, 59:4523-4537.
19. Bryant J.D., Froelich P.N., Showers W.J., Genna B.J. Biologic and climatic signals in the oxygen isotopic composition of Eocene-Oligocene equid enamel phosphate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 1996, 126:75-89.
20. Bryant J.D., Koch P.L., Froelich P.N., Showers W.J., Genna B.J. Oxygen isotope partitioning between phosphate and carbonate in mammalian apatite. Geochim. Cosmochim. Acta 1996, 60:5145-5148.
21. Cerling T.E., Harris J.M. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 1999, 120:347-363.
22. Cerling T.E., Sharp Z. Stable carbon and oxygen isotope analysis of fossil tooth enamel using laser ablation. Palaeogeogr. Palaeoclimatol. Palaeoecol. 1996, 126:173-186.
23. Cerling T.E., Harris J.M., Hart J.A., Kaleme P., Klingel H., Leakey M.G., Levin N.E., Lewison R.L., Passey B.H. Stable isotope ecology of the common hippopotamus. J. Zool. 2008, 276:204-212.
24. Chritz K.L., Dyke G.J., Zazzo A., Lister A.M., Monaghan N.T., Sigwart J.D. Palaeobiology of an extinct Ice Age mammal: stable isotope and cementum analysis of giant deer teeth. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2009, 282:133-144.
25. Codron J., Codron D., Sponheimer M., Kirkman K., Duffy K.J., Raubenheimer E.J., Mélice J.L., Grant R., Clauss M., Lee-Thorp J.A. Stable isotope series from elephant ivory reveal lifetime histories of a true dietary generalist. Proc. Biol. Sci. 2012, 279:2433-2441.
26. DeNiro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 1978, 42:495-506.
27. Elliott J.C. Structure, crystal chemistry and density of enamel apatites. Dental Enamel (Ciba Foundation Symposium 205) 1997, 54-72. Wiley Online Library, Chichester, UK. D. Chadwick, G. Cardew (Eds.).
28. Elliott J.C. Calcium phosphate biominerals. Rev. Mineral. Geochem. 2002, 48:427-453.
29. Elliott J.C., Holcomb D.W., Young R.A. Infrared determination of the degree of substitution of hydroxyl by carbonate ions in human dental enamel. Oecologia 1985, 37:372-375.
30. Fisher D.C., Fox D.L. Oxygen isotopes in mammoth teeth: sample design, mineralization patterns, and enamel-dentine comparisons. J. Vert. Palaeontol. 1998, 18(3 Suppl.):41A-42A.
31. Fox D.L., Fisher D.C. Stable isotope ecology of a late Miocene population of Gomphotherium productus (Mammalia, Proboscidea) from Port of Entry Pit, Oklahoma, USA. Palaios 2001, 16:279.
32. Fox D.L., Fisher D.C. Dietary reconstruction of Miocene Gomphotherium (Mammalia, Proboscidea) from the Great Plains region, USA, based on the carbon isotope composition of tusk and molar enamel. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2004, 206:311-335.
33. Fraser R.A., Grün R., Privat K., Gagan M.K. Stable-isotope microprofiling of wombat tooth enamel records seasonal changes in vegetation and environmental conditions in eastern Australia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2008, 269:66-77.
34. Frémondeau D., Cucchi T., Casabianca F. Seasonality of birth and diet of pigs from stable isotope analyses of tooth enamel. J. Archaeol. Sci. 2012, 39:2023-2035.
35. Fricke H.C., O'Neil J.R. Inter-and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeoclimatological and palaeobiological research. Palaeogeogr. Palaeoclimatol. Palaeoecol. 1996, 126:91-100.
36. 4) of mammalian tooth enamel as a record of seasonal variations in continental climate variables. Geochim. Cosmochim. Acta 1998, 62:1839-1850.
37. Glick P.L. Patterns of enamel maturation. J. Dent. Res. 1979, 58:883-895.
38. Gomez S., Boyde A. Correlated alkaline phosphatase histochemistry and quantitative backscattered electron imaging in the study of rat incisor ameloblasts and enamel mineralization. Microsc. Res. Tech. 1994, 29:29-36.
39. Hallin K.A., Schoeninger M.J., Schwarcz H.P. Paleoclimate during Neandertal and anatomically modern human occupation at Amud and Qafzeh, Israel: the stable isotope data. J. Hum. Evol. 2012, 62:59-73.
40. Higgins P., Macfadden B.J. Seasonal and geographic climate variabilities during the Last Glacial Maximum in North America: applying isotopic analysis and macrophysical climate models. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2009, 283:15-27.
41. Hiller C.R., Robinson C., Weatherell J. Variations in the composition of developing rat incisor enamel. Calcif. Tissue Int. 1975, 18:1-12.
42. Hilson S. Teeth 2005, Cambridge University Press, New York.
43. Hoppe K., Stover S., Pascoe J., Amundson R. Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2004, 206:355-365.
44. Howell P.G.T., Davy K.M.W., Boyde A. Mean atomic number and backscattered electron coefficient calculations for some materials with low mean atomic number. Scanning 1998, 20:35-40.
45. Iacumin P., Bocherens H., Mariotti A., Longinelli A. Oxygen isotope analyses of co-existing carbonate and phosphate in biogenic apatite: a way to monitor diagenetic alteration of bone phosphate?. Earth Planet. Sci. Lett. 1996, 142:1-6.
46. 18O analysis of tooth enamel phosphate by isotope ratio monitoring gas chromatography mass spectrometry and ultraviolet laser fluorination. Chem. Geol. 1999, 153:241-248.
47. 13C and Sr intra-tooth isotopic variations applied to a palaeoethological reconstruction. Quatern. Int. 2012, 271:106-119.
48. 18O) and hydrogen (δD) isotopes in ovicaprid dentinal collagen record seasonal variation. J. Archaeol. Sci. 2008, 35:3159-3167.
49. Kita N.T., Ushikubo T., Fu B., Valley J.W. High precision SIMS oxygen isotope analysis and the effect of sample topography. Chem. Geol. 2009, 264:43-57.
50. Kita N.T., Huberty J.M., Kozdon R., Beard B.L., Valley J.W. High-precision SIMS oxygen, sulfur and iron stable isotope analyses of geological materials: accuracy, surface topography and crystal orientation. Surf. Interface Anal. 2011, 43:427-431.
51. Koch P.L., Fisher D.C., Dettman D. Oxygen isotope variation in the tusks of extinct proboscideans: a measure of season of death and seasonality. Geology 1989, 17:515-519.
52. Koch P.L., Tuross N., Fogel M.L. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J. Archaeol. Sci. 1997, 24:417-430.
53. Kohn M.J. Comment: tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series, by B.H. Passey and T.E. Cerling (2002). Geochim. Cosmochim. Acta 2004, 68:403-405.
54. Kohn M.J., Schoeninger M.J., Valley J.W. Herbivore tooth oxygen isotope compositions: effects of diet and physiology. Geochim. Cosmochim. Acta 1996, 60:3889-3896.
55. Kohn M.J., Schoeninger M.J., Valley J.W. Variability in oxygen isotope compositions of herbivore teeth: reflections of seasonality or developmental physiology?. Chem. Geol. 1998, 152:97-112.
56. Kohn M.J., Miselis J.L., Fremd T.J. Oxygen isotope evidence for progressive uplift of the Cascade Range, Oregon. Earth Planet. Sci. Lett. 2002, 204:151-165.
57. Kozdon R., Ushikubo T., Kita N.T., Spicuzza M., Valley J.W. Intratest oxygen isotope variability in the planktonic foraminifer N. pachyderma: real vs. apparent vital effects by ion microprobe. Chem. Geol. 2009, 258:327-337.
58. LeGeros R.Z., Trautz O.R., Klein E., LeGeros J.P. Two types of carbonate substitution in the apatite structure. Experientia 1969, 25:5-7.
59. Longinelli A. Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research?. Geochim. Cosmochim. Acta 1984, 48:385-390.
60. Lundgren T., Persson L.G., Engström E.U., Chabala J., Levi-Setti R., Norén J.G. A secondary ion mass spectroscopic study of the elemental composition pattern in rat incisor dental enamel during different stages of ameloblast differentiation. Arch. Oral Biol. 1998, 43:841-848.
61. Luz B., Kolodny Y., Horowitz M. Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water. Geochim. Cosmochim. Acta 1984, 48:1689-1693.
62. Martin T. Incisor enamel microstructure and systematics in rodents. Tooth Enamel Microstructure 1997, 163-175. Balkema, Rotterdam, Netherlands. W. von Koenigswald, P.M. Sander (Eds.).
63. Metcalfe J.Z., Longstaffe F.J. Mammoth tooth enamel growth rates inferred from stable isotope analysis and histology. Quatern. Res. 2012, 77:424-432.
64. Moss-Salentijn L., Moss M., Yuan M.S.-T. The ontogeny of mammalian enamel. Tooth Enamel Microstructure 1997, 5-30. Balkema, Rotterdam. W. von Koenigswald (Ed.).
65. Nelson S. Paleoseasonality inferred from equid teeth and intra-tooth isotopic variability. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2005, 222:122-144.
66. Passey B.H., Cerling T.E. Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series. Geochim. Cosmochim. Acta 2002, 66:3225-3234.
67. 18O) of very small teeth using laser ablation GC/IRMS. Chem. Geol. 2006, 235:238-249.
68. Passey B.H., Cerling T.E., Schuster G., Robinson T.F. Inverse methods for estimating primary input signals from time-averaged isotope profiles. Geochim. Cosmochim. Acta 2005, 69:4101-4116.
69. c relationship in enamel increments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2011, 310:71-83.
70. 2, hair, and enamel of a small mammal. Geochim. Cosmochim. Acta 2008, 72:19-35.
71. Robinson C., Kirkham J., Brookes S.J., Bonass W.A., Shore R.C. The chemistry of enamel development. Int. J. Dev. Biol. 1995, 39:145-152.
72. Sakae T., Hirai G. Calcification and crystallization in bovine enamel. J. Dent. Res. 1982, 61:57-59.
73. Sharp Z., Cerling T.E. Fossil isotope records of seasonal climate and ecology: straight from the horse's mouth. Geology 1998, 26:219-222.
74. Shi J., Klocke A., Zhang M., Bismayer U. Thermally-induced structural modification of dental enamel apatite decomposition and transformation of carbonate groups. Eur. J. Mineral. 2005, 17:769-775.
75. Smith C.E. Cellular and chemical events during enamel maturation. Crit. Rev. Oral Biol. Med. 1998, 9:128-161.
76. Souron A., Balasse M., Boisserie J.-R. Intra-tooth isotopic profiles of canines from extant Hippopotamus amphibius and late Pliocene hippopotamids (Shungura formation, Ethiopia): insights into the seasonality of diet and climate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2012, 342-243:97-110.
77. Stevens R.E., Balasse M., O'Connell T.C. Intra-tooth oxygen isotope variation in a known population of red deer: implications for past climate and seasonality reconstructions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2011, 301:64-74.
78. Suga S. Comparative histology of progressive mineralization pattern of developing incisor enamel of rodents. J. Dent. Res. 1979, 58:1025-1026.
79. Suga S. Progressive mineralization pattern of developing enamel during the maturation stage. J. Dent. Res. 1982, 61:1532-1542.
80. Suga S. Comparative histology of the progressive mineralization pattern of developing enamel. Mechanisms of Tooth Enamel Formation 1983, 167-203. Quintessence Publishing, Tokyo. S. Suga (Ed.).
81. Suga S. Enamel hypomineralization viewed from the pattern of progressive mineralization of human and monkey developing enamel. Adv. Dent. Res. 1989, 3:188-198.
82. Suga S., Murayama Y., Musashi T. A study of the mineralization process in the developing enamel of guinea pigs. Arch. Oral Biol. 1970, 15:597-608.
83. Suga S., Kamio N., Yoshida S., Doh A. Progressive mineralization pattern of developing enamel of dog. Jpn. J. Oral Biol. 1977, 19:219-238.
84. Tafforeau P., Bentaleb I., Jaeger J., Martin C. Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: potential implications for palaeoenvironmental isotopic studies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2007, 246:206-227.
85. Valley J. W. and Kita N. T. (2009) In situ oxygen isotope geochemistry by ion microprobe. In GAC/MAC Short Course: Secondary Ion Mass Spectrometry in the Earth and Planetary Sciences, vol. 41 (ed. M. Fayek). Mineralogical Association of Canada, Toronto, Canada, pp. 19-63.
86. Wong F., Elliott J., Davis G., Anderson P. X-ray microtomographic study of mineral distribution in enamel of mandibular rat incisors. J. Anat. 2000, 196:405-413.
87. Zazzo A., Lécuyer C., Mariotti A. Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions. Geochim. Cosmochim. Acta 2004, 68:1-12.
88. 13C intra-tooth profiles in bovine enamel: implications for mineralization pattern and isotopic attenuation. Geochim. Cosmochim. Acta 2005, 69:3631-3642.
89. Zazzo A., Balasse M., Patterson W.P. The reconstruction of mammal individual history: refining high-resolution isotope record in bovine tooth dentine. J. Archaeol. Sci. 2006, 33:1177-1187.
90. Zazzo A., Balasse M., Passey B.H., Moloney A.P., Monahan F.J., Schmidt O. The isotope record of short- and long-term dietary changes in sheep tooth enamel: implications for quantitative reconstruction of paleodiets. Geochim. Cosmochim. Acta 2010, 74:3571-3586.
91. Zazzo A., Bendrey R., Vella D., Moloney A.P., Monahan F.J., Schmidt O. A refined sampling strategy for intra-tooth stable isotope analysis of mammalian enamel. Geochim. Cosmochim. Acta 2012, 84:1-13.
92. Zhang C., Wang Y., Li Q., Wang X., Deng T., Tseng Z.J., Takeuchi G.T., Xie G., Xu Y. Diets and environments of late Cenozoic mammals in the Qaidam Basin, Tibetan Plateau: evidence from stable isotopes. Earth Planet. Sci. Lett. 2012, 333-334:70-82.