Revisiting old bones: Coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool

Geological Journal

Volumn 44, Issue 5, 2009, Pages 605-620

  Clementz, M T ^a   Fox Dobbs, K ^b,c,d   Wheatley, P V ^d   Koch, P L ^d   Doak, D F ^c  

^a UNIVERSITY OF WYOMING   (United States)

^b UNIVERSITY OF PUGET SOUND   (United States)

^c UNIVERSITY OF WYOMING   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bioapatite; Carnivore; Marine mammal; Megafauna; Palaeoecology; Stable isotope; Trophic level

Indexed keywords

APATITE; BONE; CARBON ISOTOPE; COLLAGEN; ISOTOPIC ANALYSIS; MAMMAL; PALEOECOLOGY; STABLE ISOTOPE;

MAMMALIA;

EID: 69949179645     PISSN: 00721050     EISSN: 10991034     Source Type: Journal    
DOI: 10.1002/gj.1173     Document Type: Article

References (76)

1. Ali M, Qamar IA, Ali A, Arshad M, Iqbal J. 2001. Evaluation of tropical grasses for forage yield and crude protein content in the Pothwar Plateau of Pakistan. Online Journal of Biological Sciences 1: 466-467.
2. Ambrose SH. 1990. Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science 17: 431-451.
3. Ambrose SH. 1991. Effects of diet, climate, and physiology on nitrogen isotope abundances in terrestrial foodwebs. Journal of Archaeological Science 18: 293-317.
4. Ambrose SH, Buikstra JE, Krueger HW. 2003. Status and gender differences in diet at Mound 72, Cahokia, revealed by isotopic analysis of bone. Journal of Anthropological Archaeology 22: 217-226.
5. Ambrose SH, Butler BM, Hanson DB, Hunter-Anderson RL, Krueger HW. 1997. Stable isotopic analysis of human diet in the Marianas archipelago, western Pacific. American Journal of Physical Anthropology 104: 343-361.
6. Ambrose SH, Krigbaum J. 2003. Bone chemistry and bioarchaeology. Journal of Anthropological Archaeology 22: 193-199.
7. Ambrose SH, Norr L. 1993. Experimental evidence for the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In Prehistoric Human Bone: Archaeology at the Molecular Level, Lambert JB, Grupe G (eds). Springer-Verlag: New York; 1-37.
8. Balasse M, Tresset A, Dobney K, Ambrose SH. 2005. The use of isotope ratios to test for seaweed eating in sheep. Journal of Zoology 266: 283-291.
9. 15N) in Pleistocene mammals. In Biogeochemical Approaches to Paleodietary Analyses, Katzenberg MA, Ambrose SH (eds). Kluwer Academic/Plenum Publishers: New York; 65-88.
10. Bocherens H. 2003. Isotopic biogeochemistry and the paleoecology of the mammoth steppe fauna. In Advances in Mammoth Research (Proceedings of the Second International Mammoth Conference, Rotterdam, May 16-20 1999), Reumer JWF, De Vols J, Mol D (eds). Deinsea 9; 57-76.
11. Bocherens H, Fizet M, Mariotti A. 1994a. Diet, physiology and ecology of fossil mammals as inferred by stable carbon and nitrogen isotope biogeochemistry; implications for Pleistocene bears. Palaeogeography, Palaeoclimatology, Palaeoecology 107: 213-225.
12. 18O) to the paleoecology of mammoths (Mammuthus primigenius). Historical Biology 7: 187-202.
13. Bocherens H, Mariotti A. 1992. Biogéochimie isotopique du carbone dans les os et les dents de mammifères actuels et fossiles de zones froides et tempérées. Comptes Rendus de l'Académie des Sciences, Série II, Paris 315: 1147-1153.
14. Boon PL, Bunn SE. 1994. Variations in the stable isotope composition of aquatic plants and their implications for food web analysis. Aquatic Botany 48: 99-108.
15. Caumette G, Ouypornkochagorn S, Scrimgeour CM, Raab A, Feldmann J. 2007. Monitoring the arsenic and iodine exposure of seaweedeating North Ronaldsay sheep from the gestational and suckling periods to adulthood by using horns as a dietary archive. Environmental Science and Technology 41: 2673-2679.
16. Caut S, Roemer GW, Donlan CJ, Courchamp F. 2006. Coupling stable isotopes with bioenergetics to estimate interspecific interactions. Ecological Applications 16: 1893-1900.
17. Clementz MT, Holroyd PA, Koch PL. 2007. Identifying aquatic habits of herbivorous mammals through stable isotope analysis. Palaios 23: 574-585.
18. Coltrain JB, Harris JM, Cerling TE, Ehleringer JR, Dearing M, Ward J, Allen J. 2004. Trophic level relationships among Rancho La Brea fauna and their implications for the paleoecology of the late Pleistocene based on bone collagen stable isotope chemistry. Palaeogeography, Palaeoclimatology, Palaeoecology 205: 199-219.
19. Corbett DG, Causey D, Clementz M, Koch PL, Doroff A, Lefevre C, West D. 2007. Aleuts, sea otters, and sea cows: 3,000 years of interactions in the western Aleutian Islands, Alaska. In Human impacts on ancient marine environments, Erlandson J, Rick T (eds). University of California Press: Berkeley; 56-92.
20. Dawes CJ, Lawrence JM. 1980. Seasonal changes in the proximate constituents of the seagrass Thalassia testudinum, Halodule wrightii, and Syringodium filiforme. Aquatic Botany 8: 371-380.
21. Deutsch CJ, Reid JP, Bonde RK, Easton DE, Kochman HI, O'Shea TJ. 2003. Seasonal movements, migratory behavior, and site fidelity of West Indian manatees along the Atlantic Coast of the United States. Wildlife Monographs 151: 1-77.
22. Fox-Dobbs K, Bump JK, Peterson RO, Fox DL, Koch PL. 2007. Carnivore-specific stable isotope variables and variation in the foraging ecology of modern and ancient wolf populations: case studies from Isle Royale, Minnesota, and La Brea. Canadian Journal of Zoology 85: 458-471.
23. Fox-Dobbs K, Leonard JA, Koch PL. 2008. Pleistocene megafauna from eastern Beringia: paleoecological and paleoenvironmental interpretations of stable carbon and nitrogen isotope and radiocarbon records. Palaeogeography, Palaeoclimatology, Palaeoecology 261: 30-46.
24. Garvie-Lok SJ, Varney TL, Katzenberg MA. 2004. Preparation of bone carbonate for stable isotope analysis: the effects of treatment time and acid concentration. Journal of Archaeological Science 31: 763-776.
25. Grocke D. 1997. Stable-isotope studies on the collagenic and hydroxylapatite components of fossils: palaeoecological implications. Lethaia 30: 65-78.
26. Guy PR. 1977. Coprophagy in African elephant (Loxodonta africana Blumenbach). East African Wildlife Journal 15: 174.
27. 14N ratios of plants in South Africa and Nambia: relationship to climate and coastal/saline environments. Oecologia 74: 236-246.
28. 3 plants: implications for palaeodiet studies. Journal of Archaeological Science 26: 637-650.
29. Hedges REM. 2003. On bone collagen - apatite-carbonate isotopic relationships. International Journal of Osteoarchaeology 13: 66-79.
30. Hedges REM, Clement JG, Thomas DL, O'Connell TC. 2007. Collagen turnover in the adult femoral mid-shaft: modeled from anthropogenic radiocarbon tracer measurements. American Journal of Physical Anthropology 133: 783-895.
31. Hedges REM, Millard AR. 1995. Measurements and relationships of diagenetic alteration of bone from thee archaeological sites. Journal of Archaeological Science 22: 201-209.
32. Hedges REM, Reynard L. 2007. Nitrogen isotopes and the trophic level of humans in archaeology. Journal of Archaeological Science 34: 1240-1251.
33. Hemminga MA, Mateo MA. 1996. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Marine Ecology Progress Series 140: 285-298.
34. Hu Y, Ambrose SH, Wang C. 2006. Stable isotopic analysis of human bones from Jiahu site, Henan, China: implications for the transition to agriculture. Journal of Archaeological Science 33: 1319-1330.
35. Iacumin P, Nikolaev V, Ramigni M. 2000. C and N stable isotope measurements on Eurasian fossil mammals, 40,000 to 10,000 years BP: Herbivore physiologies and palaeoenvironmental reconstruction. Palaeogeography, Palaeoclimatolatology, Palaeoecology 163: 33-47.
36. Jim S, Ambrose SH, Evershed RP. 2004. Stable carbon isotopic evidence for differences in the dietary origin of bone cholesterol, collagen and apatite: implications for their use in palaeodietary reconstruction. Geochimica et Cosmochimica Acta 68: 61-72.
37. Jim S, Jones V, Ambrose SH, Evershed RP. 2006. Quantifying dietary macronutrient sources of carbon for bone collagen biosynthesis using natural abundance stable carbon isotope analysis. British Journal of Nutrition 95: 1055-1062.
38. Kellner CM, Schoeninger MJ. 2007. A simple carbon isotope model for reconstructing prehistoric human diet. American Journal of Physical Anthroplogy 133: 1112-1127.
39. Kelly JF. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78: 1-27.
40. Koch PL. 1991. The isotopic ecology of Pleistocene proboscideans. Journal of Vertebrate Paleontology 11: 40A.
41. Koch PL. 2007. Isotopic study of the biology of modern and fossil vertebrates. In Stable Isotopes in Ecology and Environmental Science, 2nd edn, Michener R, Lajtha K (eds). Blackwell Publishing: Boston; 99-154.
42. Koch PL, Behrensmeyer AK, Stott AW, Tuross N, Evershed RP, Fogel ML. 2001. The effects of weathering on the stable isotope composition of bones. Ancient Biomolecules 3: 117-134.
43. Koch PL, Fogel ML, Tuross N. 1994. Tracing the diets of fossil animals using stable isotopes. In Stable Isotopes in Ecology and Environmental Science, Lajtha K, Michener RH (eds). Blackwell: Oxford; 63-92.
44. Kohn MJ, Cerling TE. 2002. Stable isotope compositions of biological apatite. In Phosphates: Geochemical, Geobiological, and Materials Importance (Reviews in Mineralogy and Geochemistry 48), Kohn MJ, Rakovan J, Hughes JM (eds). Mineralogical Society of America and The Geochemical Society 455-488.
45. Kohn MJ, McKay MP, Knight JL. 2005. Dining in the Pleistocene-who's on the menu? Geology 33: 649-652.
46. Krueger HW, Sullivan CH. 1984. Models for carbon isotope fractionation between diet and bone. American Chemical Society Symposium Series, Stable Isotopes in Nutrition 258: 205-220.
47. Lee-Thorp JA. 2000. Preservation of biogenic carbon isotope signals in Plio-Pleistocene bone and tooth mineral. In Biogeochemical Approaches to Paleodietary Analysis, Ambrose S, Katzenberg KA (eds). Plenum Press: New York; 89-116.
48. Lee-Thorp JA, Sealy JC, van der Merwe NJ. 1989. Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. Journal of Archaeological Science 16: 595-599.
49. Leggett K. 2004. Coprophagy and unusual thermoregulatory behaviour in desert-dwelling elephants of north-western Namibia. Pachyderm 36: 113-115.
50. MacDonald-Beyers K, Labisky RF. 2005. Influence of flood waters on survival, reproduction, and habitat use of white-tailed deer in the Florida Everglades. Wetlands 25: 659-666.
51. Martínez del Rio C, Wolf N, Carleton SA, Gannes L.Z. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91-111.
52. 15N and animal age. Geochimica et Cosmochimica Acta 48: 1135-1140.
53. Newsome SD, Phillips PL, Culleton BJ, Guilderson TP, Koch PL. 2004. Dietary reconstruction of an early to middle Holocene human population from the central California coast: insights from advanced stable isotope mixing models. Journal of Archaeological Science 31: 1101-1115.
54. 2, and bioapatite in different mammals. Journal of Archaeological Science 32: 1459-1470.
55. Person A, Bocherens H, Saliége J, Paris F, Zeitoun V, Gérard V. 1995. Early diagenetic evolution of bone phosphate: an X-ray diffractometry analysis. Journal of Archaeological Science 22: 211-221.
56. Peterson RO. 1977. Wolf ecology and prey relationships on Isle Royale. U.S. National Park Service Scientific Monograph Series 11.
57. Post DM. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718.
58. Raven JA, Johnston AM, Kubler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH. 2002. Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrass. Functional Plant Biology 29: 355-378.
59. Rees PA. 1982. Gross assimilation efficiency and food passage time in the African elephant. African Journal of Ecology 20: 147-222.
60. Robbins CT, Felicetti LA, Sponheimer M. 2005. The effects of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144: 534-540.
61. 12C ratios in bone collagen and strontium levels in bone mineral. Journal of Human Evolution 14: 515-525.
62. 2 of cows, sheep and camels. Isotopes in Environmental and Health Studies 34: 75-79.
63. Smith DW, Peterson RO, Houston DB. 2003. Yellowstone after wolves. BioScience 53: 330-340.
64. 14N preferentially excreted? Journal of Archaeological Science 30: 1649-1655.
65. Taheruzzaman Q, Kushari DP. 1989. Evaluation of some common aquatic macrophytes cultivated in enriched water as possible source of protein and biogas. Hydrobiologia Bulletin 23: 207-212.
66. Thewissen JGM, Williams EM, Roe LJ, Hussain ST. 2001. Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413: 277-281.
67. Thurber JM, Peterson RO. 1993. Effects of population density and pack size on the foraging ecology of gray wolves. Journal of Mammalogy 74: 879-889.
68. 2, bone collagen, bioapatite, and soft tissues. In Prehistoric Human Bone-Archaeology at the Molecular Level, Lambert JB, Grupe G (eds). Springer-Verlag: Berlin; 121-155.
69. Trueman CNG, Behrensmeyer AK, Tuross N, Weiner S. 2004. Mineralogical and compositional changes in bones exposed on soil surfaces in Amboseli National Park, Kenya: diagenetic mechanisms and the role of sediment pore fluids. Journal of Archaeological Science 31: 721-739.
70. Trueman CNG, Privat K, Field J. 2008. Why do crystallinity values fail to predict the extent of diagenetic alteration of bone mineral? Palaeogeography, Palaeoclimatology, Palaeoecology 266: 160-167.
71. van Geel B, Aptroot A, Baittinger C, Birks HH, Bull ID, Cross HB, Evershed RP, Gravendeel B, Kompanje EJO, Kuperus P, Mol D, Nierop KGJ, Pals JP, Tikhonov AN, van Reenen G, van Tienderen PH. 2008. The ecological implications of a Yakutian mammoth's last meal. Quaternary Research 69: 361-376.
72. van Vuren D, Coblentz BE. 1987. Some ecological effects of feral sheep on Santa Cruz Island, California, USA. Biological conservation 41: 253-268.
73. Wang Y, Cerling TE. 1994. A model of fossil tooth and bone diagenesis: implications for paleodiet reconstruction from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology 107: 281-289.
74. Wenk C. 2001. The role of dietary fibre in the digestive physiology of the pig. Animal Feed Science and Technology 90: 21-33.
75. Western D, Lindsay WK. 1984. Seasonal herd dynamics of a savanna elephant population. African Journal of Ecology 22: 229-244.
76. Zazzo A, Smith GR, Patterson WP, Dufour E. 2006. Life history reconstruction of modern and fossil sockeye salmon (Oncorhynchus nerka) by oxygen isotopic analysis of otoliths, vertebrae, and teeth: Implication for paleoenvironmental reconstructions. Earth and Planetary Science Letters 249: 200-215.