Stable isotope analysis of well-preserved 120,000-year-old herbivore bone collagen from the Middle Palaeolithic site of Neumark-Nord 2, Germany reveals niche separation between bovids and equids

Palaeogeography, Palaeoclimatology, Palaeoecology

Volumn 333-334, Issue , 2012, Pages 168-177

  Britton, Kate ^a,b   Gaudzinski Windheuser, Sabine ^c   Roebroeks, Wil ^d   Kindler, Lutz ^c   Richards, Michael P ^a,e  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d LEIDEN UNIVERSITY   (Netherlands)

^e Department of Anthropology ^*  (Canada)

Author keywords

Bone collagen; Diet; Herbivores; Palaeoecology; Resource partitioning; Stable isotopes

Indexed keywords

ARCHAEOLOGY; BONE; CARBON ISOTOPE; COLLAGEN; DATA SET; FEEDING ECOLOGY; FOOD PREFERENCE; HERBIVORE; INTERGLACIAL; ISOTOPIC ANALYSIS; NICHE PARTITIONING; NITROGEN ISOTOPE; PALEOECOLOGY; PALEOLITHIC; PLEISTOCENE; PRESERVATION; SPECIES DIVERSITY; STABLE ISOTOPE; UNGULATE;

GERMANY;

BOVIDAE; EQUIDAE; EQUUS;

EID: 84860433698     PISSN: 00310182     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.palaeo.2012.03.028     Document Type: Article

References (106)

1. Ambrose S.H. Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science 1990, 17:431-451.
2. Balasse M., Tresset A. Early weaning of Neolithic domestic cattle (Bercy, France) revealed by intra-tooth variation in nitrogen isotope ratios. Journal of Archaeological Science 2002, 29:853-859.
3. Balasse M., Bocherens H., Mariotti A. Intra-bone variability of collagen and apatite isotopic composition used as evidence of a change of diet. Journal of Archaeological Science 1999, 26:593-598.
4. Ben-David M., Shochat E., Adams L.G. Utility of stable isotope analysis in studying foraging ecology of herbivores: examples from moose and caribou. Alces 2001, 37:421-434.
5. Bocherens H. Isotopic biogeochemistry and the palaeoecology of the mammoth steppe fauna. DEINSEA-Annual of the Natural History Museum Rotterdam 2003, 9:57-76.
6. Bocherens H., Drucker D. Trophic level isotopic enrichment of carbon and nitrogen in bone collagen: case studies from recent and ancient terrestrial ecosystems. International Journal of Osteoarchaeology 2003, 13:46-53.
7. Bocherens H., Fogel M.L., Tuross N., Zeder M. Trophic structure and climatic information from isotopic signatures in Pleistocene cave fauna of Southern England. Journal of Archaeological Science 1995, 22:327-340.
8. Bocherens H., Billiou D., Patou-Mathis M., Bonjean D., Otte M., Mariotti A. Paleobiological implications of the isotopic signatures (C-13, N-15) of fossil mammal collagen in Scladina cave (Sclayn, Belgium). Quaternary Research 1997, 48:370-380.
9. Bocherens H., Billiou D., Mariotti A., Patou-Mathis M., Otte M., Bonjean D., Toussaint M. Palaeonvironmental and palaeodietary implications of isotopic biogeochemistry of last interglacial Neanderthal and mammal bones in Scladina Cave (Belgium). Journal of Archaeological Science 1999, 26:599-607.
10. Bocherens H., Billiou D., Mariotti A., Toussaint M., Patou-Mathis M., Bonjean D., Otte M. New isotopic evidence for dietary habits of Neandertals from Belgium. Journal of Human Evolution 2001, 40:497-505.
11. Bocherens H., Drucker D.G., Billiou D., Patou-Mathis M., Vandermeersch B. Isotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal: review and use of a multi-source mixing model. Journal of Human Evolution 2005, 49:71-87.
12. Bogaard A., Heaton T.H.E., Poulton P., Merbach I. The impact of manuring on nitrogen isotope ratios in cereals: archaeological implications for reconstruction of diet and crop management practices. Journal of Archaeological Science 2007, 34:335-343.
13. Britton K., Grimes V., Niven L., Steele T., Mcpherron S., Soressi M., Kelly T.E., Jaubert J., Hublin J.-J., Richards M.P. Strontium isotope evidence for migration in late Pleistocene Rangifer: implications for Neanderthal hunting strategies at the Middle Palaeolithic site of Jonzac, France. Journal of Human Evolution 2011, 61:176-185.
14. Brown T.A., Nelson D.E., Vogel J.S., Southon J.R. Improved collagen extraction by modified Longin method. Radiocarbon 1988, 30:171-177.
15. Casey M.M., Post D.M. The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 2011, 106:131-148.
16. 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, 120:337-363.
17. Cerling T., Harris J.M., Leakey M.G. Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia 1999, 120:364-374.
18. Cerling T.E., Hart J.A., Hart T.B. Stable isotope ecology in the Ituri Forest. Oecologia 2004, 138:5-12.
19. 15N in soils and plants from chemically and organically fertilized uplands. Soil Biology and Biochemistry 2003, 35:1493-1500.
20. Cleveringa P., Meijer T., Van Leeuwen R.J.W., De Wolf H., Pouwer R., Lissenberg T., Burger A.W. The Eemian type locality at Amersfoort in the central Netherlands: redeployment of old and new data. Geologie en Mijnbouw / Netherlands Journal of Geosciences 2000, 79 (2/3):197-216. T. Van Kolfschoten, P.L. Gibbard (Eds.).
21. Cloern J.E., Canuel E.A., Harris D. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 2002, 47:713-729.
22. Collins M.J., Galley P. Towards an optimal method of archaeological collagen extraction: the influence of pH and grinding. Ancient Biomolecules 1998, 2:209-222.
23. Collins M.J., Nielsen-Marsh C.M., Hiller J., Smith C.I., Roberts J.P., Prigodich R.V., Wess T.J., Csapò J., Millard A.R., Turner-Walker G. The survival of organic matter in bone: a review. Archaeometry 2002, 44:383-394.
24. Coltrain J.B., Harris J.M., Cerling T.E., Ehleringer J.R., Dearing M.-D., Ward J., Allen J. Rancho La Brea stable isotope biogeochemistry and its implications for the palaeoecology of late Pleistocene, coastal southern California. Palaeogeography, Palaeoclimatology, Palaeoecology 2004, 205:199-219.
25. Crutzen P.J., Aslemann I., Seiler W. Methane production by domestic animals, wild ruminants, and other herbivorous fauna, and humans. Tellus 1986, 38B:271-284.
26. Deniro M.J. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 1985, 317:806-809.
27. Deniro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 1978, 42:495-506.
28. Dobberstein R.C., Collins M.J., Craig O.E., Taylor G., Penkman K.E.H., Ritz-Timme S. Archaeological collagen: why worry about collagen diagenesis?. Archaeological and Anthropological Sciences 2009, 1:31-42.
29. Drucker D., Bocherens H., Pike-Tay A., Mariotti A. Isotopic tracking of seasonal dietary change in dentine collagen: preliminary data from modern caribou. Earth and Planetary Sciences 2001, 333:303-309.
30. Drucker D.G., Bocherens H., Billiou D. Evidence for shifting environmental conditions in Southwestern France from 33000 to 15000years ago derived from carbon-13 and nitrogen-15 natural abundances in collagen of large herbivores. Earth and Planetary Science Letters 2003, 216:163-173.
31. 15N) isotopes in mandibles of modern caribou of Qamanirjuaq (Rangifer tarandus groenlandicus) and Banks Island (Rangifer tarandus pearyi): Implications for tracing seasonal and temporal changes in diet. International Journal of Osteoarchaeology 2010, 10.1002/oa.1220.
32. Eissman L. Quaternary geology of the eastern Germany (Saxony, Saxon-Anhalt, South Brandenburg, Thüringia), type area of the Elsterian and Saalian Stages in Europe. Quaternary Science Reviews 2002, 21:1275-1346.
33. Evans R.D. Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 2001, 6:121-126.
34. Feranec R.S. Stable carbon isotope values reveal evidence of resource partitioning among ungulates from modem C-3-dominated ecosystems in North America. Palaeogeography, Palaeoclimatology, Palaeoecology 2007, 252:575-585.
35. Feranec R.S., Hadly E.A., Paytan A. Determining landscape use of Holocene mammals using strontium isotopes. Oecologia 2007, 153:943-950.
36. Feranec R., Garcia N., Diez J.C., Arsuaga J.L. Understanding the ecology of mammalian carnivorans and herbivores from Valdegoba cave (Burgos, northern Spain) through stable isotope analysis. Palaeogeography, Palaeoclimatology, Palaeoecology 2010, 297:263-272.
37. Fizet M., Mariotti A., Bocherens H., Langebadre B., Vandermeersch B., Borel J.P., Bellon G. Effect of diet, physiology and climate on carbon and nitrogen stable isotopes of collagen in a late Pleistocene anthropic palaeoecosytem-Marillac, Charente, France. Journal of Archaeological Science 1995, 22:67-79.
38. Gadbury C., Todd L., Jahren A.H., Amundson R. Spatial and temporal variations in the isotopic composition of bison tooth enamel from the Early Holocene Hudson-Meng Bone Bed, Nebraska. Palaeogeography, Palaeoclimatology, Palaeoecology 2000, 157:79-93.
39. Grogan P., Bruns T.D., Chapin F.S. Fire effects on ecosystem nitrogen cycling in a Californian bishop pine forest. Oecologia 2000, 122:537-544.
40. Guthrie R.D. Mammals of the mammoth steppe as paleoenvironmental indicators. Paleoecology of Beringia 1982, 307-326. Academic Press, New York. D.M. Hopkins, J.V.J. Matthews, C.E. Schweger, S.B. Young (Eds.).
41. Gwynne M.D., Bell R.H.V. Selection of vegetation components by grazing ungulates in the Serengeti National Park. Nature 1968, 220:390-393.
42. 14N ratios of plants in South Africa and Namibia: relationship to climate and coastal/saline environments. Oecologia 1987, 74:236-246.
43. 12C ratios of C3 plants: implications for palaeodiet studies. Journal of Archaeological Science 1999, 26:637-649.
44. Heaton T.H.E., Vogel J.C., Von La Chevallerie G., Collett G. Climatic influence on the isotopic composition of bone nitrogen. Nature 1986, 322:822-823.
45. Hedges R.E.M., Millard A.R. Bones and groundwater: towards the modelling of diagenetic processes. Journal of Archaeological Science 1995, 22:155-164.
46. Hedges R.E.M., Stevens R.E., Richards M.P. Bone as a stable isotope archive for local climatic information. Quaternary Science Reviews 2004, 23:959-965.
47. Hicks B.J., Wipfli M.S., Lang D.W., Lang M.E. Marine-derived nitrogen and carbon in freshwater-riparian food webs of the Copper River Delta, southcentral Alaska. Oecologia 2005, 144:558-569.
48. 15N and nitrogen concentrations may indicate plant-mycorrhizial interactions. Oecologia 2000, 122:273-283.
49. Hoppe K.A., Koch P.L., Carlson R.W., Webb D.S. Tracking mammoths and mastodons: reconstruction of migratory behaviour using strontium isotope ratios. Geology 1999, 27:439-442.
50. Hoppe K.A., Stover S.M., Pascoe J.R., Amundson R. Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeography, Palaeoclimatology, Palaeoecology 2004, 206:355-365.
51. Janis C. The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 1976, 30:757-774.
52. Jans M.M.E., Nielsen-Marsh C.M., Smith C.I., Collins M.J., Kars H. Characterisation of microbial attack on archaeological bone. Journal of Archaeological Science 2004, 31:87-95.
53. Jones A.M., O'connell T.C., Young E.D., Scott K., Buckingham C.M., Iacumin P., Brasier M.D. Biogeochemical data from well preserved 200ka collagen and skeletal remains. Earth and Planetary Science Letters 2001, 193:143-149.
54. Keppel G., Wickens T.D. Design and Analysis: A Researcher's Handbook 2004, Pearson Prentice Hall, Upper Saddle River.
55. Koch P.L., Heisinger J., Moss C., Carlson R.W., Fogel M.L., Behrensmeyer A.K. Isotopic tracking of change in diet and habitat use in African elephants. Science 1995, 267:1340-1343.
56. Koch P.L., Hoppe K.A., Webb D.S. The isotopic ecology of late Pleistocene mammals in North America. Part 1: Florida. Chemical Geology 1998, 152:119-138.
57. Kohn M.J. You are what you eat. Science 1999, 283:335-336.
58. Krysl L.J., Hubbert M.E., Sowell B.F., Plumb G.E., Jewett T.K., Smith M.A., Waggoner J.W. Horses and cattle grazing in the Wyoming Red Desert, I. Food habits and dietary overlap. Journal of Range Management 1984, 31:72-76.
59. Laurat T., Brühl E. Zum Stand der archäologischen Untersuchungen im Tagebau Neumark-Nord, Ldkr. Jahresschrift für Mitteldeutsche Vorgeschichte 2006, 90:9-69.
60. Lee-Thorp J., Van Der Merwe N.J. Carbon isotope analysis of fossil bone apatite. South African Journal of Science 1987, 83:712-715.
61. Livingston H.G., Payne W.J.A., Friends M.T. Urea extretion in ruminants. Nature 1962, 194:1057-1058.
62. Longin R. New method of collagen extraction for radiocarbon dating. Nature 1971, 230:241-242.
63. Macfadden B.J. Geographic variation in diets of ancient populations of 5-million-year-old (early Pliocene) horses from southern North America. Palaeogeography, Palaeoclimatology, Palaeoecology 2008, 266:83-94.
64. Maguas C., Brugnoli E. Spatial variation in carbon isotope discrimintation across the thalli of several lichen species. Plant, Cell & Environment 1996, 19:437-446.
65. Mania D., Mania U. La stratigraphie et le Paléolithique du complexe saalien dans la région de la Saale et de l'Elbe. L'Anthropologie 2008, 112:15-47.
66. Mania D., Thomae M., Litt T., Weber T. Neumark-Gröbern: Beiträge zur Jagd des mittelpaläolithischen Menschen. Veröffentlichungen des Landesmuseum für Vorgeschichte in Halle 43 1990.
67. Menard C., Duncan P., Fleurance G., Georges J.Y., Lila M. Comparative foraging and nutrition of horses and cattle in European wetlands. Journal of Applied Ecology 2002, 39:120-133.
68. Menke B., Tynni R. Das Eeminterglazial und das Weichselfrühglazial von Rederstall/Dittmarschen und ihre Bedeutung für die mitteleuropäische Jungpleistozängliederung. Geoogisches Jahrbuch 1984, A76:3.
69. Nadelhoffer K.J., Fry B. Nitrogen isotope studies in forest ecosystems. Stable isotopes in ecology and environmental science 1994, Blackwell, Oxford, pp. K. Lajtha, R.H. Michener (Eds.).
70. 15N natural abundances and N use by tundra plants. Oecologia 1996, 107:386-394.
71. Nielsen-Marsh C.M., Hedges R.E.M. Patterns of diagenesis in bone I: The effects of site environments. Journal of Archaeological Science 2000, 27:1139-1150.
72. Nielsen-Marsh C.M., Gernaey A., Turner-Walker G., Hedges R.E.M., Pike A., Collins M. The chemical degradation of bone. Human Osteology in Archaology and Forensic Science 2000, 439-454. GMM, London. M. Cox, S. Mays (Eds.).
73. Nielsen-Marsh C.M., Smith C.I., Jans M., Nord A., Kars H., Collins M.J. Bone diagenesis in the European Holocene II: taphonomic and environmental considerations. Journal of Archaeological Science 2007, 34:1523-1531.
74. 13C stable isotopes. Journal of Archaeological Science 2005, 32:855-871.
75. Park R., Epstein S. Carbon isotope fractionation during photosynthesis. Geochimica et Cosmochimica Acta 1960, 21:110-126.
76. Pellegrini M., Donahue R.E., Chenery C., Evans J., Lee-Thorp J., Montgomery J., Mussi M. Faunal migration in late-glacial central Italy: implications for human resource exploitation. Rapid Communications in Mass Spectrometry 2008, 22:1714-1726.
77. Richards M.P., Hedges R.E.M. Variations in bone collagen delta C-13 and delta N-15 values of fauna from Northwest Europe over the last 40000years. Palaeogeography, Palaeoclimatology, Palaeoecology 2003, 193:261-267.
78. Richards M.P., Pettitt P.B., Trinkaus E., Smith F.H., Paunovic M., Karavanic I. Neanderthal diet at Vindija and Neanderthal predation: the evidence from stable isotopes. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:7663-7666.
79. Richards M.P., Taylor G., Steele T., Mcpherron S.P., Soressi M., Jaubert J., Orschiedt J., Mallye J.B., Rendu W., Hublin J.J. Isotopic dietary analysis of a Neanderthal and associated fauna from the site of Jonzac (Charente-Maritime), France. Journal of Human Evolution 2008, 55:179-185.
80. Ryden H. America's Last Wild Horses 1972, Ballantine Books, New York.
81. Schaller G.B. Wildlife of the Tibetan Steppe 1998, University of Chicago Press, Chicago.
82. Schmidt-Nielsen B. Urea excretion in mammals. Physiological Reviews 1958, 38:139-168.
83. Schoeninger M.J., Deniro M.J. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 1984, 48:625-639.
84. 15N enrichment in the Sahara: in search of a global relationship. Journal of Archaeological Science 1999, 26:629-636.
85. Schwertl M., Auerswald K., Schäufele R., Schnyder H. Carbon and nitrogen stable isotope composition of cattle hair: ecological fingerprints of production systems?. Agriculture, Ecosystems and Environment 2005, 109:153-165.
86. 15N abundance. Australian Journal of Plant Physiology 1986, 13:699-757.
87. Sier M.J., Roebroecks W., Bakels C.C., Dekkers M.J., Bruhl E., De Loecker D., Gaudzinski-Windheuser S., Hesse N., Jagich A., Kindler L., Kuijper W.J., Laurat T., Mücher H.J., Penkman K.E., Richter D., Van Hinsbergen D.J. Direct terrestrial-marine correlation demonstrates suprisingly late onset of the last interglacial in Central and Northwestern Europe. Quaternary Research 2011, 75:213-218.
88. Slade L.M., Robinson D.W., Casey K.E. Nitrogen metabolism in non ruminant herbivores. 1-The influence of non protein nitrogen and protein quality on the nitrogen retention of adult mares. Journal of Animal Science 1970, 30:753-760.
89. Smith B.N., Epstein S. Biogeochemistry of the stable isotopes of hydrogen and carbon in salt marsh biota. Plant Physiology 1970, 46:738-742.
90. Smith C.I., Nielsen-Marsh C.M., Jans M.M.E., Collins M.J. Bone diagenesis in the European Holocene I: patterns and mechanisms. Journal of Archaeological Science 2007, 34:1485-1493.
91. Smuts G.L. Interrelations between predators, prey, and their environment. Bioscience 1978, 28:316-320.
92. 15N values from a controlled feeding study. International Journal of Osteoarchaeology 2003, 13:80-87.
93. 15N for tracer studies. Journal of Agricultural Science 1978, 90:7-9.
94. Stevens R.E., Hedges R.E.M. Carbon and nitrogen stable isotope analysis of northwest European horse bone and tooth collagen, 40,000 BP-present: Palaeoclimatic interpretations. Quaternary Science Reviews 2004, 23:977-991.
95. Stevens R.E., Jacobi R., Street M., Germonpre M., Conard N.J., Munzel S.C., Hedges R.E.M. Nitrogen isotope analyses of reindeer (Rangifer tarandus), 45,000BP to 900BP: palaeoenvironmental reconstructions. Palaeogeography, Palaeoclimatology, Palaeoecology 2008, 262:32-45.
96. Strahl J., Krbetschek M.R., Luckert J., Machalett B., Meng S., Oches E.A., Rappsilber I., Wansa S., Zöller L. Geologie, Paläontologie und Geochronologie des Eem-Beckens Neumark-Nord 2 und Vergleich mit dem Becken Neumark-Nord 1 (Geiseltal, Sachsen-Anhalt). E&G Quaternary Science Journal 2010, 59:120-167.
97. 15N of Pleistocene mammoths: implications for paleoecology of the mammoth steppe. Palaeogeography, Palaeoclimatology, Palaeoecology 2010, 286:88-96.
98. Teeri J.A. Stable carbon isotope analysis of mosses and lichens growing in xeric and moist habitats. The Bryologist 1981, 84:82-84.
99. Van Der Merwe N.J., Medina E. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. Journal of Archaeological Science 1991, 18:249-259.
100. Van Groenigen J.-W., Van Kessel C. Salinity-induced patterns of natural abundance carbon-13 and nitrogen-15 in plant and soil. Soil Science Society of America Journal 2002, 66:489-498.
101. Van Klinken G.J. Bone collagen quality indicators for palaeodietary and radiocarbon measurements. Journal of Archaeological Science 1999, 26:687-695.
102. Van Klinken G.J., Richards M.P., Hedges R.E.M. An overview of causes for stable isotopic variations in past European human populations: environmental, ecophysiological, and cultural effects. Biogeochemical Approaches to Palaeodietary Analysis 2000, 39-63. Kluwer Academic/Plenum publishers, New York. S. Ambrose, A. Katzenberg (Eds.).
103. Van Leeuwen R.J., Beets D., Bosch J.H.A., Burger A.W., Cleveringa P., Van Harten D., Herngreen G.F.W., Langereis C.G., Meijer T., Pouwer R., De Wolf H. Stratigraphy and integrated facies analysis of the Eemian in the Amsterdam-Terminal borehole, the Netherlands. Geologie en Mijnbouw/Netherlands Journal of Geosciences 2000, 79 (2/3):161-196. T. Van Kolfschoten, P.L. Gibbard (Eds.).
104. 2-fixing plants from selected ecosystems. Oecologia (Berlin) 1982, 54:317-325.
105. 86Sr analyses of tooth enamel carbonate. Quaternary Research 2010, 73:449-463.
106. Zagwijn W.H. Vegetation, climate and radiocarbon datings in the Late Pleistocene of The Netherlands, Part I: Eemian and Early Weichselian. Mededelingen Geologische Stichting 1961, 14:15-45.