Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-28T05:51:02.126Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal variation in kangaroo tooth enamel oxygen and carbon isotopes in southern Australia

Published online by Cambridge University Press:  20 June 2012

Tom H. Brookman  and
Stanley H. Ambrose
Tom H. Brookman*
Affiliation:
School of Geographical and Environmental Studies, University of Adelaide, South Australia 5005, Australia
Stanley H. Ambrose
Affiliation:
Department of Anthropology, University of Illinois, 109 Davenport Hall, 607 South Mathews Avenue, Urbana, IL 61801, USA
*
⁎Corresponding author at: Department of Geological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand. Fax: + 64 33642769. Email Address:[email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Serial sampling of tooth enamel growth increments for carbon and oxygen isotopic analyses of Macropus (kangaroo) teeth was performed to assess the potential for reconstructing paleoseasonality. The carbon isotope composition of tooth enamel apatite carbonate reflects the proportional intake of C3 and C4 vegetation. The oxygen isotopic composition of enamel reflects that of ingested and metabolic water. Tooth enamel forms sequentially from the tip of the crown to the base, so dietary and environmental changes during the tooth's formation can be detected. δ13C and δ18O values were determined for a series of enamel samples drilled from the 3rd and 4th molars of kangaroos that were collected along a 900 km north–south transect in southern Australia. The serial sampling method did not yield pronounced seasonal isotopic variation patterns in Macropus enamel. The full extent of dietary isotopic variation may be obscured by attenuation of the isotopic signal during enamel mineralisation. Brachydont (low-crowned) Macropus teeth may be less sensitive to seasonal variation in isotopic composition due to time-averaging during mineralisation. However, geographic variations observed suggest that there may be potential for tracking latitudinal shifts in vegetation zones and seasonal environmental patterns in response to climate change.

Keywords

Carbon isotopesOxygen isotopesSeasonalityKangarooTooth enamelPaleoclimateAustralia
Type
Articles
Information
Quaternary Research , Volume 78 , Issue 2 , September 2012 , pp. 256 - 265
Copyright
University of Washington

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ambrose, S.H. Isotopic analysis of paleodiets: methodological and interpretive considerations. Sandford, M.K. Investigations of Ancient Human Tissue: Chemical Analyses in Anthropology. (1993). Gordon and Breach, Langhorne. 59–130.Google Scholar
Ambrose, S.H., and Norr, L. Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. Lambert, J.B., and Grupe, G. Prehistoric Human Bone — Archaeology at the Molecular Level. (1993). Springer-Verlag, New York. 1–37.Google Scholar
Ayliffe, L.K., and Chivas, A.R. Oxygen isotope composition of the bone phosphate of Australian kangaroos: potential as a palaeoenvironmental recorder. Geochimica et Cosmochimica Acta 54, (1990). 2603–2609.Google Scholar
B.O.M., Climate of South Australia. Australian Government, Bureau of Meteorology. http://www.bom.gov.au/lam/climate/levelthree/ausclim/ausclimsa.htm(2008). Google Scholar
Bailey, P.T., Martensz, P.N., and Barker, R. The red kangaroo, Megalia rufa (Desmarest), in north-western New South Wales. CSIRO Wildlife Research 16, (1971). 29–39.CrossRefGoogle Scholar
Balasse, M. Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling. International Journal of Osteoarchaeology 12, (2002). 155–165.Google Scholar
Balasse, M. Potential biases in sampling design and interpretation of intra-tooth isotope analysis. International Journal of Osteoarchaeology 13, (2003). 3–10.Google Scholar
Balasse, M., Ambrose, S.H., Smith, A.B., and 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. Journal of Archaeological Science 29, (2002). 917–932.CrossRefGoogle Scholar
Balasse, M., Smith, A.B., Ambrose, S.H., and Leigh, S.R. Determining sheep birth seasonality by analysis of tooth enamel oxygen isotope ratios: the Late Stone Age site of Kasteelberg (South Africa). Journal of Archaeological Science 29, (2003). 917–932.Google Scholar
Balasse, M., Tresset, A., Dobney, K., and Ambrose, S.H. The use of isotope ratios to test for seaweed eating in sheep. Journal of the Zoological Society of London 266, (2005). 283–291.Google Scholar
Balasse, M., Tresset, A., and Ambrose, S.H. Stable isotope evidence (δ13C, δ18O) for winter feeding on seaweed by Neolithic sheep of Scotland. Journal of Zoology 270, (2006). 170–176.Google Scholar
Bryant, D., and Froelich, P. A model of oxygen isotope fractionation in body water of large mammals. Geochimica et Cosmochimica Acta 59, (1995). 4523–4537.CrossRefGoogle Scholar
Buchmann, N., Guehl, J.M., Barigah, T.S., and Ehleringer, J.R. Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110, (1997). 120–131.CrossRefGoogle Scholar
Caughley, G., Brown, B., Dostine, P., and Grice, D. The grey kangaroo overlap zone. Australian Wildlife Research 11, (1984). 1–10.Google Scholar
Cerling, T.E., and Harris, J.M. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, (1999). 347–363.CrossRefGoogle ScholarPubMed
Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quade, J., Eisenmann, V., and Ehleringer, J.R. Global vegetation change through the Miocene/Pliocene boundary. Nature 389, (1997). 153–158.Google Scholar
Cerling, T.E., Harris, J.M., and Passey, B.H. Diets of East African bovidae based on stable isotope analysis. Journal of Mammalogy 84, (2003). 456–470.Google Scholar
Clementz, M.T., Koch, P.L., and Beck, C.A. Diet induced differences in carbon isotope fractionation between sirenians and terrestrial ungulates. Marine Biology 151, (2007). 1773–1784.Google Scholar
Codron, D., Lee-Thorp, J.A., Sponheimer, M., de Ruiter, D., and Codron, J. What insights can baboon feeding ecology provide for early hominin niche differentiation?. International Journal of Primatology 29, (2008). 757–772.Google Scholar
Connin, S.L., Betancourt, J., and Quade, J. Late Pleistocene C4 plant dominance and summer rainfall in the southwestern United States from isotopic study of herbivore teeth. Quaternary Research 50, (1998). 179–193.Google Scholar
Coplen, T.B., Kendall, C., and Hopple, J. Comparison of stable isotope reference samples. Nature 302, (1983). 236–238.Google Scholar
Craig, H. Isotopic variation in meteoric waters. Science 133, (1961). 1702–1703.Google Scholar
Dansgaard, W. Stable isotopes in precipitation. Tellus 16, (1964). 436–468.CrossRefGoogle Scholar
Darling, W.G., Bath, A.H., Gibson, J.J., and Rozanski, K. Isotopes in water. Leng, M.J. Isotopes in Palaeoenvironmental Research. (2005). Springer, Netherlands. 1–66.Google Scholar
Dawson, T. Kangaroos: Biology of the Largest Marsupial. (1995). University of New South Wales Press, Sydney.Google Scholar
DeNiro, M.J., and Epstein, S. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, (1978). 495–506.Google Scholar
Ealey, E.H.M., Bentley, P.J., and Main, A.R. Studies on water metabolism of the hill kangaroo, Macropus Robustus (Gould), in northwest Australia. Ecology 46, (1965). 473–479.Google Scholar
Farquhar, G.D. On the nature of carbon isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, (1983). 205–226.Google Scholar
Farquhar, G.D., Ehleringer, J.R., and Hubick, K.T. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology 40, (1989). 503–537.Google Scholar
Field, J., and Wroe, S. Aridity, faunal adaptations and Australian Late Pleistocene extinctions. World Archaeology 44, (2012). 56–74.Google Scholar
Francey, R.J., and Farquhar, G.D. An explanation of 13C/12C variations in tree rings. Nature 297, (1982). 28–31.Google Scholar
Fraser, R.A. A Study of Stable Carbon, Nitrogen and Oxygen Isotopes in Modern Marsupial Herbivores. (2005). Australian National University, Google Scholar
Fraser, R.A., Grün, R., Privat, K., and Gagan, M.K. Stable-isotope microprofiling of wombat tooth enamel records seasonal changes in vegetation and environmental conditions in eastern Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 269, (2008). 66–77.Google Scholar
Fricke, H.C., Clyde, W.C., O'Neil, J.R., and Gingerich, P.D. Evidence for rapid climate change in North America during the latest Paleocene thermal maximum: oxygen isotope compositions of biogenic phosphate from Bighorn Basin (Wyoming). Earth and Planetary Science Letters 160, (1998). 193–208.Google Scholar
Hattersley, P.W. The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57, (1983). 113–128.Google Scholar
Hedges, R.E.M., Stevens, R.E., and Koch, P.L. Isotopes in bones and teeth. Leng, M.J. Isotopes in Palaeoenvironmental Research. (2005). Springer, Netherlands. 117–145.Google Scholar
Helliker, B.R., and Ehleringer, J.R. Differential 18O enrichment in C3 versus C4 grasses. Functional Plant Biology 29, (2002). 435–442.Google Scholar
Higgins, P., and MacFadden, B.J. “Amount Effect” recorded in oxygen isotopes of Late Glacial horse (Equus) and bison (Bison) teeth from the Sonoran and Chihuahuan deserts, southwestern United States. Palaeogeography, Palaeoclimatology, Palaeoecology 206, (2004). 337–353.CrossRefGoogle Scholar
Hoppe, K.A., Stover, S.M., Pascoe, J.R., and Amundson, R. Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeography, Palaeoclimatology, Palaeoecology 206, (2004). 355–365.Google Scholar
Hume, I.D. Digestive Physiology and Nutrition of Marsupials. (1982). Cambridge University Press, Cambridge.Google Scholar
Jackson, S. Australian Mammals: Biology and Captive Management. (2003). CSIRO Publishing, Collingwood.Google Scholar
Johnson, B.J., Miller, G.H., Fogel, M.L., Magee, J.W., Gagan, M.K., and Chivas, A.R. 65, 000 years of vegetation change in central Australia and the Australian summer monsoon. Science 284, (1999). 1150–1152.CrossRefGoogle Scholar
Johnson, B.J., Miller, G.H., Magee, J.W., Gagan, M.K., Fogel, M.L., and Quay, P.D. Carbon isotope evidence for an abrupt reduction in grasses coincident with European settlement of Lake Eyre, South Australia. The Holocene 15, (2005). 888–896.CrossRefGoogle Scholar
Kirkpatrick, T.H. Studies of Macropodidae in Queensland; 2. Age estimation in the grey kangaroo, the red kangaroo, the eastern wallaroo and the red-necked wallaby, with notes on dental abnormalities. Queensland Journal of Agricultural and Animal Sciences 22, (1965). 301–317.Google Scholar
Kirkpatrick, T.H. Studies in Macropodidae in Queensland; 8. Age estimation in the red kangaroo (Megaleia rufa (Desmarest)). Queensland Journal of Agricultural and Animal Sciences 27, (1970). 461–462.Google Scholar
Kirkpatrick, T.H. The development of the dentition of Macropus giganteus (Shaw). Australian Mammalogy 2, (1978). 29–36.Google Scholar
Kirkpatrick, T.J. Biology for management. Lavery, H.J. The Kangaroo Keepers. (1985). University of Queensland Press, St Lucia. 135–160.Google Scholar
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). Geochimica et Cosmochimica Acta 68, (2004). 403–405.Google Scholar
Krueger, H.W., and Sullivan, C.H. Models for carbon isotope fractionation between diet and bone. Turnlund, J.R., and Johnson, P.E. Stable Isotopes in Nutrition. American Chemical Society Symposium Series (1984). 205–220.Google Scholar
Lee-Thorp, J.A. Preservation of biogenic carbon isotopic signals in Plio-Pleistocene bone and tooth mineral. Ambrose, S.H., and Katzenberg, M.A. Biogeochemical Approaches to Paleodietary Analysis. (2000). Kluwer Academic/Plenum, New York. 89–115.Google Scholar
Levin, N., Cerling, T.E., Passey, B.J., Harris, J.M., and Ehleringer, J.R. A stable isotope aridity index for terrestrial environments. Proceedings of the National Academy of Sciences of the United States of America 103, (2006). 11201–11205.Google Scholar
Liu, J., Fu, G., Song, X., Charles, S.P., Zhang, Y., Han, D., and Wang, S. Stable isotope compositions in Australian precipitation. Journal of Geophysical Research 115, (2010). D23307 http://dx.doi.org/10.1029/2010JD014403 Google Scholar
Longinelli, A. Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research. Geochimica et Cosmochimica Acta 48, (1984). 385–390.CrossRefGoogle Scholar
Lourandos, H., and David, B. Long-term archaeological and environmental trends: a comparison from Late Pleistocene–Holocene Australia. Kershaw, P., David, B., Tapper, N., Penny, D., and Brown, J. Bridging Wallace's Line: the Environmental and Cultural History and Dynamics of the SE-Asian–Australian Region. (2002). Catena Verlag, Reiskitchen. 307–338.Google Scholar
Marino, B.M., and McElroy, M.B. Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349, (1991). 127–131.Google Scholar
McCullough, D.R., and McCullough, Y. Kangaroos in Outback Australia: Comparative Ecology and Behavior of Three Coexisting Species. (2000). Columbia University Press, New York.Google Scholar
Murphy, B.P., and Bowman, D.M.J.S. Kangaroo metabolism does not cause the relationship between bone collagen δ15N and water availability. Functional Ecology 20, (2006). 1062–1069.Google Scholar
Murphy, B.P., Bowman, D.M.J.S., and Gagan, M.K. The interactive effect of temperature and humidity on the oxygen isotope composition of kangaroos. Functional Ecology 21, (2007). 757–766.Google Scholar
Murphy, B.P., Bowman, D.M.J.S., and Gagan, M.K. Sources of carbon isotope variation in kangaroo bone collagen and tooth enamel. Geochimica et Cosmochimica Acta 71, (2007). 3847–3858.Google Scholar
Murphy, B.P., Williamson, G.J., and Bowman, D.J.S. Did central Australian megafaunal extinctions coincide with abrupt ecosystem collapse or gradual climate change?. Global Ecology and Biogeography 21, (2012). 142–151.Google Scholar
Nelson, S.V. Paleoseasonality inferred from equid teeth and intra-tooth isotopic variability. Palaeogeography, Palaeoclimatology, Palaeoecology 222, (2005). 122–144.Google Scholar
O'Leary, M.H. Carbon isotopes in photosynthesis. Bioscience 38, (1988). 328–336.CrossRefGoogle Scholar
Passey, B.H., and Cerling, T.E. Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series. Geochimica et Cosmochimica Acta 66, (2002). 3225–3234.Google Scholar
Passey, B.H., and Cerling, T.E. Response to the comment by M.J. Kohn on “Tooth enamel mineralization in ungulates: Implications for recovering a primary isotopic time-series”, by B.H. Passey and T.E. Cerling (2002). Geochimica et Cosmochimica Acta 68, (2004). 407–410.Google Scholar
Passey, B.H., and Cerling, T.E. In situ stable isotope analysis (δ13C, δ18O) of very small teeth using laser ablation GC/IRMS. Chemical Geology 235, (2006). 238–249.Google Scholar
Pate, F.D., and Anson, T.J. Stable nitrogen isotope values in arid-land kangaroos correlated with mean annual rainfall: potential as a palaeoclimatic indicator. International Journal of Osteoarchaeology 18, (2008). 317–326.Google Scholar
Pate, F.D., and Krull, E. Carbon isotope discrimination by C3 pasture grasses along a rainfall gradient in South Australia: implications for palaeoecological studies. Quaternary Australasia 14, (2007). 29–33.Google Scholar
Pate, F.D., and Noble, A.H. Geographic distribution of C3 and C4 grasses recorded from stable carbon isotope values of bone collagen of South Australian herbivores. Australian Journal of Botany 48, (2000). 203–207.Google Scholar
Pate, F.D., Anson, T.J., Noble, A.H., and Schoeninger, M.J. Bone collagen stable carbon and nitrogen isotope variability in modern South Australian mammals: a baseline for palaeoecological inferences. Quaternary Australasia 16, (1998). 43–51.Google Scholar
Prideaux, G.J., Ayliffe, L.K., DeSantis, L.R.G., Schubert, B.W., Murray, P.F., Gagan, M.K., and Cerling, T.E. Extinction implications of a chenopod browse diet for a giant Pleistocene kangaroo. Proceedings of the National Academy of Sciences of the United States of America 106, (2009). 11646–11650.Google Scholar
Ramesh, R., Bhattacharya, S.K., and Gopalan, K. Climatic correlations in the stable isotope records of silver fir (Abies pindow) trees from Kashmir, India. Earth and Planetary Science Letters 79, (1986). 66–74.Google Scholar
Roberts, A.L., Pate, D.F., and Hunter, R. Late Holocene climatic changes recorded in macropod bone collagen stable carbon and nitrogen isotopes at Fromm's Landing, South Australia. Australian Archaeology 49, (1999). 48–49.Google Scholar
Roberts, R.G., Flannery, T.F., Ayliffe, L.K., Yoshida, H., Olley, J.M., Prideaux, J.M., Laslett, G.M., Baynes, A., Smith, M.A., Jones, R., and Smith, B.L. New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago. Science 292, (2000). 1888–1892.Google Scholar
Rozanski, K., Araguás-Araguás, L., and Gonfiantini, R. Isotopic patterns in modern global precipitation. Swart, P.K., Lohmann, K.C., McKenzie, J., and Savin, S. Climate Change in Continental Isotopic Records. Geophysical Monograph. (1993). American Geophysical Union, Washington. 1–36.Google Scholar
Rule, S., Brook, B.W., Haberle, S.W., Turney, C.S.M., Kershaw, P.A., and Johnson, C.S. The aftermath of megafaunal extinction: ecosystem transformation in Pleistocene Australia. Science 335, (2012). 1483–1486.Google Scholar
Schwerdtfeger, P., and Curran, E. Climate of the Flinders Ranges. Davies, M., Twidale, C.R., and Tyler, M.J. Natural History of the Flinders Ranges. (1996). Royal Society of South Australia, Adelaide. 63–75.Google Scholar
Sponheimer, M., Passey, B.H., de Ruiter, D.J., Guatelli-Steinberg, D., Cerling, T.E., and Lee-Thorp, J.A. Isotopic evidence for dietary variability in the early Hominin Paranthropus robustus . Science 314, (2006). 980–982.Google Scholar
Tieszen, L.L. Natural variations in the carbon isotope values of plants: implications for archaeology, ecology, and paleoecology. Journal of Archaeological Science 18, (1991). 227–248.Google Scholar
Tieszen, L.L., and Fagre, T. Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite and soft tissue experiments. Lambert, J.B., and Grupe, G. Molecular Archaeology of Prehistoric Human Bone. (1993). Springer, Berlin. 121–155.Google Scholar
van der Merwe, N.J., and Medina, E. Photosynthesis and 13C/12C in Amazonian rain forests. Geochimica et Cosmochimica Acta 53, (1989). 1091–1094.Google Scholar
Wang, Y., and Cerling, T.E. A model of fossil tooth and bone diagenesis: implications for paleodiet reconstruction from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology 107, (1994). 281–289.CrossRefGoogle Scholar
Wang, Y., Kromhout, E., Zhang, C., Xy, Y., Parker, W., Deng, T., and Qiu, Z. Stable isotopic variations in modern herbivore tooth enamel, plants and water on the Tibetan Plateau: implications for paleoclimate and paleoelevation reconstructions. Palaeogeography, Palaeoclimatology, Palaeoecology 260, (2008). 359–374.Google Scholar
Warriner, C., and Tuross, N. Alkaline cooking and stable isotope diet-tissue discrimination in swine: archaeological implications. Journal of Archaeological Science 36, (2009). 1690–1697.Google Scholar
Wilson, G.R. Age structures of populations of kangaroos (Macropodidae) taken by professional shooters in New South Wales. Australian Wildlife Research 2, (1975). 1–9.Google Scholar
Yakir, D. Variations in the natural abundance of oxygen-18 and deuterium in plant carbohydrates. Plant, Cell & Environment 15, (1992). 1005–1020.Google Scholar
Zazzo, A., Balasse, M., and Patterson, W.P. High-resolution δ13C intratooth profiles in bovine enamel: implications for mineralization pattern and isotopic attenuation. Geochimica et Cosmochimica Acta 69, (2005). 3631–3642.Google Scholar