Abstract
Tooth enamel apatite carbonate carbon and oxygen isotope ratios of modern kangaroos (Macropus spp.) collected on a 900-km latitudinal transect spanning a C3–C4 transition zone were analysed to create a reference set for palaeoenvironmental reconstruction in southern Australia. The carbon isotope composition of enamel carbonate reflects the proportional intake of C3 and C4 vegetation, and its oxygen isotope composition reflects that of ingested water. Tooth enamel forms incrementally, recording dietary and environmental changes during mineralisation. Analyses show only weak correlations between climate records and latitudinal changes in δ13C and δ18O. No species achieved the δ13C values (~−1.0 ‰) expected for 100 % C4 grazing diets; kangaroos at low latitudes that are classified as feeding primarily on C4 grasses (grazers) have δ13C of up to −3.5 ‰. In these areas, δ13C below −12 ‰ suggests a 100 % C3 grass and/or leafy plant (browse) diet while animals from higher latitude have lower δ13C. Animals from semi-arid areas have δ18O of 34–40 ‰, while grazers from temperate areas have lower values (~28–30 ‰). Three patterns with implications for palaeoenvironmental reconstruction emerge: (1) all species in semi-arid areas regularly browse to supplement limited grass resources; (2) all species within an environmental zone have similar carbon and oxygen isotope compositions, meaning data from different kangaroo species can be pooled for palaeoenvironmental investigations; (3) relatively small regional environmental differences can be distinguished when δ13C and δ18O data are used together. These data demonstrate that diet–isotope and climate–isotope relationships should be evaluated in modern ecosystems before application to the regional fossil record.
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References
Ambrose SH (1993) Isotopic analysis of paleodiets: methodological and interpretive considerations. In: Sandford MK (ed) Investigations of ancient human tissue: chemical analyses in anthropology. Gordon and Breach, Langhorne, pp 59–130
Ambrose SH, DeNiro MJ (1986) The isotopic ecology of East African mammals. Oecologia 69:395–406
Ambrose SH, Norr L (1993) Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In: Lambert JB, Grupe G (eds) Prehistoric human bone—archaeology at the molecular level. Springer, New York, pp 1–37
Ayliffe LK, Chivas AR (1990) Oxygen isotope composition of the bone phosphate of Australian kangaroos: potential as a palaeoenvironmental recorder. Geochim Cosmochim Acta 54:2603–2609
Bailey PT, Martensz PN, Barker R (1971) The red kangaroo, Megalia rufa (Desmarest), in north-western New South Wales. CSIRO Wildl Res 16:29–39
Balasse M (2002) Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling. Int J Osteoarchaeol 12:155–165
Balasse M (2003) Potential biases in sampling design and interpretation of intra-tooth isotope analysis. Int J Osteoarchaeol 13:3–10
Balasse M, Ambrose SH (2003) Distinguishing sheep and goats using dental morphology and stable carbon isotopes in C4 grassland environments. J Archaeol Sci 32:691–702
Balasse M, Ambrose SH, Smith AB, Price TD (2002) 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 29:917–932
Balasse M, Smith AB, Ambrose SH, Leigh SR (2003) Determining sheep birth seasonality by analysis of tooth enamel oxygen isotope ratios: the Late Stone Age site of Kasteelberg (South Africa). J Archaeol Sci 29:917–932
Balasse M, Tresset A, Dobney K, Ambrose SH (2005) The use of isotope ratios to test for seaweed eating in sheep. J Zool 266:283–291
Balasse M, Tresset A, Ambrose SH (2006) Stable isotope evidence (δ13C, δ18O) for winter feeding on seaweed by neolithic sheep of Scotland. J Zool 270:170–176
Bell RHV (1982) The effect of soil nutrient availability on community structure in African ecosystems. In: Huntley BJ, Walker BH (eds) Ecology of tropical savannas. Springer, New York, pp 193–216
BOM (2008a) Australian climate zones. http://www.bom.gov.au/climate/environ/other/kpn_all.shtml Australian Government, Bureau of Meteorology
BOM (2008b) Climate data online. http://www.bom.gov.au/climate/averages/ Australian Government, Bureau of Meteorology
BOM (2008c) Climate of South Australia. http://www.bom.gov.au/lam/climate/levelthree/ausclim/ausclimsa.htm Australian Government, Bureau of Meteorology
Brookman TH, Ambrose SH (2012) Seasonal variation in kangaroo tooth enamel oxygen and carbon isotopes in South Australia. Quat Res (in press). doi:10.1016/j.yqres.2012.05.011
Bryant D, Froelich P (1995) A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta 59:4523–4537
Buchmann N, Guehl JM, Barigah TS, Ehleringer JR (1997) Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110:120–131
Caughley G, Brown B, Dostine P, Grice D (1984) The grey kangaroo overlap zone. Aust Wildl Res 11:1–10
Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite carbonate in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363
Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158
Cerling TE, Harris JM, Passey BH (2003) Diets of East African bovidae based on stable isotope analysis. J Mammal 84:456–470
Churchill DM, de Corona A (1972) The distribution of victorian plants. Dominion, North Blackburn
Clementz MT, Koch PL, Beck CA (2007) Diet induced differences in carbon isotope fractionation between sirenians and terrestrial ungulates. Mar Biol 151:1773–1784
Colinvaux P (1981) A paleothermometer of promise. Q Rev Archaeol 2:5
Connin SL, Betancourt J, Quade J (1998) Late Pleistocene C4 plant dominance and summer rainfall in the south-western United States from isotopic study of herbivore teeth. Quat Res 50:179–193
Coplen TB, Kenall C, Hopple J (1983) Comparison of stable isotope reference samples. Nature 302:236–238
Craig H (1961) Isotopic variation in meteoric waters. Science 133:1702–1703
Croft DB (1987) Socio-ecology of the antilopine wallaroo, Macropus antilopinus, in the northern territory, with observations on sympatric M. robustus woodwardii and M. agilis. Aust Wildl Res 4:243–255
Dalgaard P (2002) Introductory statistics with R. Springer, New York
Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468
Darling WG, Bath AH, Gibson JJ, Rozanski K (2005) Isotopes in water In: Leng MJ (ed) Isotopes in palaeoenvironmental research. Springer, Netherlands, pp 1–66
Dawson T (1995) Kangaroos: biology of the largest marsupial. University of New South Wales Press, Sydney
Dawson TJ, Ellis BA (1994) Diets of mammalian herbivores in Australian arid shrublands: seasonal effects on overlap between red kangaroos, sheep and rabbits and on dietary niche breadths and electivities. J Arid Environ 26:257–271
Dawson TJ, Ellis BA (1996) Diets of mammalian herbivores in Australian arid, hilly shrublands: seasonal effects on overlap between euros (hill kangaroos), sheep and feral goats, and on dietary niche breadths and electivities. J Arid Environ 34:491–506
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
Ealey EHM (1967) Ecology of the euro, Macropus robustus (Gould) in north-western Australia. II. Behaviours, movements, and drinking patterns. CSIRO Wildl Res 12:27–51
Ealey EHM, Main AR (1967) Ecology of the euro, Macropus robustus (Gould), in north-western Australia: III seasonal changes in nutrition. CSIRO Wildl Res 12:53–65
Ealey EHM, Bentley PJ, Main AR (1965) Studies on water metabolism of the hill kangaroo, Macropus Robustus (Gould), in northwest Australia. Ecology 46:473–479
Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299
Emrich K, Ehhalt DH, Vogel JC (1970) Carbon isotope fractionation during the precipitation of calcium carbonate. Earth Planet Sci Lett 8:363–371
Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205–226
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol 40:503–537
Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31
Fraser RA, Grün R, Privat K, Gagan MK (2008) Stable-isotope microprofiling of wombat tooth enamel records seasonal changes in vegetation and environmental conditions in eastern Australia. Palaeogeogr Palaeoclimatol Palaeoecol 269:66–77
Fricke HC, Clyde WC, O’Neil JR, Gingerich PD (1998) 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 Planet Sci Lett 160:193–208
Gadbury C, Todd L, Jahren AH, Amundson R (2000) Spatial and temporal variation in the isotopic composition of bison tooth enamel from the early Holocene Hudson-Meng bone bed, Nebraska. Palaeogeogr Palaeoclimatol Palaeoecol 157:93–97
Gell PA, Bickford S (1996) Vegetation. In: Davies M, Twidale CR, Tyler MJ (eds) Natural history of the Flinders ranges. Royal Society of South Australia, Adelaide, pp 86–101
Glasby P, Williams MAJ, McKirdy DM, Symonds R, Chivas AR (2007) Late Pleistocene environments in the Flinders ranges, Australia: preliminary evidence from microfossils and stable isotopes. Quat Aust 24:19–28
Griffiths M, Barker R (1966) The plants eaten by sheep and by kangaroos grazing together in a paddock in south-western Queensland. CSIRO Wildl Res 11:145–167
Haberlah D, Glasby P, Williams MAJ, Hill SM, Williams F, Rhodes EJ, Gostin V, O’Flaherty A, Jacobsen GE (2010a) ‘Of droughts and flooding rains’: an alluvial loess record from central South Australia spanning the last glacial cycle. Geological Society, London, Special Publications 346:185–223
Haberlah D, Williams MAJ, Halverson G, McTainsh GH, Hill SM, Hrstka T, Jaime P, Butcher AR, Glasby P (2010b) Loess and floods: high-resolution multi-proxy data of Last glacial maximum (LGM) slackwater deposition in the Flinders ranges, semi-arid South Australia. Quat Sci Rev 29:2673–2693
Hattersley PW (1983) The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57:113–128
Helliker BR, Ehleringer JR (2002) Differential 18O enrichment in C3 versus C4 grasses. Funct Plant Biol 29:435–442
Higgins P, MacFadden BJ (2004) “Amount effect” recorded in oxygen isotopes of Late glacial horse (Equus) and bison (Bison) teeth from the Sonoran and Chihuahuan deserts, south-western United States. Palaeogeogr Palaeoclimatol Palaeoecol 206:337–353
Hoppe KA, Stover SM, Pascoe JR, Amundson R (2004) Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeogr Palaeoclimatol Palaeoecol 206:355–365
Hume ID (1982) Digestive physiology and nutrition of marsupials. Cambridge University Press, Cambridge
Jackson S (2003) Australian mammals: biology and captive management. CSIRO Publishing, Collingwood
Kirkpatrick TH (1965) 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. Queensl J Agric Anim Sci 22:301–317
Kirkpatrick TH (1970) Studies in Macropodidae in Queensland. 8. Age estimation in the red kangaroo (Megaleia rufa (Desmarest)). Queensl J Agric Anim Sci 27:461–462
Kirkpatrick TH (1978) The development of the dentition of Macropus giganteus (shaw). Aust Mammal 2:29–36
Kirkpatrick TJ (1985) Biology for management. In: Lavery HJ (ed) The kangaroo keepers. University of Queensland Press, St Lucia, pp 135–160
Kohn MJ, Schoeninger MJ, Valley JW (1998) Variability in oxygen isotope compositions of herbivore teeth: reflections of seasonality or developmental physiology? Chem Geol 152:97–112
Krueger HW, Sullivan CH (1984) Models for carbon isotope fractionation between diet and bone. In: Turnland JR, Johnson PE (eds) Stable isotopes in nutrition, vol 258, American Chemical SocietyWashington, DC, pp 205–220
Lee-Thorp JA (2000) Preservation of biogenic carbon isotopic signals in Plio-Pleistocene bone and tooth mineral. In: Ambrose SH, Katzenberg MA (eds) Biogeochemical approaches to paleodietary analysis. Kluwer Academic/Plenum, New York, pp 89–115
Levin N, Cerling TE, Passey BJ, Harris JM, Ehleringer JR (2006) A stable isotope aridity index for terrestrial environments. PNAS 103:11201–11205
Liu J, Fu G, Song X, Charles,SP, Zhang Y,Han D, Wang S (2010) Stable isotopic compositions in Australian precipitation. J Geophys Res 115. doi:10.1029/2010JD01443
Livingston DA, Clayton WD (1980) An altitudinal cline in tropical African grass floras and its paleoecological significance. Quat Res 13:392–402
Macho G, Williamson DK (2002) The effects of ecology on life history strategies and metabolic disturbances during development: an example from the African bovids. Biol J Linn Soc 75:271–279
Marino BM, McElroy MB (1991) Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349:127–131
McCullough DR, McCullough Y (2000) Kangaroos in outback Australia: comparative ecology and behavior of three coexisting species. Columbia University Press, New York
Miller GH, Fogel ML, Magee JW, Gagan MK, Clarke SJ, Johnson BJ (2005) Ecosystem collapse in Pleistocene Australia and a human role in megafaunal extinction. Science 309:287–290
Murphy BP, Bowman DMJS (2006) Kangaroo metabolism does not cause the relationship between bone collagen δ15N and water availability. Funct Ecol 20:1062–1069
Murphy BP, Bowman DMJS, Gagan MK (2007a) The interactive effect of temperature and humidity on the oxygen isotope composition of kangaroos. Funct Ecol 21:757–766
Murphy BP, Bowman DMJS, Gagan MK (2007b) Sources of carbon isotope variation in kangaroo bone collagen and tooth enamel. Geochim Cosmochim Acta 71:3847–3858
Nelson SV (2005) Paleoseasonality inferred from equid teeth and intra-tooth isotopic variability. Palaeogeogr Palaeoclimatol Palaeoecol 222:122–144
O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336
Passey BH, Cerling TE (2006) In situ stable isotope analysis (δ13C, δ18O) of very small teeth using laser ablation GC/IRMS. Chem Geol 235:238–249
Pate FD (1997) Bone chemistry and paleodiet: reconstructing prehistoric subsistence-settlement systems in Australia. J Anthrop Archaeol 16:103–120
Pate FD, Noble AH (2000) Geographic distribution of C3 and C4 grasses recorded from stable carbon isotope values of bone collagen of South Australian herbivores. Aust J Bot 48:203–207
Ramesh R, Bhattacharya SK, Gopalan K (1986) Climatic correlations in the stable isotope records of silver fir (Abies pindow) trees from Kashmir, India. Earth Planet Sci Lett 79:66–74
Rozanski K, Araguás-Araguás L, Gonfiantini R (1993) Isotopic patterns in modern global precipitation. In: Swart PK, Lohmann KC, McKenzie J, Savin S (eds) Climate change in continental isotopic records, vol 78. American Geophysical Union, Washington, pp 1–36
Scholes RJ, Archer SR (1997) Tree-grass interactions in savannas. Annu Rev Ecol Syst 28:517–544
Schwerdtfeger P, Curran E (1996) Climate of the Flinders ranges. In: Davies M, Twidale CR, Tyler MJ (eds) Natural history of the Flinders ranges. Royal Society of South Australia, Adelaide, pp 63–75
Taylor RJ (1980) Distribution of feeding activity of the eastern grey kangaroo, Macropus giganteus, in coastal lowland of south-east Queensland. Aust Wildl Res 7:317–325
Taylor RJ (1983) The diet of the eastern grey kangaroo and wallaroo in areas of improved and native pasture in the New England tablelands. Aust Wildl Res 10:203–211
Teeri JA, Stowe LG (1976) Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:1–12
Tieszen LL (1991) Natural variations in the carbon isotope values of plants: implications for archaeology, ecology, and paleoecology. J Archaeol Sci 18:227–248
Tieszen LL, Fagre T (1993) Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite carbonate and soft tissue experiments. In: Lambert JB, Grupe G (eds) Molecular archaeology of prehistoric human bone. Springer, Berlin, pp 121–155
Tieszen LL, Hein D, Qvortrup SA, Troughton JA, Imbamba SK (1979a) Use of δ13C values of East African herbivores to determine vegetation selectivity. Oecologia 37:351–359
Tieszen LL, Senyimba MM, Imbamba SK, Troughton JH (1979b) The distribution of C3 and C4 grasses along an altitudinal and moisture gradient in Kenya. Oecologia 37:337–350
van der Merwe NJ, Medina E (1989) Photosynthesis and 13C/12C in Amazonian rain forests. Geochim Cosmochim Acta 53:1091–1094
Vogel JC, Fuls A, Ellis RP (1978) The geographical distribution of Kranz grasses in South Africa. S Afr J Sci 74:209–219
Wang Y, Kromhout E, Zhang C, Xy Y, Parker W, Deng T, Qiu Z (2008) Stable isotopic variations in modern herbivore tooth enamel, plants and water on the Tibetan Plateau: implications for paleoclimate and paleoelevation reconstructions. Palaeogeogr Palaeoclimatol Palaeoecol 260:359–374
White TD, Ambrose SH, Suwa G, Su DF, DeGusta D, Bernor RL, Boisserie JR, Brunet M, Delson E, Frost S, Garcia N, Giaourtsakis IX, Haile-Selassie Y, Howell FC, Lehmann T, Likius A, Pehevan C, Saegusa H, Semprebon G, Teaford M, Vrba E (2009) Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326:87–93
Widga C, Walker JD, Stockli LD (2010) Middle Holocene Bison diet and mobility in the eastern Great Plains (USA) based on δ13C, δ18O, and 87Sr/86Sr analyses of tooth enamel carbonate. Quat Res 73:449–463
Williams DLG (1980) Catalogue of Pleistocene vertebrate fossils and sites in South Australia. Trans R Soc S Aust 104:101–115
Williams MAJ, Prescott JR, Chappell J, Adamson D, Cock B, Walker K, Gell P (2001) The enigma of a Late Pleistocene wetland in the Flinders ranges, South Australia. Quat Int 83–85:129–144
Wilson GR (1975) Age structures of populations of kangaroos (Macropodidae) taken by professional shooters in New South Wales. Aust Wildl Res 2:1–9
Wynn JG, Bird MI (2008) Environmental controls on the stable carbon isotopic composition of soil organic carbon: implications for modelling the distribution of C3 and C4 plants in Australia. Tellus 60B:604–621
Yakir D (1992) Variations in the natural abundance of oxygen-18 and deuterium in plant carbohydrates. Plant Cell Environ 15:1005–1020
Acknowledgments
We thank Martin A. J. Williams and Galen Halverson of the University of Adelaide for their support and Keith Hackley, Wang Hong and Eric Johnson of the Illinois State Geological Survey for their technical assistance. Brett Murphy, Rebecca Fraser, Jim McNamara, Angus and Abby MacGregor, Chris Button, Karl Gardner and the Flinders ranges National Park and ‘Bounceback’ program rangers all provided valuable assistance. Brett Bryan and James Paull of CSIRO Land and Water provided climatic data. Dan Yakir provided insightful comments that greatly improved the manuscript. This research was funded by the Royal Geographical Society of South Australia and the Royal Zoological Society of South Australia. Funding for mass spectrometry instrumentation was provided by National Science Foundation (USA) grant SBR-9871480.
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Brookman, T.H., Ambrose, S.H. Kangaroo tooth enamel oxygen and carbon isotope variation on a latitudinal transect in southern Australia: implications for palaeoenvironmental reconstruction. Oecologia 171, 403–416 (2013). https://doi.org/10.1007/s00442-012-2425-6
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DOI: https://doi.org/10.1007/s00442-012-2425-6