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Stable Isotopes in Yellow-Bellied Marmot (Marmota Flaviventris) Fossils Reveal Environmental Stability in the Late Quaternary of the Colorado Rocky Mountains

Published online by Cambridge University Press:  20 January 2017

Linda M. Reynard*
Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA
David J. Meltzer
Department of Anthropology, Southern Methodist University, Dallas, TX 75275, USA
Steven D. Emslie
Department of Biology and Marine Biology, University of North Carolina, 601 S. College Road, Wilmington, NC 28403, USA
Noreen Tuross
Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA
*Corresponding author at: Department of Human Evolutionary Biology, 11 Divinity Avenue, Cambridge, MA, 02138, USA., E-mail (L.M. Reynard).


High elevation plant and animal communities are considered extremely sensitive to environmental change. We investigated an exceptional fossil record of yellow-bellied marmot (Marmota flaviventris) specimens that was recovered from Cement Creek Cave (elev. 2860 m) and ranged in age from radiocarbon background circa 49.8 cal ka BP to ~ 1 cal ka BP. We coupled isotopic and radiocarbon measurements (δ18O, δD, δ15N, δ13C, and 14C) of bone collagen from individually-AMS dated specimens of marmots to assess ecological responses by this species to environmental change over time in a high elevation basin in the Rocky Mountains of southwestern Colorado, USA. We find little change in all four isotope ratios over time, demonstrating considerable environmental stability during periods when the marmots were present. The stable ecology and the apparent persistence of the small mammal community in the cave fauna throughout the late Quaternary are in marked contrast to the changes that occurred in the large mammal community, including local extirpation and extinction, at the end of the Pleistocene.

Research Article
University of Washington

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Allen, B., Anderson, R.(2000). A continuous, high-resolution record of late Pleistocene climate variability from the Estancia Basin, New Mexico. Geological Society of America Bulletin 112, 14441458.2.0.CO;2>CrossRefGoogle Scholar
Anderson, L. (2011). Holocene record of precipitation seasonality from lake calcite 18O in the Central Rocky Mountains, United States. Geology 39, 211214.CrossRefGoogle Scholar
Armour, J., Fawcett, P., Geissman, J.(2002). 15 k.y. paleoclimatic and glacial record from northern New Mexico. Geology 30, 723726.2.0.CO;2>CrossRefGoogle Scholar
Asmerom, Y., Polyak, V.J., Burns, S.J.(2010). Variable winter moisture in the southwestern United States linked to rapid glacial climate shifts. Nature Geoscience 3, 114117.CrossRefGoogle Scholar
Barrell, J. (1969). Flora of the Gunnison Basin. Natural Land Institute, Rockford, Illinois.Google Scholar
Bartlein, P., Anderson, K., Anderson, P., Edwards, M., Mock, C., Thompson, R., Webb, R., Whitlock, C.(1998). Paleoclimate simulations for North America over the past 21,000 years: features of the simulated climate and comparisons with paleoenvironmental data. Quaternary Science Reviews 17, 549585.CrossRefGoogle Scholar
Benson, L., Madole, R., Landis, G., Gosse, J.(2005). New data for Late Pleistocene Pinedale alpine glaciation from southwestern Colorado. Quaternary Science Reviews 24, 4965.CrossRefGoogle Scholar
Birchall, J., O'Connell, T.C., Heaton, T.H.E., Hedges, R.E.M.(2005). Hydrogen isotope ratios in animal body protein reflect trophic level. Journal of Animal Ecology 74, 877881.CrossRefGoogle Scholar
Briles, C.E., Whitlock, C., Meltzer, D.J.(2012). Last glacial"interglacial environments in the southern Rocky Mountains, USA and implications for Younger Dryas-age human occupation. Quaternary Research 77, 96103.CrossRefGoogle Scholar
Broecker, W.S., McGee, D., Adams, K.D., Cheng, H., Edwards, R.L., Oviatt, C.G., Quade, J.(2009). A Great Basin-wide dry episode during the first half of the Mystery Interval?. Quaternary Science Reviews 28, 25572563.CrossRefGoogle Scholar
Bronk Ramsey, C. (2009). Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337360.CrossRefGoogle Scholar
Brugger, K.A. (2007). Cosmogenic 10Be and 36Cl ages from Late Pleistocene terminal moraine complexes in the Taylor River drainage basin, central Colorado, USA. Quaternary Science Reviews 26, 494499.CrossRefGoogle Scholar
Brugger, K.A. (2010). Climate in the Southern Sawatch Range and Elk Mountains, Colorado, USA, during the Last Glacial Maximum: inferences using a simple degree"day model. Arctic, Antarctic, and Alpine Research 42, 164178.CrossRefGoogle Scholar
Bryant, J.D., Froehlich, P.N.(1995). A model of oxygen isotope fractionation in body water of large animals. Geochimica et Cosmochimica Acta 59, 45234537.CrossRefGoogle Scholar
Clark, P.U., Dyke, A.S., Shakun, J.D., Carlson, A.E., Clark, J., Wohlfarth, B., Mitrovica, J.X., Hostetler, S.W., McCabe, A.M.(2009). The Last Glacial Maximum. Science 325, 710714.CrossRefGoogle ScholarPubMed
Cole, K., Fisher, J., Ironside, K., Mead, J., Koehler, P.(2013). The biogeographic histories of Pinus edulis and Pinus monophylla over the last 50,000 years. Quaternary International 310, 96110.CrossRefGoogle Scholar
Coplen, T.B. (2007). Calibration of the calcite"water oxygen-isotope geothermometer at Devils Hole, Nevada, a natural laboratory. Geochimica et Cosmochimica Acta 71, 39483957.CrossRefGoogle Scholar
Cormie, A.B., Schwarcz, A.P., Gray, J.(1994). Relation between hydrogen isotopic ratios of bone collagen and rain. Geochimica et Cosmochimica Acta 58, 377391.CrossRefGoogle Scholar
Criss, R.E. (1999). Principles of Stable Isotope Distribution. Oxford University Press, Oxford.Google Scholar
Dansgaard, W. (1964). Stable isotopes in precipitation. Tellus 4, 436468.Google Scholar
Day, C.C., Henderson, G.M.(2011). Oxygen isotopes in calcite grown under cave-analogue conditions. Geochimica et Cosmochimica Acta 75, 39563972.CrossRefGoogle Scholar
DeNiro, M.J. (1985). Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317, 806809.CrossRefGoogle Scholar
DeNiro, M.J., Epstein, S.(1978). Influence of diet on distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495506.CrossRefGoogle Scholar
Drucker, D.G., Bocherens, H., Billiou, D.(2003). Evidence for shifting environmental conditions in Southwestern France from 33 000 to 15 000 years ago derived from carbon-13 and nitrogen-15 natural abundances in collagen of large herbivores. Earth and Planetary Science Letters 216, 163173.CrossRefGoogle Scholar
Emslie, S.D. (1986). Late Pleistocene vertebrates from Gunnison County, Colorado. Journal of Paleontology 60, 170176.CrossRefGoogle Scholar
Emslie, S.D. (2002). Fossil shrews (Insectivora: Soricidae) from the late Pleistocene of Colorado. Southwestern Naturalist 47, 6269.CrossRefGoogle Scholar
Emslie, S.D., Meltzer, D.J.(2010). A unique high-elevation fossil assemblage spanning the Last Glacial Maximum from Cement Creek Cave, Colorado. Poster presented at the21st Biennial American Quaternary Association Meeting, Laramie, WY.Google Scholar
Fairchild, I.J., Treble, P.C.(2009). Trace elements in speleothems as recorders of environmental change. Quaternary Science Reviews 28, 449468.CrossRefGoogle Scholar
Fall, P. (1997a). ), Timberline fluctuations and late Quaternary paleoclimates in the southern Rocky Mountains, Colorado. Geological Society of America Bulletin 109, 13061320.2.3.CO;2>CrossRefGoogle Scholar
Fall, P. (1997b). ), Fire history and composition of the subalpine forest of western Colorado during the Holocene. Journal of Biogeography 24, 309325.CrossRefGoogle Scholar
Frase, B.A., Hoffman, R.S.(1980). Marmota flaviventris. Mammalian Species 135, 18.CrossRefGoogle Scholar
Fraser, R.A., Bogaard, A., Heaton, T., Charles, M., Jones, G., Christensen, B.T., Halstead, P., Merbach, I., Poulton, P.R., Sparkes, D., Styring, A.K.(2011). Manuring and stable nitrogen isotope ratios in cereals and pulses: towards a new archaeobotanical approach to the inference of land use and dietary practices. Journal of Archaeological Science 38, 27902804.CrossRefGoogle Scholar
Gill, J.L., Williams, J.W., Jackson, S.T., Lininger, K.B., Robinson, G.S.(2009). Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326, 11001103.CrossRefGoogle ScholarPubMed
Guido, Z., Ward, D., Anderson, R.(2007). Pacing the post-Last Glacial Maximum demise of the Animas Valley glacier and the San Juan Mountain ice cap, Colorado. Geology 35, 739742.CrossRefGoogle Scholar
Heaton, T.H.E. (1987). The 15N/14N ratio of plants in South Africa and Namibia: relationship to climate and coastal/saline environments. Oecologia 74, 236246.CrossRefGoogle Scholar
Heaton, T.H.E. (1999). Spatial, species, and temporal variations in the 13C/12C Ratios of C 3 plants: implications for palaeodiet studies. Journal of Archaeological Science 26, 637649.CrossRefGoogle Scholar
Hedges, R.E.M., Reynard, L.M.(2007). Nitrogen isotopes and the trophic level of humans in archaeology. Journal of Archaeological Science 34, 12401251.CrossRefGoogle Scholar
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, Palaeoclimatology, Palaeoecology 163, 3347.CrossRefGoogle Scholar
Iacumin, P., Di Matteo, A., Nikolaev, V., Kuznetsova, T.V.(2010). Climate information from C, N and O stable isotope analyses of mammoth bones from northern Siberia. Quaternary International 212, 206212.CrossRefGoogle Scholar
Jim, S., Ambrose, S., Evershed, R.(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, 6172.CrossRefGoogle Scholar
Kirsanow, K., Tuross, N.(2011). Oxygen and hydrogen isotopes in rodent tissues: impact of diet, water and ontogeny. Palaeogeography, Palaeoclimatology, Palaeoecology 310, 916.CrossRefGoogle Scholar
Kirsanow, K., Makarewicz, C., Tuross, N.(2008). Stable oxygen (?18O) and hydrogen (?D) isotopes in ovicaprid dentinal collagen record seasonal variation. Journal of Archaeological Science 35, 31593167.CrossRefGoogle Scholar
Leonard, E. (2007). Modeled patterns of Late Pleistocene glacier inception and growth in the Southern and Central Rocky Mountains, USA: sensitivity to climate change and paleoclimatic implications. Quaternary Science Reviews 26, 21522166.CrossRefGoogle Scholar
Leyden, J.J., Wassenaar, L.I., Hobson, K.A., Walker, E.G.(2006). Stable hydrogen isotopes of bison bone collagen as a proxy for Holocene climate on the Northern Great Plains. Palaeogeography, Palaeoclimatology, Palaeoecology 239, 8799.CrossRefGoogle Scholar
McLean, B.S., Emslie, S.D.(2012). Stable isotopes reflect the ecological stability of two high-elevation mammals from the late Quaternary of Colorado. Quaternary Research 77, 408417.CrossRefGoogle Scholar
McLean, B.S., Ward, J.K., Polito, M.J., Emslie, S.D.(2014). Responses of high-elevation herbaceous plant assemblages to low glacial CO 2 concentrations revealed by fossil marmot (Marmota) teeth. Oecologia 175, 11171127.CrossRefGoogle ScholarPubMed
Minagawa, M., Wada, E.(1984). Stepwise enrichment of 15N along food chains: further evidence and the relation between ?15N and animal age. Geochimica et Cosmochimica Acta 48, 11351140.CrossRefGoogle Scholar
Navarro, N., L"cuyer, C., Montuire, S., Langlois, C., Martineau, F.(2004). Oxygen isotope compositions of phosphate from arvicoline teeth and quaternary climatic changes, Gigny, French Jura. Quaternary Research 62, 172182.CrossRefGoogle Scholar
Podlesak, D.W., Torregrossa, A.M., Ehleringer, J.R., Dearing, M.D., Passey, B.H., Cerling, T.E.(2008). Turnover of oxygen and hydrogen isotopes in the body water, CO 2, hair, and enamel of a small mammal. Geochimica et Cosmochimica Acta 72, 1935.CrossRefGoogle Scholar
Polyak, V.J., Asmerom, Y., Burns, S.J., Lachniet, M.S.(2012). Climatic backdrop to the terminal Pleistocene extinction of North American mammals. Geology 40, 10231026.CrossRefGoogle Scholar
Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Ramsey, C.B., Buck, C.E., Cheng, H., Edwards, R.L., Friedrich, M., Grootes, P.M., Guilderson, T.P., Haflidason, H., Hajdas, I., Hatte, C., Heaton, T.J., Hoffmann, D.L., Hogg, A.G., Hughen, K.A., Kaiser, K.F., Kromer, B., Manning, S.W., Niu, M., Reimer, R.W., Richards, D.A., Scott, E.M., Southon, J.R., Staff, R.A., Turney, C.S.M., van der Plicht, J.(2013). IntCal13 and Marine13 radiocarbon age calibration curves 0"50,000 years cal BP. Radiocarbon 55, 18691887.CrossRefGoogle Scholar
Reynard, L.M., Hedges, R.E.M.(2008). Stable hydrogen isotopes of bone collagen in palaeodietary and palaeoenvironmental reconstruction. Journal of Archaeological Science 35, 19341942.CrossRefGoogle Scholar
Richards, M.P., Hedges, R.E.M.(2003). Variations in bone collagen ?13C and ?15N values of fauna from Northwest Europe over the last 40 000 years. Palaeogeography, Palaeoclimatology, Palaeoecology 193, 261267.CrossRefGoogle Scholar
Schmitt, J., Schneider, R., Elsig, J., Leuenberger, D., Lourantou, A., Chappellaz, J., K"hler, P., Joos, F., Stocker, T.F., Leuenberger, M., Fischer, H.(2012). Carbon isotope constraints on the deglacial CO 2 rise from ice cores. Science 336, 711714.CrossRefGoogle ScholarPubMed
Schubert, B.A., Jahren, A.H.(2012). The effect of atmospheric CO 2 concentration on carbon isotope fractionation in C 3 land plants. Geochimica et Cosmochimica Acta 96, 2943.CrossRefGoogle Scholar
Spaulding, W.G., Leopold, E.B., Van Devender, T.R.(1983). Late Wisconsin paleoecology of the American Southwest. Porter, S. Late-Quaternary Environments of the United StatesThe Late Pleistocene. vol. 1, University of Minnesota Press, Minneapolis.259293.Google Scholar
Stevens, R.E., Hedges, R.E.M.(2004). Carbon and nitrogen stable isotope analysis of northwest European horse bone and tooth collagen, 40,000 BP"present: palaeoclimatic interpretations. Quaternary Science Reviews 23, 977991.CrossRefGoogle Scholar
Stiger, M. (2001). Hunter"gatherer Archaeology of the Colorado High Country. University Press of Colorado, Boulder.Google Scholar
Stiger, M. (2006). A Folsom structure in the Colorado mountains. American Antiquity 71, 321351.CrossRefGoogle Scholar
Stute, M., Schlosser, P., Clark, J., Broecker, W.(1992). Paleotemperatures in the Southwestern United States derived from noble-gases in ground-water. Science 256, 10001003.CrossRefGoogle ScholarPubMed
Szpak, P., Groecke, D.R., Debruyne, R., MacPhee, R.D.E., Guthrie, R.D., Froese, D., Zazula, G.D., Patterson, W.P., Poinar, H.N.(2010). Regional differences in bone collagen ?13C and ?15N of Pleistocene mammoths: implications for paleoecology of the mammoth steppe. Palaeogeography, Palaeoclimatology, Palaeoecology 286, 8896.CrossRefGoogle Scholar
Thompson, R.S., Whitlock, C., Bartlein, P.J., Harrison, S.P., Spaulding, W.G.(1993). Climate change in the western United States since 18,000 yr B.P.. Wright jr., H.E., Kutzbach, J.E., Webb III, T., Ruddiman, W.F., Street-Perrott, F.A., Bartlein, P.J. Global Climates Since the Last Glacial Maximum. University of Minnesota Press, Minneapolis.468513.Google Scholar
Tieszen, L.L., Fagre, T.(1993). Effect of diet quality and composition on the isotopic composition of respiratory CO 2, bone collagen, bioapatite, and soft tissues. Lambert, J.B., Grupe, G. Prehistoric Human Bone: Archaeology at the Molecular Level Springer-Verlag, Berlin.121155.CrossRefGoogle Scholar
Tuross, N. (2012). Comparative decalcification methods, radiocarbon dates, and stable isotopes of the VIRI bones. Radiocarbon 54, 837844.CrossRefGoogle Scholar
Tuross, N., Fogel, M.L., Hare, P.E.(1988). Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochimica et Cosmochimica Acta 52, 929935.CrossRefGoogle Scholar
Tuross, N., Warinner, C., Kirsanow, K., Kester, C.(2008). Organic oxygen and hydrogen isotopes in a porcine controlled dietary study. Rapid Communications in Mass Spectrometry 22, 17411745.CrossRefGoogle Scholar
Vogel, J.C., van der Merwe, N.J.(1977). Isotopic evidence for early maize cultivation in New York State. American Antiquity 42, 238242.CrossRefGoogle Scholar
Wagner, J.D.M., Cole, J.E., Beck, J.W., Patchett, P.J., Henderson, G.M., Barnett, H.R.(2010). Moisture variability in the Southwestern United States linked to abrupt Glacial climate change. Nature Geoscience 3, 110113.CrossRefGoogle Scholar
Warinner, C., Tuross, N.(2009). Alkaline cooking and stable isotope tissue-diet spacing in swine: archaeological implications. Journal of Archaeological Science 36, 16901697.CrossRefGoogle Scholar
Warinner, C., Robles Garcia, N., Tuross, N.(2013). Maize, beans and the floral isotopic diversity of Highland Oaxaca, Mexico. Journal of Archaeological Science 40, 868873.CrossRefGoogle Scholar
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Stable Isotopes in Yellow-Bellied Marmot (Marmota Flaviventris) Fossils Reveal Environmental Stability in the Late Quaternary of the Colorado Rocky Mountains
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