Skip to main content
×
Home

The Ecological implications of a Yakutian mammoth's last meal

  • Bas van Geel (a1), André Aptroot (a2), Claudia Baittinger (a3), Hilary H. Birks (a4), Ian D. Bull (a5), Hugh B. Cross (a6), Richard P. Evershed (a5), Barbara Gravendeel (a1) (a6), Erwin J.O. Kompanje (a7), Peter Kuperus (a1), Dick Mol (a8), Klaas G.J. Nierop (a1), Jan Peter Pals (a9), Alexei N. Tikhonov (a10), Guido van Reenen (a1) and Peter H. van Tienderen (a1)...
Abstract

Part of a large male woolly mammoth (Mammuthus primigenius) was preserved in permafrost in northern Yakutia. It was radiocarbon dated to ca. 18,50014C yr BP (ca. 22,500 cal yr BP). Dung from the lower intestine was subjected to a multiproxy array of microscopic, chemical, and molecular techniques to reconstruct the diet, the season of death, and the paleoenvironment. Pollen and plant macro-remains showed that grasses and sedges were the main food, with considerable amounts of dwarf willow twigs and a variety of herbs and mosses. Analyses of 110-bp fragments of the plastid rbcL gene amplified from DNA and of organic compounds supplemented the microscopic identifications. Fruit-bodies of dung-inhabiting Ascomycete fungi which develop after at least one week of exposure to air were found inside the intestine. Therefore the mammoth had eaten dung. It was probably mammoth dung as no bile acids were detected among the fecal biomarkers analysed. The plant assemblage and the presence of the first spring vessels of terminal tree-rings of dwarf willows indicated that the animal died in early spring. The mammoth lived in extensive cold treeless grassland vegetation interspersed with wetter, more productive meadows. The study demonstrated the paleoecological potential of several biochemical analytical techniques.

Copyright
Corresponding author
*Corrresponding author. Fax: +31 20 5257832.E-mail address: vanGeel@science.uva.nl (B. van Geel).
References
Hide All
Ager T.A., (2003). Late Quaternary vegetation and climate history of the central Bering land bridge from St. Michael Island, western Alaska. Quaternary Research 60, 1932.
Akashi S., Saito K., (1960). A branched saturated C15 acid (sarcinic acid) from sarcina phospholipids and a similar acid from several microbial lipids. Journal of Biochemistry 47, 222229.
Andreev A.A., Tarasov P.E., Siegert C., Ebel T., Klimanov V.A., Melles M., Bobrov A.A., Dereviagin A.Yu., Lubinski D.J., Hubberten H.-W., (2003). Late Pleistocene and Holocene vegetation and climate on the northern Taymyr Peninsula, Arctic Russia. Boreas 32, 484505.
Aptroot A., van Geel B., (2006). Fungi of the colon of the Yukagir Mammoth and from stratigraphically related permafrost samples. Review of Palaeobotany and Palynology 141, 225230.
Bethell P.H., Goad L.J., Evershed R.P., Ottaway J., (1994). The study of molecular markers of human activity: The use of coprostanol in the soil as an indicator of human faecal material. Journal of Archaeological Science 21, 619632.
Birks H.H., (2001). Plant macrofossils. Smol J.P., Birks H.J.B., Last W.M., Tracking environmental change using lake sediments. Volume 3, Terrestrial, algal and silicious indicators. Kluwer Academic Publishers, 4974.
Bull I.D., van Bergen P.F., Poulton P.R., Evershed R.P., (1998). Organic geochemical studies of soils from the Rothamsted Classical Experiments-II, Soils from the Hoosfield Spring Barley Experiment treated with different quantities of manure. Organic Geochemistry 28, 1126.
Bull I.D., Simpson I.A., van Bergen P.F., Evershed R.P., (1999a). Muck ‘n’ molecules: Organic geochemical methods for detecting ancient manuring. Antiquity 73, 8696.
Bull I.D., Simpson I.A., Dockrill S.J., Evershed R.P., (1999b). Organic geochemical evidence for the origin of ancient anthropogenic soil deposits at Tofts Ness, Sanday, Orkney. Organic Geochemistry 30, 535556.
Bull I.D., Betancourt P.P., Evershed R.P., (2002a). An organic geochemical investigation of the practice of manuring at a Minoan site on Pseira Island, Crete. Geoarchaeology 16, 223242.
Bull I.D., Lockheart M.J., Elhmmali M.M., Roberts D.J., Evershed R.P., (2002b). The origin of faeces by means of biomarker detection. Environment International 27, 647654.
Bull I.D., Elhmmali M.M., Roberts D.J., Evershed R.P., (2003). Using steroidal biomarkers to track the abandonement of a Roman wastewater course at the Agora (Athens, Greece). Archaeometry 45, 149161.
Challinor J.M., (2001). Review: development and applications of thermally assisted hydrolysis and methylation reactions. Journal of Analytical and Applied Pyrolysis 61, 334.
Cooper A., Poinar H., (2001). Ancient DNA: do it right or not at all. Science 289, 1139.
Cwynar L.C., (1982). A late-Quaternary vegetation history from Hanging Lake, Northern Yukon. Ecological Monographs 52, 124.
Cwynar L., Ritchie J.C., (1980). Arctic steppe-tundra: a Yukon perspective. Science 208, 13751377.
Davis O.K., (1987). Spores of the dung fungus Sporormiella: increased abundance in historic sediments and before Pleistocene megafaunal extinction. Quaternary Research 28, 290294.
Davis O.K., Shafer D.S., (2006). Sporormiella fungal spores, a palynological means of detecting herbivore density. Palaeogeography, Palaeoclimatology, Palaeoecology 237, 4050.
Davis O.K., Kolva D.A., Mehringer P.J., (1977). Pollen analysis of Wildcat Lake, Whitman County, Washington: the last 1000 years. Northwest Science 51, 1330.
Davis O.K., Mead J.I., Martin P.S., Agenbroad L.D., (1985). Riparian plants were a major component of the diet of mammoths of Southern Utah. Current Research in the Pleistocene 2, 8182.
De Leeuw J.W., Versteegh G.J.M., van Bergen P.F., (2006). Biomacromolecules of algae and plants and their fossil analogues. Plant Ecology 182, 209233.
Drescher-Schneider R., Jacquat C., Schoch W., (2007). Palaeobotanical investigations at the mammoth site of Niederweningen (Kanton Zürich), Switzerland. Quaternary International 164–165, 113129.
Elhmmali M.M., Roberts D.J., Evershed R.P., (1997). Bile acids as a new class of sewage pollution indicator. Environmental Science and Technology 31, 36633668.
Elhmmali M.M., Roberts D.J., Evershed R.P., (2000). Combined analysis of bile acids and sterols/stanols from riverine particulates to assess sewage discharges and other faecal sources. Environmental Science and Technology 34, 3946.
Elias S.A., Short S.K., Nelson C.H., Birks H.H., (1996). Life and times of the Bering land bridge. Nature 382, 6063.
Evershed R.P., Bethell P.H., Reynolds P., Walsh N.J., (1997). 5b-Stigmastanol and related 5b-stanols as biomarkers of manuring: analysis of modern experimental materials and assessment of the archaeological potential. Journal of Archaeological Science 24, 485495.
Fægri K., Iversen J., Fægri K., Kaland P.E., Krzywinski K., (1989). Textbook of Pollen Analysis. 4th edition Wiley and Sons, New York., .
Fajardo G., Hornicke H., (1989). Problems in estimating the extent of coprophagy in the rat. British Journal of Nutrition 62, 551561.
Fox-Dobbs K., Leonard J.A., Koch P.L., in press. Pleistocene megafauna from eastern Beringia: paleoecological and paleoenvironmental interpretations of stable carbon and nitrogen isotope and radiocarbon records. Palaeogeography, Palaeoclimatology, Palaeoecology. doi:10.1016/j.palaeo.2007.12.011.
François R.J., Eulderink F., Bywaters E.G., E.G.L. , (1995). Commented glossary for rheumatic spinal diseases, based on pathology. Annals of the Rheumatic Diseases 54, 615625.
Goetcheus V.G., Birks H.H., (2001). Full-glacial upland tundra vegetation preserved under tephra in the Beringia National Park, Seward Peninsula, Alaska. Quaternary Science Reviews 20, 135147.
Gorlova R.N., (1982a). Large remains of plants from the stomach of the Shandrin Mammoth. Trudy Zoologicheskogo Instituta 3, 3435.
Gorlova R.N., (1982b). The plant macroremains found in the enteron tract of the Yuribeyskiy mammoth. Sokolov V.E., The Yuribeyskiy Mammoth. Nauka, Moscow., 3743.
Guthrie R.D., (1990). Frozen Fauna of the Mammoth Steppe. The University of Chicago Press, Chicago., .
Guthrie R.D., (2001). Origin and causes of the mammoth steppe: a story of cloud cover, woolly mammal tooth pits, buckles, and inside-out Beringia. Quaternary Science Reviews 20, 549574.
Guthrie R.D., (2006). New carbon dates link climatic change with human colonization and Pleistocene extinctions. Nature 441, 207209.
Hagey L.R., Schteingart C.D., Tonnu H.T., Rossi S.S., Hofmann A.F., (1993). Unique bile alcohols (3,6,7,25,27-pentahydroxy cholestanes) and absence of bile-acids are a common feature of 3 ancient mammals. Hepatology 18, 4, A177-A177.
Heal O.W., Anderson J.M., Swift M.J., (1997). Plant litter quality and decomposition: an historic overview. Cadish G., Giller K.E., Driven by Nature; Plant Litter Quality and Decomposition. CAB International, Wallingford., 330.
Hofreiter M., Poinar H.N., Spaulding W.G., Bauer D., Martin S., Possnert G., Pääbo S., (2000). A molecular analysis of ground sloth diet through the last glaciation. Molecular Ecology 9, 19751984.
Hofreiter M., Betancourt J.L., Sbriller A.P., Markgraf V., McDonald H.G., (2003). Phylogeny, diet, and habitat of an extinct ground sloth from Cuchillo Cura, Neuquen Province, southwest Argentina. Quaternary Research 59, 364378.
Iacumin P., Davanzo S., Nikolaev V., (2006). Spatial and temporal variations in the 13C/12C and 15N/14N ratios of mammoth hairs: palaeodiet and palaeoclimatic implications. Chemical Geology 231, 1625.
Kienast F., (2007). Plant macrofossil records — Arctic Eurasia. Elias S.A., Encyclopedia of Quaternary Science vol. 3. Elsevier, 24222434.
Kienast F., Siegert C., Derevyagin A.Y., Mai H.D., (2001). Climatic implications of late Quaternary plant macrofossil assemblages from the Taimyr Peninsula, Siberia. Global and Planetary Change 31, 265281.
Kienast F., Schirrmeister L., Siegert C., Tarasov P., (2005). Palaeobotanical evidence for warm summers in the East Siberian Arctic during the last cold stage. Quaternary Research 63, 283300.
Killops S.D., Killops J.K., (1993). An introduction to organic geochemistry. Longman Scientific and Technical. England, Harlow, Essex., .
Kolattukudy P.E., (2001). Polyesters in higher plants. Scheper T., Advances in Biochemical Engineering/Biotechnology vol. 71, Springer-Verlag, Heidelberg., 149.,Berlin.
Kompanje E.J.O., (1999). Considerations on the comparative pathology of the vertebrae in Mysticeti and Odontoceti; evidence for the occurrence of discarthrosis, zygarthrosis, infectious spondylitis and spondyloarthritis. Zoölogische Mededeelingen Leiden 73, 99130.
Kompanje E.J.O., Klaver P.S.J., De Vries G.T., (2000). Spondyloarthropathy and osteoarthrosis in three Indomalayan bears: Ursus ursinus Cuvier, 1823, Ursus thibetanus Raffles, 1821, and Ursus malayanus Shaw & Nodder, 1791 (Mammalia; Carnivora: Ursidae). Contributions to Zoology 69, 259269.
Krug J.C., Benny G.L., Keller H.W., (2004). Coprophilous fungi. Mueller G.M., Bills G.F., Foster M.S., Biodiversity of fungi. Elsevier, Amsterdam., 468499.
Kuch M., Rohland N., Betancourt J.L., Latorre C., Steppan S., Poinar H.N., (2002). Molecular analysis of an 11,700-year old rodent midden from the Atacama Desert, Chile. Molecular Ecology 11, 913924.
Kuroki S., Schteingart C.D., Hagey L.R., Cohen B.I., Mosbach E.H., Rossi S.S., Hofmann A.F., Matoba N., Une M., Hoshita T., Odell D.K., (1988). Bile salts of the West Indian manatee, Trichechus manatus latirostris: novel bile alcohol sulfates and the absence of bile acids. Journal of Lipid Research 29, 509522.
Leggett K., (2004). Coprophagy and unusual thermoregulatory behaviour in desert-dwelling elephants of north-western Namibia. Pachyderm 36, 113115.
Liu T.S., Li X.G., (1984). Mammoths in China. Klein P.S., Klein R.G., Quaternary Extinctions: A Prehistoric Revolution. University of Arizona Press, Tucson., 517527.
Mead J.I., Agenbroad L.D., Davis O.K., Martin P.S., (1986). Dung of Mammuthus in the arid southwest, North America. Quaternary Research 25, 121127.
Mol D., Tikhonov A.N., van der Plicht J., Bolshiyanov D.Yu., (2003). Discoveries of woolly mammoth, Mammuthus primigenius (Proboscidea: Elephantidae) and some other Pleistocene mammals on the Taimyr Peninsula. Russian Journal of Theriology 2, 7795.
Mol D., Buigues B., Tikhonov A., Lazarev P., van Geel B., Fisher D., Boeskorov G., (2005). The Yukagir Mammoth — An Animal of the Cold Steppe (in Japanese). European Editions. Moscow.
Mol D., Shoshani J., Tikhonov A., van Geel B., Sano S., Lazarev P., Boeskorov G., Agenbroad L.D., (2006a). The Yukagir Mammoth: brief history, 14C dates, individual age, gender, size, physical and environmental conditions and storage. Scientific Annals, School of Geology, Aristotle University of Thessaloniki, Special Volume 98 299314.
Mol D., Tikhonov A., van der Plicht J., Kahlke R.D., Debruyne R., van Geel B., van Reenen G., Pals J.P., de Marliave C., Reumer J.W.F., (2006b). Results of the CERPOLEX/Mammuthus Expeditions on the Taimyr Peninsula, Arctic Siberia, Russian Federation. Quaternary International 142–143, 186202.
Mol D., Shoshani J., Tikhonov A.N., Boeskorov G.G., Lazarev P.A., Agenbroad L., Suzuki N., Buigues B., (2007). Anatomical-morphological features and individual age of the Yukagir mammoth. Boeskorov G.G., Tikhonov A.N., Suzuki N., The Yukagir Mammoth. Saint-Petersburg University Publishing House, Saint-Petersburg., 97118.,(in Russian and in English).
Nierop K.G.J., (2001). Temporal and vertical organic matter differentiation along a vegetation succession as revealed by pyrolysis and thermally assisted hydrolysis and methylation. Journal of Analytical and Applied Pyrolysis 61, 111132.
Nierop K.G.J., Verstraten J.M., (2004). Rapid molecular assessment of the bioturbation extent in sandy soil horizons under pine using ester-bound lipids by on-line thermally assisted hydrolysis and methylation-gas chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry 18, 10811088.
Nierop K.G.J., Jansen B., Hageman J.A., Verstraten J.M., (2006). The complementarity of extractable and ester-bound lipids in a soil profile under pine. Plant and Soil 286, 269285.
Olivier R.C.D., (1982). Ecology and behavior of living elephants: bases for adaptations concerning the extinct woolly mammoths. Hopkins D.M., Matthews J.V., Schweger C.E., Young S.B., Paleoecology of Beringia. Academic Press, New York., 281290.
Reimer P.J., Baillie M.G.L., Bard E., Bayliss A., Beck J.W., Bertrand C.J.H., Blackwell P.G., Buck C.E., Burr G.S., Cutler K.B., Damon P.E., Edwards R.L., Fairbanks R.G., Friedrich M., Guilderson T.P., Hogg A.G., Hughen K.A., Kromer B., McCormac F.G., Manning S.W., Ramsey C.B., Reimer R.W., Remmele S., Southon J.R., Stuiver M., Talamo S., Taylor F.W., van der Plicht J., Weyhenmeyer C.E., (2004). IntCal04 Terrestrial radiocarbon age calibration, 26 – 0 ka BP. Radiocarbon 46, 10291058.
Rollo F., Ubaldi M., Erminin L., Marota I., (2002). Otzi's last meals: DNA analysis of the intestinal content of the Neolithic glacier mummy from the Alps. Proceedings of the National Academy of Science 99, 1259412599.
Rothschild B.M., Rothschild C., (1994). No laughing matter: spondyloarthropathy and osteoarthritis in Hyaenidae. Journal of Zoo and Wildlife Medicine 25, 259263.
Rountrey A.N., Fisher D.C., Vartanyan S., Fox D.L., (2007). Carbon and nitrogen isotope analyses of a juvenile woolly mammoth tusk: evidence of weaning. Quaternary International 169–70, 166173.
Saito K., (1960). Chromatographic studies on bacterial fatty acids. Journal of Biochemistry 47, 699709.
Schmidt N.M., Baittinger C., Forchhammer M.C., (2006). Reconstructing century-long snow regimes using estimates of high Arctic Salix arctica radial growth. Arctic, Antarctic, and Alpine Research 38, 257262.
Sher A.V., Kuzmina S.A., Kuznetsova T.V., Sulerzhitsky L.D., (2005). New insights into the Weichselian environment and climate of the East Siberian Arctic, derived from fossil insects, plants, and mammals. Quaternary Science Reviews 24, 533569.
Shoshani J., Mol D., (2007). Estimated shoulder height and weight of the Yukagir mammoth (Mammuthus primigenius). Boeskorov G.G., Boeskorov A.N., Suzuki N., The Yukagir Mammoth. Saint-Petersburg University Publishing House, Saint-Petersburg., 157166.,(in Russian and in English).
Solonevich N.G., Tikhomirov B.A., Ukraintseva V.V., (1977). The preliminary results of the study of plant remnants from the enteron of Shandrin mammoth (Yakutia). Proceedings of the Zoological Institute Moscow 63, 277280.
Stuiver M., Reimer P.J., (1993). Extended 14C database and revised CALIB radiocarbon calibration program. Radiocarbon 35, 215230.
Sulerzhitsky L.D., (1997). The features of radiocarbon chronology of mammoths in Siberia and northern Eastern Europe (as substratum for human colonization). Velichko A.A., Soffer O., Humans Settle the Planet Earth: Global Dispersal of Hominids. Institute of Geography. Russian Academy of Sciences, Moscow., 184202.,(in Russian).
Tütken T., Furrer H., Vennemann T.W., (2007). Stable isotope compositions of mammoth teeth from Niederweningen, Switzerland: implications for the Late Pleistocene climate, environment, and diet. Quaternary International 164–65, 139150.
Ukraintseva V.V., (1979). Vegetation of warm intervals of late Pleistocene and the extinction of some large herbivorous mammals. Botanicheskii Zhurnal 64, 318330.
Ukraintseva V.A., (1993). Vegetation cover and environment of the Mammoth Epoch in Siberia. The Mammoth Site of Hot Springs South Dakota Inc., .
van Bergen P.F., Bull I.D., Poulton P.R., Evershed R.P., (1997). Organic geochemical studies of soils from the Rothamsted Classical Experiments — I. Total lipids, solvent insoluble residues and humic acids from Broadbalk Wilderness. Organic Geochemistry 26, 117135.
van Bergen P.F., Nott C.J., Bull I.D., Poulton P.R., Evershed R.P., (1998). Organic geochemical studies of soils from the Rothamsted Classical Experiments — IV. Preliminary results from a study of the effect of soil pH on organic matter decay. Organic Geochemistry 29, 17791795.
van der Plicht J., Beck J.W., Bard E., Baillie M.G.L., Blackwell P.G., Buck C.E., Friedrich M., Guilderson T.P., Hughen K.A., Kromer B., McCormac F.G., Bronk Ramsey C., Reimer P.J., Reimer R.W., Remmele S., Richards D.A., Southon J.R., Stuiver M., Weyhenmeyer C.E., (2004). NOTCAL04: comparison/calibration 14C records 26–50 cal kyr BP. Radiocarbon 46, 12251238.
van Geel B., Aptroot A., (2006). Fossil ascomycetes in Quaternary deposits. Nova Hedwigia 82, 313329.
van Geel B., Zazula G.D., Schweger C.E., (2007). Spores of coprophilous fungi from under the Dawson tephra (25,300 14C years BP), Yukon Territory, northwestern Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 481485.
Vasil'chuk Y., Punning J.M., Vasil'chuk A., (1997). Radiocarbon ages of mammoths in Northern Eurasia: implications for population development and Late Quaternary environment. Radiocarbon 39, 118.
Walton T.J., (1990). Waxes, cutin and suberin. Harwood J.L., Bowyer J.R., Methods in Plant Biochemistry 4. Academic Press, London., 105158.
Wampler T.P., (1999). Review — Introduction to pyrolysis–capillary gas chromatography. Journal of Chromatography A 842, 207220.
Willerslev E., Hansen A.J., Binladen J., Brand T.B., Gilbert T.P., Shapiro B., Bunce M., Wiuf C., Gilichinsky D.A., Cooper A., (2003). Diverse plant and animal genetic records from Holocene and Pleistocene sediments. Science 300, 791795.
Yurtsev B.A., (2001). The Pleistocene "Tundra-Steppe" and the productivity paradox: the landscape approach. Quaternary Science Reviews 20, 165174.
Zazula G.D., Froese D.G., Schweger C.E., Mathewes R.W., Beaudoin A.B., Telkal A.M., Harington C.R., Westgate J.A., (2003). Ice-age steppe vegetation in east Beringia. Nature 423, 603.
Zazula G.D., Schweger C.E., Beaudoin A.B., McCourt G.H., (2006a). Macrofossil and pollen evidence for full-glacial steppe within an ecological mosaic along the Bluefish River, eastern Beringia. Quaternary International 142–143, 219.
Zazula G.D., Froese D.G., Elias S.A., Kuzmina S., la Farge C., Reyes A.V., Sanborn P.T., Schweger C.E., Smith C.A.S., Mathewes R.W., (2006b). Vegetation buried under Dawson tephra (25,300 14C years BP) and locally diverse late Pleistocene paleoenvironments of Goldbottom Creek, Yukon, Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 242, 253286.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Quaternary Research
  • ISSN: 0033-5894
  • EISSN: 1096-0287
  • URL: /core/journals/quaternary-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 14 *
Loading metrics...

Abstract views

Total abstract views: 105 *
Loading metrics...

* Views captured on Cambridge Core between 20th January 2017 - 11th December 2017. This data will be updated every 24 hours.