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Mammoth tooth enamel growth rates inferred from stable isotope analysis and histology

Published online by Cambridge University Press:  20 January 2017

Jessica Z. Metcalfe  and
Fred J. Longstaffe
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Abstract

Mammoth (Mammuthus sp.) teeth are relatively abundant in Quaternary deposits from Eurasia and North America, and their isotopic compositions can be used to reconstruct past seasonal patterns in precipitation, diet, and migration. Strategies for collecting and interpreting such data, however, are strongly dependent on growth rates, which can vary among species, individuals, and within teeth. In this study, we use histological and isotopic measurements to determine enamel growth rates for a Columbian mammoth (Mammuthus columbi) tooth in two directions. Using histology, the growth rate through the enamel thickness (ET; perpendicular to the height of the tooth) is estimated at 0.8 to 1.5 mm/yr. Isotopic sampling through the innermost 0.36 mm of the ET recovered less than half a period of variation (i.e., half an inferred year of growth), which is consistent with the histological estimate for ET growth rate. A combination of histological and isotopic measurements suggests that the enamel extension rate (growth in the height of the tooth) is 13–14 mm/yr. Knowledge of enamel growth rates should improve the design and interpretation of future isotopic studies of mammoth teeth. The combination of histological and isotopic measurements may also prove useful in determining growth rates for other extinct taxa.

Keywords

MammothMammuthusProboscideanEnamelIsotopesHistologyGrowth rate

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Type
Original Articles
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Quaternary Research , Volume 77 , Issue 3 , May 2012 , pp. 424 - 432
Copyright
University of Washington

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References

Allan, J.H., (1967). Maturation of enamel. Miles, A.E.W., Structural and Chemical Organization of Teeth, Academic Press, New York, 467–494.Google Scholar
Arppe, L., Karhu, J.A., (2006). Implications for the Late Pleistocene climate in Finland and adjacent areas from the isotopic composition of mammoth skeletal remains. Palaeogeography, Palaeoclimatology, Palaeoecology. 231, 322–330.Google Scholar
Arppe, L., Karhu, J.A., (2010). Oxygen isotope values of precipitation and the thermal climate in Europe during the middle to late Weichselian ice age. Quaternary Science Reviews. 29, 1263–1275.Google Scholar
Ayliffe, L.K., Lister, A.M., Chivas, A.R., (1992). The preservation of glacial–interglacial climatic signatures in the oxygen isotopes of elephant skeletal phosphate. Palaeogeography, Palaeoclimatology, Palaeoecology. 99, 179–191.CrossRefGoogle Scholar
Ayliffe, L.K., Chivas, A.R., Leakey, M.G., (1994). The retention of primary oxygen isotope compositions of fossil elephant skeletal phosphate. Geochimica et Cosmochimica Acta. 58, 5291–5298.Google Scholar
Balasse, M., (2002). Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling. International Journal of Osteoarchaeology. 12, 155–165.Google Scholar
Balasse, M., (2003). Potential biases in sampling design and interpretation of intra-tooth isotope analysis. International Journal of Osteoarchaeology. 13, 3–10.CrossRefGoogle Scholar
Balter, V., Telouk, P., Reynard, B., Braga, J., Thackeray, F., Albarede, F., (2008). Analysis of coupled Sr/Ca and Sr-87/Sr-86 variations in enamel using laser-ablation tandem quadrupole-multicollector ICPMS. Geochimica et Cosmochimica Acta. 72, 3980–3990.Google Scholar
Bernard, A., Daux, V., Lecuyer, C., Brugal, J.P., Genty, D., Wainer, K., Gardien, V., Fourel, F., Jaubert, J., (2009). Pleistocene seasonal temperature variations recorded in the δ18O of Bison priscus teeth. Earth and Planetary Science Letters. 283, 133–143.Google Scholar
Bocherens, H., (2003). Isotopic biogeochemistry and the paleoecology of the mammoth steppe fauna. Deinsea. 9, 57–71.Google Scholar
Bromage, T.G., Lacruz, R.S., Hogg, R., Goldman, H.M., McFarlin, S.C., Warshaw, J., Dirks, W., Perez-Ochoa, A., Smolyar, I., Enlow, D.H., Boyde, A., (2009). Lamellar bone is an incremental tissue reconciling enamel rhythms, body size, and organismal life history. Calcified Tissue International. 84, 388–404.Google Scholar
Cerling, T.E., Wang, Y., Quade, J., (1993). Expansion of C4 ecosystems as an indicator of global ecological change in the Late Miocene. Nature. 361, 344–345.Google Scholar
Cerling, T.E., Harris, J.M., Leakey, M.G., (1999). Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia. 120, 364–374.Google Scholar
Coplen, T.B., (1994). Reporting stable hydrogen, carbon, and oxygen isotopic abundances. Pure and Applied Chemistry. 66, 271–276.Google Scholar
Coplen, T.B., Brand, W.A., Gehre, M., Groning, M., Meijer, H.A.J., Toman, B., Verkouteren, R.M., (2006). New guidelines for δ13C measurements. Analytical Chemistry. 78, 2439–2441.CrossRefGoogle ScholarPubMed
Dirks, W., Bromage, T.G., Agenbroad, L.D., (2012). The duration and rate of molar plate formation in Palaeoloxodon cypriotes and Mammuthus columbi from dental histology. Quaternary International.. 255, 79–85.Google Scholar
Domingo, L., Cuevas-Gonzalez, J., Grimes, S.T., Fernandez, M.H., Lopez-Martinez, N., (2009). Multiproxy reconstruction of the palaeoclimate and palaeoenvironment of the Middle Miocene Somosaguas site (Madrid, Spain) using herbivore dental enamel. Palaeogeography, Palaeoclimatology, Palaeoecology. 272, 53–68.Google Scholar
Eberle, J., Fricke, H., Humphrey, J., (2009). Lower-latitude mammals as year-round residents in Eocene Arctic forests. Geology. 37, 499–502.Google Scholar
Feranec, R.S., (2004). Geographic variation in the diet of hypsodont herbivores from the Rancholabrean of Florida. Palaeogeography, Palaeoclimatology, Palaeoecology. 207, 359–369.Google Scholar
Feranec, R.S., MacFadden, K.B.J., (2000). Evolution of the grazing niche in Pleistocene mammals from Florida: evidence from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology. 162, 155–169.CrossRefGoogle Scholar
Feranec, R.S., Hadly, E.A., Paytan, A., (2009). Stable isotopes reveal seasonal competition for resources between late Pleistocene bison (Bison) and horse (Equus) from Rancho La Brea, southern California. Palaeogeography, Palaeoclimatology, Palaeoecology. 271, 153–160.Google Scholar
Ferretti, M.P., (2003). Structure and evolution of mammoth molar enamel. Acta Palaeontologica Polonica. 48, 383–396.Google Scholar
Ferretti, M.P., (2008). Enamel structure of Cuvieronius hyodon (Proboscidea, Gomphotheriidae) with a discussion on enamel evolution in elephantoids. Journal of Mammalian Evolution. 15, 37–58.CrossRefGoogle Scholar
Fisher, D.C., (2009). Paleobiology and extinction of proboscideans in the Great Lakes region of North America. Haynes, G., American Megafaunal Extinctions at the End of the Pleistocene, Springer, 55–75.CrossRefGoogle Scholar
Fisher, D.C., Fox, D.L., (2003). Season of death and terminal growth histories of Hiscock mastodons. Laub, R.S., The Hiscock Site: Late Pleistocene and Holocene Paleoecology and Archaeology of Western New York State: Proceedings of the Second Smith Symposium, Held at the Buffalo Museum of Science, October 14–15, 2001, Buffalo Society of Natural Sciences, Buffalo, 83–101.Google Scholar
Fisher, D.C., Fox, D.L., (2007). Season of death of the Dent mammoths: distinguishing single from multiple mortality events. Brunswig, R.H., Pitblado, B.L., Frontiers in Colorado Paleoindian Archaeology: From the Dent Site to the Rocky Mountains, University Press of Colorado, Boulder, 123–153.Google Scholar
FitzGerald, C.M., (1998). Do enamel microstructures have regular time dependency? Conclusions from the literature and a large-scale study. Journal of Human Evolution. 35, 371–386.Google Scholar
Fox, D.L., Fisher, D.C., (2001). Stable isotope ecology of a Late Miocene population of Gomphotherium productus (Mammalia, proboscidea) from Port of Entry Pit, Oklahoma, USA. Palaios. 16, 279–293.Google Scholar
Fox, D.L., Fisher, D.C., (2004). Dietary reconstruction of Miocene Gomphotherium (Mammalia, Proboscidea) from the Great Plains region, USA, based on the carbon isotope composition of tusk and molar enamel. Palaeogeography, Palaeoclimatology, Palaeoecology. 206, 311–335.Google Scholar
Fox, D.L., Fisher, D.C., Vartanyan, S., Tikhonov, A.N., Mol, D., Buigues, B., (2007). Paleoclimatic implications of oxygen isotopic variation in late Pleistocene and Holocene tusks of Mammuthus primigenius from northern Eurasia. Quaternary International. 169, 154–165.Google Scholar
Gadbury, C., Todd, L., Jahren, A.H., Amundson, R., (2000). Spatial and temporal variations in the isotopic composition of bison tooth enamel from the Early Holocene Hudson–Meng Bone Bed, Nebraska. Palaeogeography, Palaeoclimatology, Palaeoecology. 157, 79–93.Google Scholar
Garvie-Lok, S.J., Varney, T.L., Katzenberg, M.A., (2004). Preparation of bone carbonate for stable isotope analysis: the effects of treatment time and acid concentration. Journal of Archaeological Science. 31, 763–776.Google Scholar
Genoni, L., Iacumin, P., Nikolaev, V., Gribchenko, Y., Longinelli, A., (1998). Oxygen isotope measurements of mammoth and reindeer skeletal remains: an archive of Late Pleistocene environmental conditions in Eurasian Arctic. Earth and Planetary Science Letters. 160, 587–592.Google Scholar
Haynes, C.V., Huckell, B.B., (2007). Murray Springs: A Clovis Site with Multiple Activity Areas in the San Pedro Valley, Arizona. The University of Arizona Press, Tucson.Google Scholar
Hillson, S., (2005). Teeth. 2nd ed Cambridge University Press, Cambridge, UK ; New York.Google Scholar
Hoppe, K.A., Koch, P.L., (2006). The biogeochemistry of the Aucilla River fauna. Webb, S.D., First Floridians and Last Mastodons: The Page–Ladson Site in the Auscilla River, Springer, Netherlands, 379–401.Google Scholar
Hoppe, K.A., Koch, P.L., (2007). Reconstructing the migration patterns of late Pleistocene mammals from northern Florida, USA. Quaternary Research. 68, 347–352.Google Scholar
Hoppe, K.A., Koch, P.L., Carlson, R.W., Webb, S.D., (1999). Tracking mammoths and mastodons: reconstruction of migratory behavior using strontium isotope ratios. Geology. 27, 439–442.Google Scholar
Hoppe, K.A., Stover, S.M., Pascoe, J.R., Amundson, R., (2004). Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeography, Palaeoclimatology, Palaeoecology. 206, 355–365.Google Scholar
Hoyle, B.G., Fisher, D.C., Borns, H.W., Churchill-Dickson, L.L., Dorion, C.C., Weddle, T.K., (2004). Late Pleistocene mammoth remains from Coastal Maine, USA. Quaternary Research. 61, 277–288.Google 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, 206–212.Google Scholar
Koch, P.L., Fisher, D.C., Dettman, D., (1989). Oxygen isotope variation in the tusks of extinct proboscideans: a measure of season of death and seasonality. Geology. 17, 515–519.Google Scholar
Koch, P.L., Tuross, N., Fogel, M.L., (1997). The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. Journal of Archaeological Science. 24, 417–429.Google Scholar
Koch, P.L., Hoppe, K.A., Webb, S.D., (1998). The isotopic ecology of late Pleistocene mammals in North America — part 1. Florida. Chemical Geology. 152, 119–138.Google Scholar
Koch, P.L., Diffenbaugh, N.S., Hoppe, K.A., (2004). The effects of late Quaternary climate and pCO2 change on C4 plant abundance in the south-central United States. Palaeogeography, Palaeoclimatology, Palaeoecology. 207, 331–357.Google Scholar
Kohn, M.J., McKay, M., (2010). Stable isotopes of fossil teeth corroborate key general circulation model predictions for the Last Glacial Maximum in North America. Geophysical Research Letters. 37, L22702 .Google Scholar
Laws, R.M., (1966). Age criteria for the African elephant, Loxodonta a. africana . East African Wildlife Journal. 4, 1–37.CrossRefGoogle Scholar
MacFadden, B.J., Cerling, T.E., (1996). Mammalian herbivore communities, ancient feeding ecology, and carbon isotopes: a 10 million-sequence from the Neogene of Florida. Journal of Vertebrate Paleontology. 16, 103–115.Google Scholar
Metcalfe, J. Z., (2011). Late Pleistocene climate and proboscidean paleoecology in North America: insights from stable isotope compositions of skeletal remains. PhD Thesis, The University of Western Ontario, Canada.Google Scholar
Metcalfe, J.Z., Longstaffe, F.J., White, C.D., (2009). Method-dependent variations in stable isotope results for structural carbonate in bone bioapatite. Journal of Archaeological Science. 36, 110–121.Google Scholar
Metcalfe, J.Z., Longstaffe, F.J., Zazula, G.D., (2010). Nursing, weaning, and tooth development in woolly mammoths from Old Crow, Yukon, Canada: implications for Pleistocene extinctions. Palaeogeography, Palaeoclimatology, Palaeoecology. 298, 257–270.Google Scholar
Metcalfe, J.Z., Longstaffe, F.J., Ballenger, J.A.M., Haynes, C.V., (2011). Isotopic paleoecology of Clovis mammoths from Arizona. Proceedings of the National Academy of Sciences of the United States of America. 108, 17916–17920.CrossRefGoogle ScholarPubMed
Nargolwalla, M.C., Begun, D.R., Dean, M.C., Reid, D.J., Kordos, L., (2005). Dental development and life history in Anapithecus hernyaki . Journal of Human Evolution. 49, 99–121.Google Scholar
Passey, B.H., Cerling, T.E., (2002). Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series. Geochimica et Cosmochimica Acta. 66, 3225–3234.Google Scholar
Passey, B.H., Cerling, T.E., (2004). 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, 407–409.Google Scholar
Passey, B.H., Cerling, T.E., Schuster, G.T., Robinson, T.F., Roeder, B.L., Krueger, S.K., (2005). Inverse methods for estimating primary input signals from time-averaged isotope profiles. Geochimica et Cosmochimica Acta. 69, 4101–4116.Google Scholar
Roche, D., Segalen, L., Balan, E., Delattre, S., (2010). Preservation assessment of Miocene–Pliocene tooth enamel from Tugen Hills (Kenyan Rift Valley) through FTIR, chemical and stable-isotope analyses. Journal of Archaeological Science. 37, 1690–1699.Google Scholar
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, 166–173.CrossRefGoogle Scholar
Sánchez, B., Prado, J.L., Alberdi, M.T., (2004). Feeding ecology, dispersal, and extinction of South American Pleistocene gomphotheres (Gomphotheriidae, Proboscidea). Paleobiology. 30, 146–161.Google Scholar
Saunders, J.J., (1970). The distribution and taxonomy of Mammuthus in Arizona. Unpublished Master's thesis, The University of Arizona, Tucson.Google Scholar
Saunders, J.J., Grimm, E.C., Widga, C.C., Campbell, G.D., Curry, B.B., Grimley, D.A., Hanson, P.R., McCullum, J.P., Oliver, J.S., Treworgy, J.D., (2010). Paradigms and proboscideans in the southern Great Lakes region, USA. Quaternary International. 217, 175–187.Google Scholar
Shellis, R.P., (1984). Variations in growth of the enamel crown in human teeth and a possible relationship between growth and enamel structure. Archives of Oral Biology. 29, 697–705.Google Scholar
Smith, C.E., (1998). Cellular and chemical events during enamel maturation. Critical Reviews in Oral Biology and Medicine. 9, 128–161.Google Scholar
Smith, T.M., Tafforeau, P., (2008). New visions of dental tissue research: tooth development, chemistry, and structure. Evolutionary Anthropology. 17, 213–226.Google Scholar
Smith, T.M., Reid, D.J., Sirianni, J.E., (2006). The accuracy of histological assessments of dental development and age at death. Journal of Anatomy. 208, 125–138.Google Scholar
Suga, S., (1979). Comparative histology of progressive mineralization pattern of developing incisor enamel of rodents. Journal of Dental Research. 58, 1025–1026.CrossRefGoogle ScholarPubMed
Suga, S., (1989). Enamel hypomineralization viewed from the pattern of progressive mineralization of human and monkey developing enamel. Advances in Dental Research. 3, 188–198.Google Scholar
Tafforeau, P., Bentaleb, I., Jaeger, J.J., Martin, C., (2007). Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: potential implications for palaeoenvironmental isotopic studies. Palaeogeography, Palaeoclimatology, Palaeoecology. 246, 206–227.Google Scholar
Tutken, 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. 164–165, 139–150.Google Scholar
Ukkonen, P., Arppe, L., Houmark-Nielsen, M., Kjaer, K.H., Karhu, J.A., (2007). MIS 3 mammoth remains from Sweden: implications for faunal history, palaeoclimate and glaciation chronology. Quaternary Science Reviews. 26, 3081–3098.Google Scholar
Widga, C., Walker, J.D., Stockli, L.D., (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. Quaternary Research. 73, 449–463.Google Scholar
Zazzo, A., Lecuyer, C., Sheppard, S.M.F., Grandjean, P., Mariotti, A., (2004). Diagenesis and the reconstruction of paleoenvironments: a method to restore original δ18O values of carbonate and phosphate from fossil tooth enamel. Geochimica Et Cosmochimica Acta. 68, 2245–2258.Google Scholar
Zazzo, A., Balasse, M., Patterson, W.P., Patterson, P., (2005). High-resolution δ13C intratooth profiles in bovine enamel: implications for mineralization pattern and isotopic attenuation. Geochimica et Cosmochimica Acta. 69, 3631–3642.Google Scholar
Zazzo, A., Balasse, M., Passey, B.H., Moloney, A.P., Monahan, F.J., Schmidt, O., (2010). The isotope record of short- and long-term dietary changes in sheep tooth enamel: implications for quantitative reconstruction of paleodiets. Geochimica et Cosmochimica Acta. 74, 3571–3586.Google Scholar