Skip to main content Accessibility help
×
Home

Isotopic discrimination of resource partitioning among ungulates in C3-dominated communities from the miocene of Florida and California

  • Robert S. Feranec (a1) and Bruce J. MacFadden (a2)

Abstract

Stable isotope analysis of mammalian tooth enamel is a valuable method for examining resource partitioning in modern and ancient environments where there is a mixture of C3 and C4 plants. However, before 7 Ma North American ecosystems were composed predominantly of C3 plants, complicating isotopic assessment of resource partitioning. Study of modern African and North American ecosystems has shown that niche partitioning among mammals may be discerned in communities dominated by C3 plants, suggesting that a similar approach may work for ancient C3 ecosystems. Here, such analyses are applied to explore resource use and niche partitioning in two ancient C3-dominated communities, one from California and one from Florida. Each locality, Black Hawk Ranch (California) and the Love Bone Bed (Florida), occurs in Miocene deposits that accumulated prior to the rapid increase in C4 ecosystems 7 Myr ago. δ13C and δ18O values were obtained from the tooth enamel of eight species from Black Hawk Ranch, and 15 species from the Love Bone Bed. Results from the 197 bulk isotope samples showed significant differences in δ13C among taxa at the Love Bone Bed, but no significant differences were observed among taxa at Black Hawk Ranch. At both localities, equids generally have more positive δ13C values than co-occurring taxa, suggesting that equids occupied more open habitats, whereas antilocaprids, camelids, and proboscideans have more negative values, implying utilization of more closed communities. One result of note is the positive δ13C values of Pediomeryx (Yumaceras) hamiltoni from the Love Bone Bed, which suggests that P. (Y.) hamiltoni incorporated abundant fiber, possibly grass, in the diet similar to the horses from this locality. The lack of significant differences among taxa at Black Hawk Ranch may indicate a relatively homogeneous flora, or presence of abundant resources permitting niche overlap, whereas the opposite is implied by the presence of significantly different isotope values among taxa at the Love Bone Bed. The results from this study highlight the utility of isotopic techniques allowing discernment of resource partitioning in C3-dominated landscapes such as those that persisted for the millions of years before the rapid increase in C4 ecosystems that occurred during the late Miocene.

Copyright

References

Hide All
Axelrod, D. I. 1944. The Black Hawk Ranch flora. Carnegie Institution of Washington Publication 553:91101.
Balasse, M., Smith, A. B., Ambrose, S. H., and Leigh, S. R. 2003. 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 30:205215.
Bocherens, H. 2003. Isotopic biogeochemistry and the paleoecology of the mammoth steppe fauna. 2003. Deinsea 9:5776.
Bocherens, H., Koch, P. L., Mariotti, A., Geraads, D., and Jaeger, J.-J. 1996. Isotopic biogeochemistry (13C, 18O) of mammalian enamel from African Pleistocene hominid sites. Palaios 11:306318.
Bocherens, H., Billiou, D., Patou-Mathis, M., Bonjean, D., Otte, M., and Mariotti, A. 1997. Paleobiological implications of the isotopic signatures (13C, 15N) of fossil mammal collagen in Scladina Cave (Sclayn, Belgium). Quaternary Research 48:370380.
Brooks, J. R., Flanagan, L. B., Buchmann, N., and Ehleringer, J. R. 1997. Carbon isotope composition of boreal plants: functional grouping of life forms. Oecologia 110:301311.
Bryant, J. D., and Froelich, P. N. 1995. A model of oxygen isotope fractionation in body water of large mammals. Geochimica et Cosmochimica Acta 59:45234537.
Cerling, T. E., and Harris, J. M. 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347363.
Cerling, T. E., and Sharp, Z. D. 1996. Stable carbon and oxygen isotope analysis of fossil tooth enamel using laser ablation. Palaeogeography, Palaeoclimatology, Palaeoecology 126:173186.
Cerling, T. E., Wang, Y., and Quade, J. 1993. Expansion of C4 global ecological change in the late Miocene. Nature 361:344345.
Cerling, T. E., Harris, J. M., Ambrose, S. H., Leakey, M. G., and Solounias, N. 1997a. Dietary and environmental reconstruction with stable isotope analyses of herbivore tooth enamel from the Miocene locality of Fort Ternan, Kenya. Journal of Human Evolution 33:635650.
Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., Eisenmann, V., and Ehleringer, J. R. 1997b. Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153158.
Cerling, T. E., Hart, J. A., and Hart, T. B. 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138:512.
Condit, C. 1938. The San Pablo flora of West Central California. Carnegie Institution of Washington Publication 476:217268.
Dansgaard, W. 1964. Stable isotopes in precipitation. Tellus 16:436468.
DeNiro, M. J., and Epstein, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495506.
Drucker, D., and Bocherens, H. 2004. Carbon and nitrogen stable isotopes as tracers of change in diet breadth during middle and upper Palaeolithic in Europe. International Journal of Osteoarchaology 14:162177.
Drucker, D., Bocherens, H., Bridault, A., and Billiou, D. 2003. Carbon and nitrogen isotopic composition of red deer (Cervus elaphus) collagen as a tool for tracking palaeoenvironmental change during the Late-Glacial and Early Holocene in the northern Jura (France). Palaeogeography, Palaeoclimatology, Palaeoecology 195:375388.
Ehleringer, J. R., and Monson, R. K. 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics 24:411–39.
Ehleringer, J. R., Sage, R. F., Flanagan, L. B., and Pearcy, R. W. 1991. Climate change and the evolution of C4 photosynthesis. Trends in Ecology and Evolution 6:9599.
Farquhar, G. D., Ehleringer, J. R., and Hubick, K. T. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503–37.
Feranec, R. S. 2003. Determination of resource partitioning in a predominantly C3 environment by the analysis of stable isotope values from herbivores in Yellowstone National Park. Journal of Vertebrate Paleontology 23:49A.
Feranec, R. S. 2004. Ecological consequences of the evolution of key adaptations, and niche partitioning in C3-dominated environments. Ph.D. dissertation. University of California, Berkeley.
Fortelius, M., and Solounias, N. 2000. Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets. American Museum Novitates 3301:136.
Fortelius, M., Eronen, J., Jernvall, J., Liu, L., Pushkina, D., Rinne, J., Tesakov, A., Vislobokova, I., Zhang, Z., and Zhou, L. 2002. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evolutionary Ecology Research 4:10051016.
Fox, D. L., and Koch, P. L. 2003. Tertiary history of C4 biomass in the Great Plains, USA. Geology 31:809812.
Fricke, H. C., and O'Neil, J. R. 1996. Inter- and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeoclimatological and palaeobiological research. Palaeogeography, Palaeoclimatology, Palaeoecology 126:9199.
Fricke, H. C., and O'Neil, J. R. 1999. The correlation between 18O/16O ratios of meteoric water and surface temperature: its use in investigating terrestrial climate change over geological time. Earth and Planetary Science Letters 170:181196.
Friedli, H., Lotscher, H., Oeschger, H., Siegenthaler, U., and Stauffer, B. 1986. Ice core record of the 13C/12C ratio of atmospheric CO2 in the past two centuries. Nature 324:237238.
Fuller, W. A. 1959. The horns and teeth as indicators of age in bison. Journal of Wildlife Management 23:342344.
Gordon, I. J., and Illius, A. W. 1989. Resource partitioning by ungulates on the Isle of Rhum. Oecologia 79:383389.
Heaton, T. H. E. 1999. Spatial, species, and temporal variations in the 13C/12C ratios of C3 plants: implications for paleodiet studies. Journal of Archaeological Science 26:637649.
Helliker, B. R., and Ehleringer, J. R. 2000. Establishing a grassland signature in veins: 18O in the leaf water of C3 and C4 grasses. Proceedings of the National Academy of Sciences USA 97:78947898.
Hillson, S. 1986. Teeth. Cambridge University Press, Cambridge.
Hofmann, R. R., and Stewart, D. R. M. 1973. Grazer or browser: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia 36:226240.
Hutchinson, G. E. 1958. Concluding remarks. Cold Springs Harbor Symposium on Quantitative Biology 22:415427.
Iacumin, P., Nikolaev, V., and Ramigni, M. 2000. C and N isotope measurements on Eurasian fossil mammals, 40 000 to 10 000 years BP: herbivore physiologies and palaeoenvironmental reconstruction. Palaeogeography, Palaeoclimatology, Palaeoecology 163:3347.
Jahren, A. H., Todd, L. C., and Amundson, R. G. 1998. Stable isotope dietary analysis of bison bone samples from the Hudson-Meng bonebed: effects of paleotopography. Journal of Archaeological Science 25:465475.
Janis, C. M. 1988. An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preference. In Russell, D. E., Santoro, J.-P., and Sigogneau-Russell, D., eds. Teeth revisited. Proceedings of the seventh international symposium on dental morphology, Paris 1986. Mémoires du Museum National d'Histoire Naturelle, série C, Paris 53:367387.
Janis, C. M. 1990. Correlation of cranial and dental variables with dietary preference in mammals: a comparison of macropodids and ungulates. Memoirs of the Queensland Museum 28:349366.
Janis, C. M., and Ehrhardt, D. 1988. Correlation of relative muzzle width and relative incisor width with dietary preference. Biological Journal of the Linnean Society 92:267284.
Katzenberg, M. A. 1989. Stable isotope analysis of archaeological remains from southern Ontario. Journal of Archaeological Science 16:319329.
Katzenberg, M. A., and Weber, A. W. 1999. Stable isotope ecology and paleodiet in the Lake Baikal region of Siberia. Journal of Archaeological Science 26:651659.
Kendall, C., and Coplen, T. B. 2001. Distribution of oxygen-18 and deuterium in river waters across the United States. Hydrological Process 15:13631393.
Koch, P. L. 1998. Isotopic reconstruction of past continental environments. Annual Review of Earth and Planetary Sciences 26:573613.
Koch, P. L., Fisher, D. C., and Dettman, D. 1989. Oxygen isotope variation in the tusks of extinct proboscideans: a measure of season of death and seasonality. Geology 17:515519.
Koch, P. L., Tuross, N., and Fogel, M. L. 1997. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. Journal of Archaeological Science 24:417429.
Koch, P. L., Hoppe, K. A., and Webb, S. D. 1998. The isotopic ecology of late Pleistocene mammals in North America, Part 1. Florida. Chemical Geology 152:119138.
Kohn, M. J. 1996. Predicting animal δ18O: accounting for diet and physiological adaptation. Geochimica et Cosmochimica Acta 60:48114829.
Kohn, M. J. 2004. Comment: Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series, by B. H. Passey and T. E. Cerling. Geochimica et Cosmochimica Acta 68:403405.
Kohn, M. J., and Welker, J. M. 2005. On the temperature correlation of δ18O in modern precipitation. Earth and Planetary Science Letters 231:8796.
Kohn, M. J., Schoeninger, M. J., and Valley, J. W. 1996. Herbivore tooth oxygen isotope compositions: effect of diet and physiology. Geochimica et Cosmochimica Acta 60:38893896.
Land, L. S., Lundelius, E. L., and Valastro, S. 1980. Isotopic ecology of deer bones. Palaeogeography, Palaeoclimatology, Palaeoecology 32:143151.
Legendre, S. 1986. Analysis of mammalian communities from the late Eocene and Oligocene of southern France. Palaeovertebrata 16:191212.
Longinelli, A. 1984. Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research? Geochimica et Cosmochimica Acta 48:385390.
Luz, B., and Kolodny, Y. 1985. Oxygen isotope variations in phosphate of biogenic apatites, IV. Mammal teeth and bones. Earth and Planetary Science Letters 75:2936.
Luz, B., Kolodny, Y., and Horowitz, M. 1984. Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water. Geochimica et Cosmochimica Acta 48:16891693.
MacFadden, B. J. 1998. Tale of two rhinos: isotopic ecology, paleodiet, and niche differentiation of Aphelops and Teleoceras from the Florida Neogene. Paleobiology 24:274286.
MacFadden, B. J., and Cerling, T. E. 1996. Mammalian herbivore communities, ancient feeding ecology, and carbon isotopes; a 10 million-year sequence from the Neogene of Florida. Journal of Vertebrate Paleontology 16:103115.
MacFadden, B. J., and Higgins, P. 2004. Ancient ecology of 15-million-year-old browsing mammals within C3 plant communities from Panama. Oecologia 140:169182.
MacFadden, B. J., Solounias, N., and Cerling, T. E. 1999. Ancient diets, ecology, and extinction of 5-million-year-old horses from Florida. Science 283:824827.
Magnusson, W. E., Sanaiotti, T. M., Lima, A. P., Martinelli, L. A., Victoria, R. L., de Araujo, M. C., and Albernaz, A. L. 2002. A comparison of δ13C ratios of surface soils in savannas and forests in Amazonia. Journal of Biogeography 29:857863.
Marino, B. D., and McElroy, M. B. 1991. Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349:127131.
Marino, B. D., McElroy, M. B., Salawitch, R. J., and Spaulding, W. G. 1992. Glacial-to-interglacial variations in the carbon isotopic composition of atmospheric CO2 . Nature 357:461466.
O'Leary, M. H. 1988. Carbon isotopes in photosynthesis. Bio–Science 38:328336.
O'Leary, M. H., Madhavan, S., and Paneth, P. 1992. Physical and chemical basis of carbon isotope fractionation in plants. Plant, Cell and Environment 15:10991104.
Ometto, J. P. H., Flanagan, L. B., Martinelli, L. A., and Ehleringer, J. R. 2005. Oxygen isotope ratios of waters and respired CO2 in Amazonian forest and pasture ecosystems. Ecological Applications 15:5870.
Pagani, M., Arthur, M. A., and Freeman, K. H. 1999. Miocene evolution of atmospheric carbon dioxide. Paleoceanography 14:273292.
Passey, B. H., Cerling, T. E., Perkins, M. E., Voorhies, M. R., Harris, J. M., and Tucker, S. T. 2002. Environmental change in the Great Plains: an isotopic record from fossil horses. Journal of Geology 110:123140.
Prothero, D. R., and Tedford, R. H. 2000. Magnetic stratigraphy of the type Montediablan stage (Late Miocene), Black Hawk Ranch, Contra Costa County, California: implications for regional correlation. PaleoBios 20:110.
Quade, J., Cerling, T. E., Barry, J. C., Morgan, M. E., Pilbeam, D. R., Chivas, A. R., Lee-Thorp, J. A., and van der Merwe, N. A. 1992. A 16-Ma record of paleodiet using carbon and oxygen isotopes in fossil teeth from Pakistan. Chemical Geology 94:183192.
Quade, J., Cerling, T. E., Andrews, P., and Alpagut, B. 1995. Paleodietary reconstruction of Miocene faunas from Pasalar, Turkey, using stable carbon and oxygen isotopes of fossil tooth enamel. Journal of Human Evolution 28:373384.
Rees, J. W., Kainer, R. A., and Davis, R. W. 1966. Chronology of mineralization and eruption of mandibular teeth in mule deer. Journal of Wildlife Management 30:629631.
Richards, M. P., and Hedges, R. E. M. 2003. Variations in bone collagen δ13C and δ15N values of fauna from Northwest Europe over the last 40 000 years. Palaeogeography, Palaeoclimatology, Palaeoecology 193:261267.
Rossetti, D. de F., de Toledo, P. M., Moraes-Santos, H. M., and de Araujo Santos, A. E. Jr. 2004. Reconstructing habitats in central Amazonia using megafauna, sedimentology, radiocarbon, and isotope analyses. Quaternary Research 61:289300.
Rozanski, K., Araguas-Araguas, L., and Gonfiantini, R. 1992. Relation between long term trends of oxygen-18 isotope composition of precipitation and climate. Science 258:981985.
Sage, R. F., Wedin, D. A., and Li, M. 1999. The biogeography of C4 photosynthesis: patterns and controlling factors. Academic Press, New York.
Schoener, T. W. 1974. The compression hypothesis and temporal resource partitioning. Proceedings of the National Academy of Sciences USA 71:41694172.
Semprebon, G., Janis, C. M., and Solounias, N. 2004. The diets of the Dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change. Journal of Vertebrate Paleontology 24:427444.
Severinghaus, C. W. 1949. Tooth development and wear as criteria of age in white-tailed deer. Journal of Wildlife Management 13:195217.
Solounias, N., Moelleken, M. C., and Plavcan, J. M. 1995. Predicting the diets of extant bovids using masseteric morphology. Journal of Vertebrate Paleontology 14:287300.
Stowe, L. G., and Teeri, J. A. 1978. The geographic distribution of C4 species of the Dicotyledonae in relation to climate. American Naturalist 112:609623.
Tedford, R. H., Albright, L. B. III, Barnosky, A. D., Ferrusquia-Villafranca, I., Hunt, R. M., Storer, J. E., Swisher, C. C. III, Voorhies, M. R., Webb, S. D., and Whistler, D. P. 2004. Mammalian biochronology of the Arikareean through Hemphillian interval (Late Oligocene through Early Pliocene epochs). Pp. 169231 in Woodburne, M. O., ed. Late Cretaceous and Cenozoic mammals of North America: biostratigraphy and geochronology. Columbia University Press, New York.
Teeri, J. A., and Stowe, L. G. 1976. Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:112.
Tieszen, L. L. 1978. Carbon isotope fractionation in biological materials. Nature 276:9798.
Tieszen, L. L. 1994. Stable isotopes on the plains: vegetation analyses and diet determinations. Pp. 261282 in Owsley, D. W. and Jantz, R. L., eds. Skeletal biology in the Great Plains: migration, warfare, health, and subsistence. Smithsonian Institution Press, Washington D.C.
Tieszen, L. L., Hein, D., Qvortrup, S. A., Troughton, J. H., and Imbamba, S. K. 1979. Use of δ13C values to determine vegetation selectivity in East African herbivores. Oecologia 37:351359.
Tieszen, L. L., Reed, B. C., Bliss, N. B., Wylie, B. K., and Dejong, D. D. 1997. NDVI, C3 and C4 production, and distribution in Great Plains grassland land cover classes. Ecological Applications 7:5978.
van der Merwe, N. A., and Medina, E. 1991. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. Journal of Archaeological Science 18:249259.
Vogel, J. C. 1978. Isotopic assessment of the dietary habits of ungulates. South African Journal of Science 74:298301.
Wang, Y., Cerling, T. E., and MacFadden, B. J. 1994. Fossil horses and carbon isotopes: new evidence for Cenozoic dietary, habitat, and ecosystem changes in North America. Palaeogeography Palaeoclimatology Palaeoecology 107:269279.
Webb, S. D. 1983. A new species of Pediomeryx from the Late Miocene of Florida, and its relationships within the Subfamily Cranioceratinae (Ruminantia: Dromomerycidae). Journal of Mammalogy 64:261276.
Webb, S. D., MacFadden, B. J., and Baskin, J. A. 1981. Geology and paleontology of the Love Bone Bed from the late Miocene of Florida. American Journal of Science 281:513544.
Wegrzyn, M., and Serwatka, S. 1984. Teeth eruption in the European bison. Acta Theriologica 29:111121.
Yakir, D. 1992. Variations in the natural abundance of oxygen-18 and deuterium in plant carbohydrates. Plant, Cell and Environment 15:10051020.
Yakir, D., and Sternberg, L. da S. L. 2000. The use of stable isotopes to study ecosystem gas exchange. Oecologia 123:297311.
Yakir, D., DeNiro, M. J., and Gat, J. R. 1990. Natural deuterium and oxygen-18 enrichment in leaf water of cotton plants grown under wet and dry conditions: evidence for water compartmentation and its dynamics. Plant, Cell and Environment 13:4956.
Type Description Title
PDF
Supplementary materials

Feranec and MacFadden supplementary material
Appendix

 PDF (63 KB)
63 KB

Metrics

Full text views

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

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed