Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-28T02:43:52.177Z Has data issue: false hasContentIssue false

Stable isotopes, hypsodonty, and the paleodiet of Hemiauchenia (Mammalia: Camelidae): a morphological specialization creating ecological generalization

Published online by Cambridge University Press:  08 April 2016

Robert S. Feranec*
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720. E-mail: feranec@socrates.berkeley.edu

Abstract

Morphological adaptations may indicate increased specialization (narrowing of ecological niche) or expansion of the suite of lifestyles available to an organism (increasing niche breadth). Hypsodonty in mammals generally has been interpreted as a specialization into a grazing niche from a browsing niche. Here I examine the feeding strategy of the extinct hypsodont camel Hemiauchenia through an analysis of stable carbon isotope values from its tooth enamel, which was used to clarify its feeding strategy and to resolve conflicting interpretations of dental versus muzzle attributes. The paleodiet of Hemiauchenia is then used to test whether hypsodonty correlates to grazing within fossil Lamini. This study focuses on fossils from Florida, which is geographically ideal because unlike other regions of the country almost all extant plants on which animals browse use the C3 photosynthetic pathway. In contrast, most of the grasses and sedges utilized by grazers use the C4 photosynthetic pathway. If Hemiauchenia was an obligate grazer, the stable carbon isotope values of tooth enamel should reflect primarily a diet of C4 grass and sedge (>−1.3%). If Hemiauchenia was mainly a browser, the isotopic value should be considerably more negative reflecting ingestion primarily of C3 browse (<−7.9%). The mean δ13C values for Hemiauchenia during each time interval average more negative than −8.0%, indicating a dominantly C3 browse diet, and there is no evidence for abandonment of the browsing niche from the Hemphillian through the Rancholabrean North American Land Mammal Ages. However, an increase in the range of isotopic values indicates a diet with a higher proportion of C4 grasses and sedges through time. This study therefore suggests that Hemiauchenia was a hypsodont intermediate feeder with preference for browse during the past 5 million years. Hypsodonty is not strictly associated with obligate grazing; instead it may, in this case, represent an adaptation to widen niche breadth that allowed grazing as well as browsing.

Type
Articles
Copyright
Copyright © The Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Bryant, J. D., Froelich, P. N., Showers, W. J., and Genna, B. J. 1996a. A tale of two quarries: biologic and taphonomic signatures in the oxygen isotopic composition of tooth enamel phosphate from modern and Miocene equids. Palaios 11:397408.Google Scholar
Bryant, J. D., Froelich, P. N., Showers, W. J., and Genna, B. J. 1996b. Biologic and climatic signals in the oxygen isotopic composition of Eocene-Oligocene equid enamel phosphate. Palaeogeography, Palaeoclimatology, Palaeoecology 126:7589.Google Scholar
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.Google Scholar
Cerling, T. E., Harris, J. M., and Leakey, M. G. 1999. Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia 120:364374.Google Scholar
Cowling, S. A. 1999. Simulated effects of low atmospheric CO2 on structure and composition of North American vegetation at the Last Glacial Maximum. Global Ecology and Biogeography 8:8193.Google Scholar
DeNiro, M. J., and Epstein, S. 1978. Carbon isotopic evidence for different feeding patterns in two hyrax species occupying the same habitat. Science 201:906908.Google Scholar
Dompierre, H., and Churcher, C. S. 1996. Premaxillary shape as an indicator of the diet of seven extinct late Cenozoic New World camels. Journal of Vertebrate Paleontology 16:141148.Google Scholar
Easley, M. C., and Judd, W. S. 1990. Vascular flora of the southern upland property of Paynes Prairie State Preserve, Alachua County, Florida. Castanea 55:142186.Google Scholar
Ehleringer, J. R., and Monson, R. K. 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics 24:411439.Google Scholar
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.Google Scholar
Ehleringer, J. R., Cerling, T. E., and Helliker, B. R. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285299.Google Scholar
Emslie, S. D., and Morgan, G. S. 1995. Taphonomy of a late Pleistocene carnivore den, Dade County, Florida. Pp. 6583in Steadman, D. W. and Mead, J. I., eds. Late Quaternary environments and deep history: a tribute to Paul S. Martin. Scientific Papers, Vol. 3. The Mammoth Site of Hot Springs, Hot Springs, S. Dak.Google Scholar
Feranec, R. S., and MacFadden, B. J. 2000. Evolution of the grazing niche in Pleistocene mammals from Florida: evidence from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology 162:155169.Google Scholar
Fraser, M. D. 1998. Diet composition of guanacos (Lama guanicoe) and sheep (Ovis aries) grazing in grassland communities typical of UK uplands. Small Ruminant Research 29:201212.Google Scholar
Fraser, M. D. 1999. A comparison of the diet composition of guanacos (Lama guanicoe) and sheep when grazing swards with different clover: grass ratios. Small Ruminant Research 32:231241.Google Scholar
Friedli, H., Lötscher, H., Oeschger, H., Seigenthaler, U., and Stauffer, B. 1986. Ice core record of the 13C/12C ratio of atmospheric CO2 in the past two centuries. Nature 324:237238.Google Scholar
Gauthier-Pilters, H. 1984. Aspects of dromedary ecology and ethology. Pp. 412430in Cockrill, W. R., ed. The camelid: an all-purpose animal. Scandinavian Institute of African Studies, Uppsala.Google Scholar
Heckathorn, S. A., McNaughton, S. J., and Coleman, J. S. 1999. C4 plants and herbivory. Pp. 285312in Sage, R. F. and Monson, R. K., eds. C4 plant biology. Academic Press, New York.Google Scholar
Hillson, S. 1986. Teeth. Cambridge University Press, Cambridge.Google Scholar
Hofmann, R. R., and Stewart, D. R. M. 1972. Grazer or browser: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia 36:226240.Google Scholar
Honey, J. G., Harrison, J. A., Prothero, D. R., and Stevens, M. S. 1998. Camelidae. Pp. 439462in Janis, C. M., Scott, K. M., and Jacobs, L. L., eds. Evolution of Tertiary mammals of North America, Vol. 1. Terrestrial carnivores, ungulates, and ungulatelike mammals. Cambridge University Press, New York.Google Scholar
Huffman, J. M., and Judd, W. S. 1998. Vascular flora of Myakka River State Park, Sarasota and Manatee Counties, Florida. Castanea 63:2550.Google Scholar
Hutchinson, G. E. 1958. Concluding remarks. Cold Springs Harbor Symposium on Quantitative Biology 22:415427.Google Scholar
Janis, C. M. 1988. An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preferences. Pp. 367387in Russell, D. E., Santoro, J. P., and Sigogneau-Russell, D., eds. Teeth revisited: proceedings of the VIIIth international symposium on dental morphology, Paris 1986. Mémoires du Muséum National d'Histoire Naturelle C 53: 367–387.Google Scholar
Janis, C. M. 1989. A climatic explanation for patterns of evolutionary diversity in ungulate mammals. Palaeontology 32:463481.Google Scholar
Janis, C. M. 1995. Correlations between craniodental and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. Pp. 7698in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Janis, C. M., and Ehrhardt, D. 1988. Correlation of relative muzzle width and relative incisor width with dietary preference in ungulates. Zoological Journal of the Linnean Society 92:267284.Google Scholar
Janis, C. M., Damuth, J., and Theodor, J. M. 2000. Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? Proceedings of the National Academy of Sciences USA 97:78997904.Google Scholar
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.Google Scholar
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.Google Scholar
Koford, C. B. 1957. The vicuña and the puna. Ecological Monographs 27:153219.Google Scholar
Kohler-Rollefson, I. U. 1991. Camelus dromedarius. Mammalian Species 375:18.Google Scholar
Lundelius, E. L., Downs, T., Lindsay, E. H., Semken, H. A., Zakrzewski, R. J., Churcher, C. S., Harington, C. R., Shultz, G. E., and Webb, S. D. 1987. The North American Quaternary Sequence. Pp. 211235in Woodburne, M. O., ed. Cenozoic mammals of North America: geochronology and biostratigraphy. University of California Press, Berkeley.Google Scholar
MacFadden, B. J. 1995. Magnetic polarity stratigraphy and correlation of the Leisey Shell Pits, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:107116.Google Scholar
MacFadden, B. J. 1997. Origin and evolution of the grazing guild in New World terrestrial mammals. Trends in Ecology and Evolution 12:182187.Google Scholar
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.Google Scholar
MacFadden, B. J., Solunias, N., and Ceding, T. E. 1999. Ancient diets, ecology, and extinction of 5-million-year-old horses from Florida. Science 283:824827.Google Scholar
Marino, B. D., and McElroy, M. B. 1991. Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 249:127131.Google Scholar
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.Google Scholar
McNaughton, S. J. 1991. Evolutionary ecology of large tropical herbivores. Pp. 509522in Price, P. W., Lewinsohn, T. M., Fernandes, G. W., and Benson, W. W., eds. Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley-Interscience, New York.Google Scholar
McNaughton, S. J., Tarrants, J. L., McNaughton, M. M., and Davis, R. H. 1985. Silica as a defense against herbivory and a growth promoter in African grasses. Ecology 66:528535.Google Scholar
Migongo-Bake, W., and Hansen, R. M. 1987. Seasonal diets of camels, cattle, sheep, and goats in a common range in eastern Africa. Journal of Range Management 40:7679.Google Scholar
Newman, D. M. R. 1984. The feeds and feeding habits of Old and New World camels. Pp. 250292in Cockrill, W. R., ed. The camelid: an all-purpose animal. Scandinavian Institute of African Studies, Uppsala.Google Scholar
Nowak, R. M. 1999. Walker's mammals of the world, 6th ed. Johns Hopkins University Press, Baltimore.Google Scholar
O'Leary, M. H. 1988. Carbon isotopes in photosynthesis. Bio-Science 38:328336.Google Scholar
Perez-Barberia, F. J., Gordon, I. J., and Nores, C. 2001. Evolutionary transitions among feeding styles and habitats in ungulates. Evolutionary Ecology Research 3:221230.Google Scholar
Puig, S., Videla, F., Monge, S., and Roig, V. 1996. Seasonal variations in guanaco diet (Lama guanicoe Muller 1776) and food availability in northern Patagonia, Argentina. Journal of Arid Environments 34:215224.Google Scholar
Puig, S., Videla, F., and Cona, M. I. 1997. Diet and abundance of the guanaco (Lama guanicoe Muller 1776) in four habitats of northern Patagonia, Argentina. Journal of Arid Environments 36:343357.Google Scholar
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. J. 1992. A 16-Ma record of paleodiet using carbon and oxygen isotopes in fossil teeth from Pakistan. Chemical Geology (Isotope Geosciences Section) 94:183192.Google Scholar
Rich, F. J., and Newsom, L. A. 1995. Preliminary palynology and macroplant report for the Leisey Shell Pits, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:117126.Google Scholar
Sage, R. F., Wedin, D. A., and Li, M. 1999. The biogeography of C4 photosynthesis: patterns and controlling factors. Pp. 313373in Sage, R. F. and Monson, R. K., eds. C4 plant biology. Academic Press, New York.Google Scholar
Schoeninger, M. J., and DeNiro, M. J. 1982. Carbon isotope ratios of apatite from fossil bone cannot be used to reconstruct diets of ancient animals. Nature 297:577578.Google Scholar
Solounias, N., Teaford, M., and Walker, A. 1988. Interpreting the diet of extinct ruminants: the case of a non-browsing giraffid. Paleobiology 14:287300.Google Scholar
Solounias, N., Moelleken, M. C., and Plavcan, J. M. 1995. Predicting the diets of extinct bovids using masseteric morphology. Journal of Vertebrate Paleontology 15:795805.Google Scholar
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.Google Scholar
Strömberg, C. A. E. 2002. The origin and spread of grass-dominated ecosystems in the late Tertiary of North America: preliminary results concerning the evolution of hypsodonty. Palaeogeography, Palaeoclimatology, Palaeoecology 177:5975.Google Scholar
Strömberg, C. A. E., LaGarry, H. E., and LaGarry, L. A. 2000. New paleobotanical records from the late Tertiary of Nebraska. Geological Society of America Abstracts with Programs 32:A-221.Google Scholar
Teeri, J. A., and Stowe, L. G. 1976. Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:112.Google Scholar
Teeri, J. A., Stowe, L. G., and Livingstone, D. A. 1980. The distribution of C4 species of the Cyperaceae in North America in relation to climate. Oecologia 47:307310.Google Scholar
Tieszen, L. L., Bradley, B. C., Bliss, N. B., Wylie, B. K., and Dejong, D. D. 1997. NDVI, C3 and C4 production, and distributions in Great Plains grassland land cover classes. Ecological Applications 7:5978.Google Scholar
Wang, Y., and Cerling, T. E. 1994. A model of fossil tooth and bone diagenesis: implications for paleodiet reconstruction from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology 107:281289.Google Scholar
Webb, S. D. 1974. Pleistocene mammals of Florida. University Presses of Florida, Gainesville.Google Scholar
Webb, S. D. 1991. Historical Biogeography. Pp. 70100in Myers, R. L. and Ewel, J. J., eds. Ecosystems of Florida. University of Central Florida Press, Orlando.Google Scholar
Webb, S. D., and Stehli, F. G. 1995. Selenodont Artiodactyla (Camelidae and Cervidae) from the Leisey Shell Pits, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:621643.Google Scholar
Witmer, L. M. 1995. The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils. Pp. 1933in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Woodburne, M. O. 1987. Cenozoic mammals of North America: geochronology and biostratigraphy. University of California Press, Berkeley.Google Scholar