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Stable isotope evidence for changes in dietary niche partitioning among hadrosaurian and ceratopsian dinosaurs of the Hell Creek Formation, North Dakota

Published online by Cambridge University Press:  08 April 2016

Henry C. Fricke  and
Dean A. Pearson
Henry C. Fricke
Affiliation:
Department of Geology, Colorado College, Colorado Springs, Colorado 80903. E-mail: hfricke@coloradocollege.edu
Dean A. Pearson
Affiliation:
Department of Paleontology, Pioneer Trails Regional Museum, Bowman, North Dakota 58623
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Abstract

Questions related to dinosaur behavior can be difficult to answer conclusively by using morphological studies alone. As a complement to these approaches, carbon and oxygen isotope ratios of tooth enamel can provide insight into habitat and dietary preferences of herbivorous dinosaurs. This approach is based on the isotopic variability in plant material and in surface waters of the past, which is in turn reflected by carbon and oxygen isotope ratios of animals that ingested the organic matter or drank the water. Thus, it has the potential to identify and characterize dietary and habitat preferences for coexisting taxa.

In this study, stable isotope ratios from coexisting hadrosaurian and ceratopsian dinosaurs of the Hell Creek Formation of North Dakota are compared for four different stratigraphic levels. Isotopic offsets between tooth enamel and tooth dentine, as well as taxonomic differences in means and in patterns of isotopic data among taxa, indicate that primary paleoecological information is preserved. The existence of taxonomic offsets also provides the first direct evidence for dietary niche partitioning among these herbivorous dinosaur taxa. Of particular interest is the observation that the nature of this partitioning changes over time: for some localities ceratopsian dinosaurs have higher carbon and oxygen isotope ratios than hadrosaurs, indicating a preference for plants living in open settings near the coast, whereas for other localities isotope ratios are lower, indicating a preference for plants in the understory of forests. In most cases the isotope ratios among hadrosaurs are similar and are interpreted to represent a dietary preference for plants of the forest canopy. The inferred differences in ceratopsian behavior are suggested to represent a change in vegetation cover and hence habitat availability in response to sea level change or to the position of river distributaries. Given our current lack of taxonomic resolution, it is not possible to determine if dietary and habitat preferences inferred from stable isotope data are associated with single, or multiple, species of hadrosaurian/ceratopsian dinosaurs.

Type
Articles
Information
Paleobiology , Volume 34 , Issue 4 , Fall 2008 , pp. 534 - 552
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Amiot, R., Lecuyer, C., Buffetaut, E., Escarguel, G., Fluteau, F., and Martineau, F. 2006. Oxygen isotopes from biogenic apatites suggest widespread endothermy in Cretaceous dinosaurs. Earth and Planetary Science Letters 246:41–54.Google Scholar
Aucour, A.-M., Gomez, B., Sheppard, S. M. F., and Thevenard, F. 2008. δ13C and stomatal number variability in the Cretaceous conifer Frenelopsis . Palaeogeography, Palaeoclimatology, Paleoecology 257:462–473.Google Scholar
Badgley, C. 1986. Counting individuals in mammalian fossil assemblages from fluvial environments. Palaios 1:328–338.CrossRefGoogle Scholar
Bocherens, H. 2003. Isotopic biogeochemistry and the paleoecology of the mammoth steppe fauna. Deinsea 9:57–76.Google Scholar
Bocherens, H., Koch, P. L., Mariotti, A., Geraads, D., and Jaeger, J. J. 1996. Isotopic biogeochemistry (13C, 18O) and mammalian enamel from African Pleistocene hominid sites. Palaios 11:306–318.Google Scholar
Botha, J., Lee-Thorp, J., and Chinsamy, A. 2005. The palaeoecology of the non-mammalian cynodonts Diademodon and Cynognathus from the Karoo Basin of South Africa, using stable light isotope analysis. Palaeogeography, Palaeoclimatology, Paleoecology 223:303–316.Google Scholar
Boutton, T. W. 1991. Stable carbon isotope ratios of natural materials. II. Atmospheric, terrestrial, marine, and freshwater environments. Pp. 173–185 in Coleman, D. C. and Fry, B., eds. Carbon isotope techniques. Academic Press, New York.Google Scholar
Brinkman, D. B., Ryan, M. J., and Eberth, D. A. 1998. The paleogeographic and stratigraphic distribution of ceratopsids (Ornithischia) in the upper Judith River Group of western Canada. Palaios 13:160–169.Google Scholar
Bryant, J. D., and Froelich, P. N. 1995. A model of oxygen isotope fractionation in body water of large mammals. Geochimica et Cosmochimica Acta 59:4523–4537.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 120:347–363.Google Scholar
Cerling, T. E., Hart, J. A., and Hart, T. B. 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138:5–12.Google Scholar
Chin, K., Tokaryk, G. M., Erickson, G. M., and Calk, L. C. 1998. A king-sized theropod coprolite. Nature 393:680–682.Google Scholar
Clementz, M. T., and Koch, P. L. 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129:461–472.Google Scholar
Clementz, M. T., Hoppe, K. A., and Koch, P. L. 2003. A paleoecological paradox: the habitat and dietary preferences of the extinct tethythere Desmostylus, inferred from stable isotope analysis. Paleobiology 29:506–519.Google Scholar
Clementz, M. T., Goswami, A., Gingerich, P. D., and Koch, P. L. 2006. Isotopic records from early whales and sea cows: contrasting patterns of ecological transition. Journal of Vertebrate Paleontology 26:355–370.Google Scholar
Dansgaard, W. 1964. Stable isotopes in precipitation. Tellus 16:436–468.Google Scholar
DeNiro, M. J., and Epstein, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495–506.Google Scholar
Dettman, D. L., and Lohmann, K. 2000. Oxygen isotope evidence for high-altitude snow in the Laramide Rocky Mountains of North America during the Late Cretaceous and Paleogene. Geology 28:243–246.Google Scholar
Dodson, P., Forster, C. A., and Sampson, S. D. 2004. Ceratopsidae. Pp. 494–516 in Weishampel, et al., 2004b.Google Scholar
Epstein, S., and Mayeda, T. 1953. Variations in the 18-O content of waters from natural sources. Geochimica et Cosmochimica Acta 4:213–224.Google Scholar
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.Google Scholar
Fastovsky, D. E. 1987. Paleoenvironments of vertebrate-bearing strata during the Cretaceous-Paleogene transition, eastern Montana and western North Dakota. Palaios 2:282–295.Google Scholar
Fastovsky, D. E., and Smith, J. B. 2004. Dinosaur Paleoecology. Pp. 614–626 in Weishampel, et al., 2004b.CrossRefGoogle Scholar
Feranec, R. S., and MacFadden, B. J. 2006. Isotopic discrimination of resource partitioning among ungulates in C3-dominated communities from the Miocene of Florida and California. Paleobiology 32:191–205.Google Scholar
Fricke, H. C. 2007. Stable isotope geochemistry of bonebed fossils: reconstructing paleoenvironments, paleoecology, and paleobiology. Pp. 437–490 in Rogers, R. R., Eberth, D. A., and Fiorillo, A. R., eds. Bonebeds: genesis, analysis, and paleobiological significance. University of Chicago Press, Chicago.Google Scholar
Fricke, H. C., and O'Neil, J. R. 1996. Inter- and intra-tooth variations in the oxygen isotope composition of mammalian tooth enamel: some implications for paleoclimatological and paleobiological research. Palaeogeography, Palaeoclimatology, Paleoecology 126:91–99.Google Scholar
Fricke, H. C., and Rogers, R. R. 2000. Multiple taxon-multiple locality approach to providing oxygen isotope evidence for warm-blooded theropod dinosaurs. Geology 28:799–802.Google Scholar
Fricke, H. C., Clyde, W. C., O'Neil, J. R., and Gingerich, P. D. 1998. Intra-tooth variation in δ18O of mammalian tooth enamel as a record of seasonal changes in continental climate variables. Geochimica et Cosmochimica Acta 62:1839–1851.Google Scholar
Fricke, H. C., Rogers, R. R., Backlund, R., Dwyer, C. N., Echt, S. 2008. Preservation of primary stable isotope signals in dinosaur remains, and environmental gradients of the Late Cretaceous of Montana and Alberta. Palaeogeography, Palaeoclimatology, Paleoecology (in press).CrossRefGoogle Scholar
Gannes, L. Z., Rio, C. M. d., and Koch, P. 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comprehensive Biochemical Physiology A 119:725–737.Google Scholar
Gat, J. R. 1996. Oxygen and hydrogen isotopes in the hydrologic cycle. Annual Review of Earth Planetary Sciences 24:225–262.CrossRefGoogle Scholar
Hartman, J. H., and Kirtland, J. I. 2002. Brackish and marine molluscs of the Hell Creek Formation of North Dakota: evidence for a persisting Cretaceous seaway. Pp. 271–296 in Hartman, et al. 2002.Google Scholar
Hartman, J. H., Johnson, K. R., and Nichols, D. J., eds. 2002. The Hell Creek Formation and the Cretaceous-Tertiary boundary in the northern Great Plains: an integrated continental record of the end of the Cretaceous. Geological Society of America Special Paper 361.Google Scholar
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 Sciences 26:637–649.CrossRefGoogle Scholar
Hedges, R. E. M. 2003. On bone collagen—apatite-carbonate isotopic relationships. International Journal of Osteoarchaeology 13:66–79.Google Scholar
Hicks, J. F., Johnson, K. R., Obradovich, J. D., Tauxe, L., and Clark, D. 2002. Magnetostratigraphy and geochronology of the Hell Creek and basal Fort Union Formations of southwestern North Dakota and a recalibration of the age of the Cretaceous-Tertiary boundary. Pp. 35–56 in Hartman, et al. 2002.Google Scholar
Hillson, S. 1986. Teeth. Cambridge University Press, Cambridge.Google Scholar
Hoppe, K. A., Amundson, R. G., Vavra, M., McClaran, M. P., and Anderson, D. L. 2004. Isotopic analysis of tooth enamel carbonate from modern North American feral horses: implications for paleoenvironmental reconstructions. Palaeogeography, Palaeoclimatology, Paleoecology 203:299–311.Google Scholar
Horner, J. R., Weishampel, D. B., and Forster, C. A. 2004. Hadrosauridae. Pp. 438–463 in Weishampel, et al., 2004b.Google Scholar
Jim, S., Ambrose, S., and 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 68:61–72.CrossRefGoogle Scholar
Johnson, K. R. 2002. Megaflora of the Hell Creek and lower Fort Union Formation in North Dakota: vegetational response to climate change, the Cretaceous-Tertiary boundary event, and rapid marine transgression. Pp. 329–392 in Hartman, et al. 2002.Google Scholar
Johnson, B. J., Fogel, M., and Miller, G. H. 1998. Stable isotopes in modern ostrich eggshell: a calibration for paleoenvironmental applications in semi-arid regions of southern Africa. Geochimica et Cosmochimica Acta, 62:2451–2461.Google Scholar
Koch, P. L. 1998. Isotopic reconstruction of past continental environments. Annual Review of Earth and Planetary Sciences 26:573–613.Google Scholar
Koch, P. L., Fogel, M., and Tuross, N. 1994. Tracing the diet of fossil animals using stable isotopes. Pp. 63–94 in Lajtha, K. and Michener, R., eds. Stable isotopes in ecology and environmental science. Blackwell Science, Oxford.Google Scholar
Koch, P. L., Tuross, N., and Fogel, M. L. 1997. The effects of sample treatment and diagnosis on the isotopic integrity of carbonate in biogenic hydroxyapatite. Journal of Archaeological Sciences 24:417–429.Google Scholar
Kohn, M. J. 1996. Predicting animal δ18O: accounting for diet and physiological adaptation. Geochimica et Cosmochimica Acta 60:4811–4829.Google Scholar
Kohn, M. J., and Cerling, T. E. 2002. Stable isotope compositions of biological apatite. Reviews in Mineralogy and Geochemistry 48:455–488.Google Scholar
Kohn, M. J., Schoeninger, M. J., and Valley, J. W. 1998. Variability in herbivore tooth oxygen isotope compositions: reflections of seasonality or developmental physiology? Chemical Geology 152:92–112.Google Scholar
Kolodny, Y., Luz, B., Sander, M., and Clemens, W. A. 1996. Dinosaur bones: fossils of pseudomorphs? The pitfalls of physiology reconstruction from apatitic fossils. Palaeogeography, Palaeoclimatology, Palaeoecology 126:161–171.Google Scholar
Lehman, T. M. 1987. Late Maastrichtian paleoenvironments and dinosaur biogeography in the western interior of North America. Palaeogeography, Palaeoclimatology, Paleoecology 60:189–217.Google Scholar
Lehman, T. M. 2001. Late Cretaceous dinosaur provinciality. Pp. 310–328 in Tanke, D. and Carpenter, K., eds. Mesozoic vertebrate life. Indiana University Press, Bloomington.Google Scholar
Lockheart, M. J., Poole, I., Van Bergen, P. F., and Evershed, R. P. 1998. Leaf carbon isotope compositions and stomatal characters: important considerations for palaeoclimate reconstructions. Organic Geochemistry 29:1003–1008.Google Scholar
Longinelli, A. 1984. Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research? Geochimica et Cosmochimica Acta 48:385–390.Google Scholar
Luz, B., and Kolodny, Y. 1985. Oxygen isotope variations in phosphates of biogenic apatites. IV. Mammal teeth and bones. Earth and Planetary Science Letters 75:29–36.Google Scholar
MacFadden, B. J., and Higgins, P. 2004. Ancient ecology of 15-million-year-old browsing mammals within C3 plant communities from Panama. Oecologia 140:169–182.Google Scholar
Martinelli, L. A., Almeida, S., Brown, I. F., Moreira, M. Z., Victoria, R. L., Sternberg, L. S. L., Ferreira, C. A. C., and Thomas, W. W. 1998. Stable carbon isotope ratio of tree leaves, boles, and fine litter in a tropical forest in Rondonia, Brazil. Oecologia 114:170–179.CrossRefGoogle Scholar
McKee, K. L., Feller, I. C., Popp, M., and Wanek, W. 2002. Mangrove isotopic (d15N and d13C) fractionation across a nitrogen vs. phosphorous limitation gradient. Ecology 83:1065–1075.Google Scholar
Murphy, E. C., Hoganson, J. W., and Johnson, K. R. 2002. Lithostratigraphy of the Hell Creek Formation in North Dakota. Pp. 9–34 in Hartman, et al. 2002.Google Scholar
Nelson, B. K., DeNiro, M. J., and Schoeninger, M. J. 1986. Effects of diagenesis on strontium, carbon, nitrogen, and oxygen concentration and isotopic composition of bone. Geochimica et Cosmochimica Acta 50:1941–1949.Google Scholar
Tu, T. T. Nguyen, Bocherens, H., Mariotti, A., Baudin, F., Pons, D., Broutin, J., Derenne, S., and Largeau, C. 1999. Ecological distribution of Cenomanian terrestrial plants based on 13C/12C ratios. Palaeogeography, Palaeoclimatology, Paleoecology 145:79–93.Google Scholar
O'Leary, M. H. 1988. Carbon isotopes in photosynthesis. Bioscience 38:328–336.Google Scholar
O'Leary, M. H., Mahavan, S., and Paneth, P. 1992. Physical and chemical basis of carbon isotope fractionation in plants. Plant, Cell and Environment 15:1099–1104.Google Scholar
Passey, B. H., Robinson, T. F., Ayliffe, L. K., Cerling, T. E., Sponheimer, M., Dearing, M. D., Roeder, B. L., and Ehleringer, J. R. 2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. Journal of Archaeological Sciences 32:1459–1470.Google Scholar
Pearson, D. A., Schaefer, T., Johnson, K. R., and Nichols, D. J. 2001. Palynologically calibrated vertebrate record from North Dakota consistent with abrupt dinosaur extinction at the K-T boundary. Geology 29:39–42.Google Scholar
Pearson, D. A., Schaefer, T., Johnson, K. R., Nichols, D. J., Hunter, J. P. 2002. Vertebrate biostratigraphy of the Hell Creek Formation in southwestern North Dakota and northwestern South Dakota. Pp. 145–168 in Hartman, et al., 2002 Google Scholar
Rozanski, K., Araguás-Araguás, L., and Gonfiantini, R. 1993. Isotopic patterns in modern global precipitation. Pp. 1–36 in Swart, P. K., Lohmann, K. C., McKenzie, J., and Savings, S., eds. Climate change in the continental isotopic records. Geophysical Monograph 78. American Geophysical Union, Washington, D.C. Google Scholar
Sage, R. F., and Monson, R. K. 1999. C4 plant biology. Academic Press, San Diego.Google Scholar
Sharp, Z. D., and Cerling, T. E. 1998. Fossil isotope records of seasonal climate and ecology: straight from the horse's mouth. Geology 26:219–222.Google Scholar
Sheehan, P. M., Fastovsky, D. E., Hoffman, R. G., Berghaus, C. B., and Gabriel, D. L. 1991. Sudden extinction of the dinosaurs: Latest Cretaceous, upper Great Plains, USA. Science 254:835–839.Google Scholar
Sheehan, P. M., Fastovsky, D. E., Barreto, C., and Hoffman, R. G. 2000. Dinosaur abundance was not declining in a “3 m gap” at the top of the Hell Creek Formation, Montana and North Dakota. Geology 28:523–526.2.0.CO;2>CrossRefGoogle Scholar
Spotila, J. R. 1980. Constraints of body size and environment on the temperature regulation of dinosaurs. Pp. 233–252 in Thomas, R. D. K. and Olson, E. C., eds. A cold look at warm-blooded dinosaurs (American Association for the Advancement of Science Selected Symposium 28). Westview, Boulder, Colo. Google Scholar
Stanton-Thomas, K., and Carlson, S. J. 2003. Microscale d18O and d13C isotopic analysis of an ontogenetic series of the hadrosaurid dinosaur Edmontosaurus: implications for physiology and ecology. Palaeogeography, Palaeoclimatology, Paleoecology 206:257–287.Google Scholar
Sternberg, L. S. L. 1989. Oxygen and hydrogen isotope ratios in plant cellulose: mechanisms and applications. Pp. 124–141 in Rundel, P. W., Ehleringer, J. R., and Nagy, K. A., eds. Stable isotopes in ecological research. Springer, Heidelberg.Google Scholar
Straight, W. H., Barrick, R. E., and Eberth, D. A. 2004. Reflections of surface water, seasonality and climate in stable oxygen isotopes from tyrannosaurid tooth enamel. Palaeogeography, Palaeoclimatology, Paleoecology 206:239–256.CrossRefGoogle Scholar
Tieszen, L. L. 1991. Natural variations in carbon isotope values of plants: implications for archaeology, ecology, and paleoecology. Journal of Archaeological Sciences 20:227–248.Google Scholar
Trueman, C. N., and Tuross, N. 2002. Trace elements in recent and fossil bone apatite. Reviews in Mineralogy and Geochemistry 48:489–521.Google Scholar
Trueman, C. N., Behrensmeyer, A. K., Tuross, N., and Weiner, S. 2004. Mineralogical and compositional changes in bones exposed on soil surfaces in Amboseli National Park, Kenya: diagenetic mechanisms and the role of sediment pore fluids. Journal of Archaeological Science 31:721–739.Google Scholar
van der Merwe, N. J., and Medina, E. 1991. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. Journal of Archaeological Science 18:249–259.Google Scholar
Varricchio, D. J. 2001. Gut contents for a Cretaceous tyrannosaur: implications for theropod digestive tracts. Journal of Paleontology 75:401–406.Google Scholar
von Fischer, J. C., and Tieszen, L. T. 1995. Carbon isotope characterization of vegetation and soil organic matter in subtropical forests in Luquillo, Puerto Rico. Biotropica 27:138–148.Google Scholar
Weishampel, D. B., Barrett, P. M., Coria, R. A., LeLoeuff, J., Xing, X., Xijin, Z., Sahni, A., Gomani, E. M. P., and Noto, C. R. 2004a. Dinosaur distribution. Pp. 517–606 in Weishampel, et al., 2004b.Google Scholar
Weishampel, D. B., Dodson, P., and Osmolska, H., eds. 2004b. The Dinosauria. University of California Press, Berkeley.Google Scholar
White, P. D., Fastovsky, D. E., and Sheehan, P. M. 1998. Taphonomy and suggested structure of the dinosaurian assemblage of the Hell Creek Formation (Maastrichtian), eastern Montana and western North Dakota. Palaios 13:41–51.Google Scholar
Wilf, P., Johnson, K. R. and Huber, B. T. 2003. Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary. Proceedings of the National Academy of Sciences USA 100:599–604.Google Scholar
Wooller, M., Smallwood, B., Scharler, U., Jacobson, M., and Fogel, M. 2003. A taphonomic study of d13C and d15N values in Rhizophora mangle leaves for a multi-proxy approach to mangrove palaeoecology. Organic Geochemistry 34:1259–1275.Google Scholar
Zazzo, A., Lecuyer, C., and Mariotti, A. 2004. Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions. Geochimica et Cosmochimica Acta 68:1–12.Google Scholar
Zylberberg, L., Sire, J. Y., and Nanci, A. 1997. Immunodetection of amelogenin-like proteins in the ganoine of experimentally regenerating scales of Calamoichthys calabaricus, a primitive Actinopterygian fish. Anatomical Record 249:86–95.Google Scholar
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