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Understanding specifics in generalist diets of carnivorans by analyzing stable carbon isotope values in Pleistocene mammals of Florida

Published online by Cambridge University Press:  08 April 2016

Robert S. Feranec  and
Larisa R. G. DeSantis
Robert S. Feranec*
Affiliation:
Research and Collections, New York State Museum, CEC 3140, Albany, New York 12230, U.S.A. E-mail: [email protected].
Larisa R. G. DeSantis
Affiliation:
Department of Earth and Environmental Science, Vanderbilt University, 2301 Vanderbilt Place, PMB 351805, Nashville, Tennessee 37235-1805, U.S.A. E-mail: [email protected]
*
Corresponding author
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Abstract

Within ancient ecosystems, it is generally difficult to determine the specific diets of species from higher trophic levels, which in turn hinders our understanding of trophic relationships and energy flow through these systems. To better understand the ecology of taxa at higher trophic levels, we used analysis of tooth enamel stable carbon isotope values to infer the dietary preferences of Canis edwardii and Smilodon gracilis from the Leisey Shell Pit 1A (LSP 1A) and Inglis 1A, two Pleistocene localities in Florida. The goals of the analyses were to (1) determine whether these carnivorans specialized in particular prey types or maintained a generalist diet; (2) ascertain whether carbon isotope values support what was previously suggested about the ecology of these species; and (3) establish what ecological details of ancient food webs can be discovered by carbon isotope analyses at higher trophic levels. Results show that the sampled carnivoran carbon isotope values are distributed among suspected prey isotope values, suggesting that varied prey were taken at the study localities. Prey compositions were modeled for each carnivoran species by using Stable Isotope Analysis in R (SIAR). The modeled diets indicate that each studied carnivoran had a generalist diet; however, there are differences in how these taxa achieved dietary generalization. At the glacial Inglis 1A locality, sampled individuals of C. edwardii and S. gracilis show similar isotope values and modeled dietary prey proportions, although both carnivorans do show a preference for grazing prey species. The similar isotopic values, and calculated prey proportions, observed between these species may imply greater interspecific competition for food. At the interglacial LSP 1A locality, C. edwardii shows values similar to those observed at Inglis 1A. In contrast, the data for S. gracilis shows a preference for consuming browsing prey species. Further, its restricted range of carbon isotope values suggests that S. gracilis may have concentrated its feeding within a particular habitat. Examination of stable carbon isotope values among species at higher trophic levels reveals that some intricacies of ancient food webs can be discerned.

Type
Articles
Information
Paleobiology , Volume 40 , Issue 3 , Summer 2014 , pp. 477 - 493
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Akersten, W. A. 1985. Canine function in Smilodon (Mammalia; Felidae; Machairodontinae). Contributions in Science, Natural History Museum, Los Angeles County 356:1–22.Google Scholar
Ambrose, S. H. 1991. Effects of diet, climate and physiology of nitrogen isotope abundances in terrestrial foodwebs. Journal of Archaeological Science 18:293–317.Google Scholar
Ambrose, S. H., and DeNiro, M. J. 1986a. Reconstruction of African diet using bone collagen carbon and nitrogen isotope ratios. Science 319:321–324.Google Scholar
Ambrose, S. H., and DeNiro, M. J. 1986b. The isotopic ecology of East African mammals. Oecologia 69:395–406.Google Scholar
Ambrose, S. H., and DeNiro, M. J. 1987. Bone nitrogen isotope composition and climate. Nature 325:201.Google Scholar
Ambrose, S. H., and DeNiro, M. J. 1989. Climate and habitat reconstruction using stable carbon and nitrogen isotope ratios of collagen in prehistoric herbivore teeth from Kenya. Quaternary Research 31:407–422.Google Scholar
Bekoff, M. 1977. Canis latrans. Mammalian Species 79:1–9.CrossRefGoogle Scholar
Berta, A. 1987. The sabercat Smilodon gracilis from Florida and a discussion of its relationships (Mammalia, Felidae, Smilodontini). Bulletin of the Florida State Museum, Biological Sciences 31:1–63.Google Scholar
Berta, A. 1995. Fossil carnivores from the Leisey Shell Pits, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:463–500.Google Scholar
Biknevicius, A. R., Van Valkenburgh, B., and Walker, J. 1996. Incisor size and shape: implications for feeding behaviors in saber-toothed “cats.” Journal of Vertebrate Paleontology 16:510–521.Google Scholar
Bocherens, H. 2000. Preservation of isotopic signals (13C, 15N) in Pleistocene mammals. Pp. 65–88inKatzenberg, M. A. and Ambrose, S. H., eds. Biogeochemical approaches to paleodietary analyses. Academic Press/Plenum, New York.Google Scholar
Bocherens, H., Fizet, M., Mariotti, A., Billiou, D., Bellon, G., Borel, J.-P., and Simone, S. 1991. Biogéochimie isotopique (13C, 15N, 18O) et paleoécologie des ours pléistocènes de la Grotte d'Aldène. Bulletin du Musée d'Anthropologie Préhistorique de Monaco 34:29–47.Google Scholar
Bocherens, H., Fizet, M., and Mariotti, A. 1994. Diet, physiology and ecology of fossil mammals as inferred from stable carbon and nitrogen isotope biogeochemistry: implications for Pleistocene bears. Palaeogeography, Palaeoclimatology, Palaeoecology 107:213–225.Google Scholar
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 48:370–380.Google Scholar
Bocherens, H., Argant, A., Argant, J., Billiou, D., Cregut-Bonnoure, E., Donat-Ayache, B., Philippe, M., and Thinon, M. 2004. Diet reconstruction of ancient brown bears (Ursus arctos) from Mont Ventoux (France) using bone collagen stable isotope biogeochemistry. Canadian Journal of Zoology 82:576–586.Google Scholar
Bolnick, D. I., Svanback, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D., and Forister, M. L. 2003. The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161:1–28.Google Scholar
Bolnick, D. I., Yang, L. H., Fordyce, J. A., Davis, J. M., and Svanback, R. 2002. Measuring individual-level resource specialization. Ecology 83:2936–2941.CrossRefGoogle Scholar
Carpenter, K. 1998. Evidence of predatory behavior by carnivorous dinosaurs. Gaia 15:135–144.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., Harris, J. M., and Leakey, M. G. 1999. Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia 120:364–374.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
Clementz., M. T., Fox-Dobbs, K., Wheatley, P. V., Koch, P. L., and Doak, D. F. 2009. Revisiting old bones: coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool. Geological Journal 44:605–620.Google Scholar
Codron, J., Codron, D., Lee-Thorp, J. A., Sponheimer, M., Bond, W. J., de Ruiter, D., and Grant, R. 2005. Taxonomic, anatomical, and spatio-temporal variations in the stable carbon and nitrogen isotopic compositions of plants from an African savanna. Journal of Archaeological Science 32:1757–1772.Google Scholar
Coltrain, J. B., Harris, J. M., Cerling, T. E., Ehleringer, J. R., Dearing, M.-D., Ward, J., and Allen, J. 2004. Rancho La Brea stable isotope biogeochemistry and its implications for the palaeoecology of late Pleistocene, coastal southern California. Palaeogeography, Palaeoclimatology, Palaeoecology 205:199–219.Google Scholar
DeNiro, M. J., and Epstein, S. 1978a. Carbon isotopic evidence for different feeding patterns in two hyrax species occupying the same habitat. Science 201:906–908.Google Scholar
DeNiro, M. J., and Epstein, S. 1978b. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495–506.Google Scholar
DeSantis, L. R. G., Feranec, R. S., and MacFadden, B. J. 2009. Effects of global warming on ancient mammalian communities and their environments. PLoS ONE 4 (6):e5750. doi: 10.1371/journal.pone.0005750.Google Scholar
DeSantis, L. R. G., Schubert, B. W., Scott, J. R., and Ungar, P. S. 2012. Implications of diet for the extinction of saber-toothed cats and American lions. PLoS ONE 7 (12):e52453. doi: 10.1371/journal.pone.005245.Google Scholar
Domingo, M. S., Domingo, L., Badgley, C., Sanisidro, O., and Morales, J. 2013. Resource partition among top predators in a Miocene food web. Proceedings of the Royal Society of London B 280:20122138.Google Scholar
Ehleringer, J. R., and Monson, R. K. 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics 24:411–439.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 6:95–99.Google Scholar
Emerson, S. B., and Radinsky, L. 1980. Functional analysis of sabertooth cranial morphology. Paleobiology 6:295–312.CrossRefGoogle Scholar
Estes, J. A., 1996. Carnivorans and ecosystem management. Wildlife Society Bulletin 24:390–396.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 40:503–537.Google Scholar
Feranec, R. S. 2005. The growth rate and growth period of the adult canine in Smilodon gracilis, and inferences on diet by analyzing stable isotopes. Bulletin of the Florida Museum of Natural History 45:369–377.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 162:155–169.Google Scholar
Feranec, R. S., Hadly, E. A., and 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
Fox-Dobbs, K., Bump, J. K., Peterson, R. O., Fox, D. L., and Koch, P. L. 2007. Carnivore-specific stable isotope variables and variation in the foraging ecology of modern and ancient wolf populations: case studies from Isle Royale, Minnesota, and La Brea. Canadian Journal of Zoology 85:458–471.Google Scholar
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 324:237–238.Google Scholar
Garten, C. T. Jr., and Taylor, G. E. Jr. 1992. Foliar δ13C within a temperate deciduous forest: spatial, temporal, and species sources of variation. Oecologia 90:1–7.Google Scholar
Gonyea, W. J. 1976. Behavioral implications of saber-toothed felid morphology. Paleobiology 2:332–342.Google Scholar
Grocke, D. R. 1997. Stable-isotope studies on the collagenic and hydroxylapatite components of fossils: palaeoecological implications. Lethaia 30:65–78.Google Scholar
Guthrie, R. D. 1984. Mosaics, allelochemics and nutrients: an ecological theory of late Pleistocene megafaunal extinctions. Pp. 259–298inMartin, P. S. and Klein, R. G., eds. Quaternary extinctions: a prehistoric revolution. University of Arizona Press, Tucson.Google Scholar
Hairston, N. G. Jr., and Hairston, N. G. Sr. 1993. Cause–effect relationships in energy flow, trophic structure, and interspecific interactions. American Naturalist 142:379–411.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 Science 26:637–649.Google Scholar
Hillson, S. 2005. Teeth, 2nd ed. Cambridge University Press, Cambridge.Google Scholar
Hulbert, R. C. 2001. The fossil vertebrates of Florida. University of Florida Press, Gainesville.Google Scholar
Hunter, M. D., and Price, P. W. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732.Google Scholar
Koch, P. L. 1998. Isotopic reconstruction of past continental environments. Annual Review of Earth and Planetary Science 26:573–613.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 24:417–429.Google Scholar
Kohn, M. J., McKay, M. P., and Knight, J. L. 2005. Dining in the Pleistocene—who's on the menu? Geology 33:649–652.Google Scholar
Leuenberger, M., Siegenthaler, U., and Langway, C. C. 1992. Carbon isotope composition of atmospheric CO2 during the last ice age from an Antarctic ice core. Nature 357:488–490.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 37:107–116.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 16:103–115.Google Scholar
Marino, B. D., and McElroy, M. B. 1991. Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349:127–131.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 357:461–466.Google Scholar
Mech, L. D. 1974. Canis lupus. Mammalian Species 37:1–6.Google Scholar
Mole, S., Joern, A., O'Leary, M. H., and Madhaven, S. 1994. Spatial and temporal variation in carbon isotope discrimination in prairie graminoids. Oecologia 97:316–321.Google Scholar
Morgan, G. S., and Hulbert, R. C. 1995. Overview of the geology and vertebrate biochronology of the Leisey Shell Pit local fauna, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:1–92.Google Scholar
Newsome, S. D., Tinker, M. T., Monson, D. H., Oftedal, O. T., Ralls, K., Staedler, M. M., Fogel, M. L., and Estes, J. A. 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974.Google Scholar
Nowak, R. M. 1999. Walker's mammals of the world. Johns Hopkins University Press, Baltimore.Google Scholar
Ogg, G. 2009. International stratigraphic chart. International Commission on Stratigraphy. http://www.stratigraphy.org/ICSchart/StratChart2009; pdf, accessed February 2014.Google Scholar
O'Leary, M. H. 1988. Carbon isotopes in photosynthesis. BioScience 38:328–-336.CrossRefGoogle Scholar
Pace, M. L., Cole, J. J., Carpenter, S. R., and Kitchell, J. F. 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution 14:483–488.Google Scholar
Palmqvist, P., Grocke, D. R., Arribas, A., and Farina, R. A. 2003. Paleoecological reconstruction of a lower Pleistocene large mammal community using biogeochemical (δ13C, δ15N, δ18O, Sr:Zn) and ecomorphological approaches. Paleobiology 29:205–229.Google Scholar
Palmqvist, P., Perez-Claros, J. A., Janis, C. M., Figueirido, B., Torregosa, V., and Grocke, D. R. 2008a. Biogeochemical and ecomorphological inferences on prey selection and resource partitioning among mammalian carnivores in an early Pleistocene community. Palaios 23:724–737.Google Scholar
Palmqvist, P., Perez-Claros, J. A., Janis, C. M., and Grocke, D. R. 2008b. Tracing the ecophysiology of ungulates and carnivoran–prey relationships in an early Pleistocene large mammal community. Palaeogeography, Palaeoclimatology, Palaeoecology 266:95–111.Google Scholar
Paradiso, J. L., and Nowak, R. M. 1972. Canis rufus. Mammalian Species 22:1–4.Google Scholar
Parnell, A. C., Inger, R., Bearhop, S., and Jackson, A. L. 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672. doi: 10.1371/journal.pone.0009672.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 Science 32:1459–1470.Google Scholar
Phillips, D. L. 2001. Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127:166–170.Google Scholar
Phillips, D. L., and Gregg, J. W. 2003. Source partitioning using stable isotopes: coping with too many variables. Oecologia 136:261–269.Google Scholar
Phillips, D. L., and Koch, P. L. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125.Google Scholar
Phillips, D. L., Newsome, S. D., and Gregg, J. W. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527.Google Scholar
Post, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.Google Scholar
Pratt, A. E., and Hulbert, R. C. Jr. 1995. Taphonomy of the terrestrial mammals of Leisey Shell Pitt 1A, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:177–250.Google Scholar
Rawn-Schatzinger, V. 1992. The scimitar cat Homotherium serum Cope. Illinois State Museum Reports of Investigations 47:1–80.Google Scholar
R Core Development Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URLhttp://www.R-project.org/.Google Scholar
Roughgarden, J. 1972. Evolution of niche width. American Naturalist 106:683–718.Google Scholar
Schmitz, O. J., Hamback, P. A., and Beckerman, A. P. 2000. Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. American Naturalist 155:141–153.Google Scholar
Sealy, J. C., Armstrong, R., and Schrire, C. 1995. Beyond lifetime averages: tracing life histories through isotopic analysis of different calcified tissues from archaeological human skeletons. Antiquity 69:290–300.Google Scholar
Sillero-Zubiri, C., and Gottelli, D. 1994. Canis simensis. Mammalian Species 485:1–6.CrossRefGoogle Scholar
Slaughter, B. H., Pine, R. H., and Pine, N. E. 1974. Eruption of cheek teeth in Insectivora and Carnivora. Journal of Mammalogy 55:115–125.Google Scholar
Svanback, R., and Bolnick, D. I. 2005. Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evolutionary Ecology Research 7:993–1012.Google Scholar
Tejada-Flores, A. E., and Shaw, C. A. 1984. Tooth replacement and skull growth in Smilodon from Rancho La Brea. Journal of Vertebrate Paleontology 4:114–121.Google Scholar
Terborgh, J., Lopez, L., Nunez, V. P.Rao, M., Shahabuddin, G., Orihuela, G., Riveros, M., Ascanio, R., Adler, G. H., Lambert, T. D., and Balbas, L. 2001. Ecological meltdown in carnivoran-free forest fragments. Science 294:1923–1926.Google Scholar
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 37:351–359.Google Scholar
Urton, E. J. M., and Hobson, K. A. 2005. Intrapopulation variation in gray wolf isotope (δ15N and δ13C) profiles: implications for the ecology of individuals. Oecologia 145:317–326.CrossRefGoogle ScholarPubMed
Van Valkenburgh, B. 1987. Canine strength and killing behavior in large carnivores. Journal of Zoology 212:379–397.Google Scholar
Van Valkenburgh, B. 1989. Carnivore dental adaptations and diet: a study of trophic diversity within guilds. Pp. 410–436inGittleman, J. L., ed. Carnivore ecology, behavior, and evolution, Vol. 1. Cornell University Press, Ithaca, N.Y.Google Scholar
Van Valkenburgh, B. 1991. Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): evolutionary interactions among sympatric carnivorans. Paleobiology 17:340–361.Google Scholar
Vogel, J. C. 1978. Isotopic assessment of the dietary habits of ungulates. South African Journal of Science 74:298–301.Google Scholar
Walton, L. R., and Joly, D. O. 2003. Canis mesomelas. Mammalian Species 715:1–9.Google Scholar
Wang, Y., and Cerling, T. E. 1994. A model of fossil tooth and bone diagenesis: implications from paleodiet reconstruction from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology 107:281–289.Google Scholar
Webb, S. D. 1974. Pleistocene mammals of Florida. University Presses of Florida, Gainesville.Google Scholar
Webb, S. D. 1976. Mammalian faunal dynamics of the great American interchange. Paleobiology 2:220–234.Google Scholar
Webb, S. D. 2006. The Great American Biotic Interchange: patterns and processes. Annals of the Missouri Botanical Garden 93:245–257.Google Scholar
Webb, S. D., Morgan, G. S., Hulbert, R. C. Jr., Jones, D. S., MacFadden, B. J., and Mueller, P. A. 1989. Geochronology of a rich early Pleistocene vertebrate fauna, Leisey Shell Pit, Tampa Bay, Florida. Quaternary Research 32:96–110.Google Scholar
Werdelin, L. 1996. Carnivoran ecomorphology: a phylogenetic perspective. Pp. 582–624inGittleman, J. L., ed. Carnivore behavior, ecology, and evolution, Vol. 2. Cornell University Press, Ithaca, N.Y.Google Scholar