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Evidence of frugivory and seed dispersal in Oligocene tortoises from South Dakota

Published online by Cambridge University Press:  04 July 2013

ALAN O. MARRON  and
JASON R. MOORE
ALAN O. MARRON*
Affiliation:
Department for Applied Mathematics and Theoretical Physics, University of Cambridge Centre for Mathematical Sciences, Wilberforce Road, Cambridge CB3 0WA, UK Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
JASON R. MOORE
Affiliation:
Department of Earth Sciences, Dartmouth College, HB 6105, Fairchild Hall, Hanover, NH 03755, USA
*
†Author for correspondence: am543@cam.ac.uk
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Abstract

Fossilized hackberry (Celtis) seeds were found within the shells of two Stylemys individuals excavated from Oligocene sediments from South Dakota. The presence of in situ skeletal elements indicates that the tortoises were buried without extensive disarticulation. Abiotic transport of the seeds into the carcasses is unlikely given the anatomically correct placement of both skeletal elements and seeds and the comparative settling velocities of the encasing sediment versus modern Celtis seeds. Ecological evidence from modern Celtis and Stylemys analogues suggests that tortoises are commonly seed dispersal agents. The fossils are therefore interpreted as enterolites, providing the oldest reliable evidence of tortoise frugivory.

Keywords

endozoochoryhackberrysaurochoryStylemysWhite River Group
Type
Rapid Communication
Information
Geological Magazine , Volume 150 , Issue 6 , November 2013 , pp. 1143 - 1149
Copyright
Copyright © Cambridge University Press 2013 

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References

Barrett, P. M. & Willis, K. J. 2001. Did dinosaurs invent flowers? Dinosaur–angiosperm coevolution revisited. Biological Reviews of the Cambridge Philosophical Society 76 (3), 411–47.Google Scholar
Benton, R. C., Evanoff, E. E., Herbel, C. L. & Terry, D. O. 2001. Baseline mapping of fossil bone beds at Badlands National Park. In 6th Annual Fossil Resources Conference, pp. 85–94. National Park Service, Lakewood, CO.Google Scholar
Birkhead, R. D., Guyer, C., Hermann, S. M. & Michener, W. K. 2005. Patterns of folivory and seed ingestion by gopher tortoises (Gopherus polyphemus) in a southeastern pine savanna. American Midland Naturalist 154 (1), 143–51.Google Scholar
Blob, R. W. 1997. Relative hydrodynamic dispersal potentials of soft-shelled turtle elements: implications for interpreting skeletal sorting in assemblages of non-mammalian terrestrial vertebrates. Palaios 12 (2), 151–64.CrossRefGoogle Scholar
Brand, L. R., Hussey, M. & Taylor, J. 2004. Taphonomy of freshwater turtles: decay and disarticulation in controlled experiments. Journal of Taphonomy 1 (4), 233–45.Google Scholar
Clark, J., Beerbower, J. R. & Kietzke, K. K. 1967. Oligocene stratigraphy, sedimentology, paleoecology and paleoclimatology in the Big Badlands of South Dakota. Fieldiana: Geology Memoirs 5, 1–157.Google Scholar
Cobo, M. & Andreu, A. C. 1988. Seed consumption and dispersal by the spur-thighed tortoise Testudo graeca . Oikos 51 (3), 267–73.Google Scholar
Corsini, J., Smith, T. & Leite, M. 2006. Paleoenvironmental implications of size, carapace position, and incidence of non-shell elements in White River turtles. Palaeogeography, Palaeoclimatology, Palaeoecology 234 (2–4), 287–303.Google Scholar
Demir, F., Doğan, H., Özcan, M. & Haciseferoğullari, H. 2002. Nutritional and physical properties of hackberry (Celtis australis L.). Journal of Food Engineering 54 (3), 241–7.Google Scholar
Dewar, E. W. 2008. Dietary ecology and community paleoecology of early tertiary mammals. Published PhD thesis. Organismic and Evolutionary Biology, University of Massachusetts, Amherst, USA.Google Scholar
Eriksson, O., Friis, E. & Löfgren, P. 2000. Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. The American Naturalist 156 (1), 47–58.Google Scholar
Evanoff, E. E., Terry, D. O., Benton, R. C. & Minkler, H. 2010. Field guide to the geology of the White River Group in the north unit of Badlands National Park. In 62nd Annual Meeting of the Geological Society of America: Rocky Mountain Section, pp. 1–32. Geological Society of America, Boulder, CO.Google Scholar
Gradstein, F. M., Ogg, J. G., Schmitz, M. & Ogg, G. 2012. The Geologic Timescale 2012. Elsevier Science Ltd, Boston, MA.Google Scholar
Hansen, D. M., Donlan, C. J., Griffiths, C. J. & Campbell, K. J. 2010. Ecological history and latent conservation potential: large and giant tortoises as a model for taxon substitutions. Ecography 33, 272–84.Google Scholar
Hardesty, B. D., Hubbell, S. P. & Bermingham, E. 2006. Genetic evidence of frequent long-distance recruitment in a vertebrate-dispersed tree. Ecology Letters 9 (5), 516–25.Google Scholar
Hay, O. P. 1908. The Fossil Turtles of North America. Carneige Institute of Washington, Washington, DC.Google Scholar
Heywood, H. 1962. Uniform and non-uniform motion of particles in fluids. In Proceedings of the Symposium on Interactions Between Fluids and Particles, pp. 1–8, London Institute of Chemical Engineers, London.Google Scholar
Hnatiuk, S. H. 1978. Plant dispersal by the Aldabran giant tortoise Geochelone gigantea (Schweigger). Oecologia 36 (3), 345–50.Google Scholar
Hutchison, J. H. 1992. Western North American reptile and amphibian record across the Eocene/Oligocene boundary, and its climatic implications. In Eocene/Oligocene Climatic and Biotic Evolution (Prothero, D. R. & Berggren, W. A. eds), pp. 451–63. Princeton University Press, New York.Google Scholar
Jahren, A. H., Gabel, M. L. & Amundson, R. 1998. Biomineralization in seeds: developmental trends in isotopic signatures of hackberry. Palaeogeography, Palaeoclimatology, Palaeoecology 138, 259–69.Google Scholar
Jerozolimski, A., Ribeiro, M. B. N. & Martins, M. 2009. Are tortoises important seed dispersers in Amazonian forests? Oecologia 161 (3), 517–28.Google Scholar
Kear, B. P. 2006. First gut contents in a Cretaceous sea turtle. Biology Letters 2 (1), 113–15.Google Scholar
Marlow, R. W. 1989. Co-evolution of a Galapagos Tortoise-Psidium Interaction. American Zoologist 29 (4), 145A.Google Scholar
McArthur, S., Meyer, J., Innis, C. & Wilkinson, R. 2008. Anatomy and physiology. In Medicine and Surgery of Tortoises and Turtles (eds S. McArthur, R. Wilkinson & J. Meyer), pp. 35–72. Blackwell Publishing Ltd., Oxford.Google Scholar
Mihlbachler, M. C., Rivals, F., Solounias, N. & Semprebon, G. M. 2011. Dietary change and evolution of horses in North America. Science 331 (6021), 1178–81.Google Scholar
Milton, S. J. 1992. Plants eaten and dispersed by adult Leopard Tortoises (Geochelone pardalis) in the Southern Karoo. South African Journal of Zoology 27 (2), 45–9.Google Scholar
Moll, D. & Jansen, K. P. 1995. Evidence for a role in seed dispersal by two tropical herbivorous turtles. Biotropica 27 (1), 121–7.Google Scholar
Moore, J. R. & Norman, D. B. 2009. Quantitatively evaluating the sources of taphonomic biasing of skeletal element abundances in fossil assemblages. Palaios 24, 591–602.Google Scholar
Prasad, V., Strömberg, C. A. E., Alimohammadian, H. & Sahni, A. 2005. Dinosaur coprolites and the early evolution of grasses and grazers. Science 310, 1177–80.Google Scholar
Prothero, D. R. & Whittlesey, K. E. 1998. Magnetic stratigraphy and biostratigraphy of the Orellan and Whitneyan land-mammal ages in the White River Group. Geological Society of America Special Papers 325, 39–61.Google Scholar
Retallack, G. J. 1983. A paleopedological approach to the interpretation of terrestrial sedimentary rocks: the mid-Tertiary fossil soils of Badlands National Park, South Dakota. Geological Society of America Bulletin 94 (7), 823–40.Google Scholar
Reynoso, V.-H. & Montellano-Ballesteros, M. 2004. A new giant turtle of the genus Gopherus (Chelonia: Testudinidae) from the Pleistocene of Tamaulipas, México, and a review of the phylogeny and biogeography of gopher tortoises. Journal of Vertebrate Paleontology 24 (4), 822–37.Google Scholar
Rodríguez-de la Rosa, R. A., Cevallos-Ferriz, S. R. S. & Silva-Pineda, A. 1998. Paleobiological implications of Campanian coprolites. Palaeogeography, Palaeoclimatology, Palaeoecology 142 (3–4), 231–54.Google Scholar
Semprebon, G., Janis, C. & Solounias, N. 2004. The diets of the dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change. Journal of Vertebrate Paleontology 24 (2), 427–44.Google Scholar
Shillito, L.-M. & Almond, M. J. 2010. Comment on: fruit and seed biomineralization and its effect on preservation by E. Messager et al. Archaeological and Anthropological Sciences 2, 25–34.Google Scholar
Solounias, N. & Semprebon, G. 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. American Museum Novitates 3366, 1–49.Google Scholar
Strong, J. N. & Fragoso, J. M. V. 2006. Seed dispersal by Geochelone carbonaria and Geochelone denticulata in northwestern Brazil. Biotropica 38 (5), 683–6.CrossRefGoogle Scholar
Tiffney, B. H. 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics 35 (1), 1–29.Google Scholar
Traveset, A. 1998. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1 (2), 151–90.Google Scholar
Valido, A. & Olesen, J. M. 2007. The importance of lizards. In Seed Dispersal: Theory and its Applications in a Changing World (ed. J. Dennis), pp. 124–47. CABI Publishing, Wallingford, UK.Google Scholar
Varela, R. O. & Bucher, E. H. 2002. Seed dispersal by Chelonoidis chilensis in the Chaco Dry Woodland of Argentina. Journal of Herpetology 36 (1), 137–40.Google Scholar
Wall, W. P. & Maddox, D. 1998. Reassessment of characteristics determining generic affinity in Gopherus and Stylemys (Testudinidae) from the White River Group, Badlands National Park. In Badlands National Park Service Paleontological Research Technical Report NPS/NRGRD/GRDTR-98/1 (Santucci, V. L. & McClelland, L. eds), pp. 8–12. National Park Service, Fort Collins, CO.Google Scholar
Wang, Y., Jahren, A. H. & Amundson, R. 1997. Potential for 14C dating of biogenic carbonate in hackberry (Celtis) endocarps. Quaternary Research 343 (47), 337–43.Google Scholar
Wenny, D. G. 2001. Advantages of seed dispersal: a re-evaluation of directed dispersal. Evolutionary Ecology Research 3, 51–74.Google Scholar
Wilson, G. P., Evans, A. R., Corfe, I. J., Smits, P. D., Fortelius, M. & Jernvall, J. 2012. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483 (7390), 457–60.Google Scholar
Zheng, X., Martin, L. D., Zhou, Z., Burnham, D. A, Zhang, F. & Miao, D. 2011. Fossil evidence of avian crops from the Early Cretaceous of China. Proceedings of the National Academy of Sciences of the USA 108 (38), 15904–7.Google Scholar
Zhu, M. Y., Vannier, J., van Iten, H. & Zhao, Y. L. 2004. Direct evidence for predation on trilobites in the Cambrian. Proceedings of the Royal Society B: Biological Sciences 271 (Suppl 5), S277–80.Google Scholar
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