Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T00:29:59.444Z Has data issue: false hasContentIssue false
  • English
  • Français

Shell geometry and habitat determination in extinct and extant turtles (Reptilia: Testudinata)

Published online by Cambridge University Press:  08 April 2016

Roger B. J. Benson ,
Gábor Domokos ,
Péter L. Várkonyi  and
Robert R. Reisz
Roger B. J. Benson
Affiliation:
Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, United Kingdom. E-mail: rbb27@cam.ac.uk
Gábor Domokos
Affiliation:
Department of Mechanics, Materials and Structures, Budapest University of Technology and Economics, H-1111 Budapest, Mùgyetem rkp 3, K242, Hungary
Péter L. Várkonyi
Affiliation:
Department of Mechanics, Materials and Structures, Budapest University of Technology and Economics, H-1111 Budapest, Mùgyetem rkp 3, K242, Hungary
Robert R. Reisz
Affiliation:
Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road, Mississauga, Ontario L5L 1C6, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

A variety of means, including forelimb proportions and shell bone histology have been used to infer the paleoecology of extinct turtles. However, the height-to-width ratio of the shell (as a one-parameter shell model) has been dismissed because of its unreliability, and more complex aspects of shell geometry have generally been overlooked. Here we use a more reliable, three-parameter geometric model of the shell outline in anterior view as a means to assess turtle paleoecology. The accuracy of predictions of extant turtle ecology based on our three-parameter shell model is comparable to that derived from forelimb proportions when distinguishing between three ecological classes (terrestrial, semiaquatic, and aquatic). Higher accuracy is obtained when distinguishing between two classes (terrestrial and non-terrestrial), because the contours of aquatic and semiaquatic turtles are often very similar. Our model classifies Proterochersis robusta, a stem turtle from the Late Triassic of Germany, as non-terrestrial, and likely semiaquatic. Our method, combined with inferences based on limb proportions, indicates a diverse range of ecotypes represented by Late Triassic stem turtles. This implies that the ecological diversification of stem-group turtles may have been rapid, or that a substantial period of currently cryptic diversification preceded the first fossil appearance of the turtle stem lineage during the Late Triassic.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 4 , Fall 2011 , pp. 547 - 562
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

Anquetin, J., Barrett, P. M., Jones, M. E. H., Moore-Fay, S., and Evans, S. E. 2009. A new stem turtle from the Middle Jurassic of Scotland: new insights into the evolution and palaeoecology of basal turtles. Proceedings of the Royal Society of London B 276:879–886.Google Scholar
Arcucci, A. B., Marsicano, C. A., and Caselli, A. T. 2004. Tetrapod association and palaeoenvironment of the Los Colorados Formation (Argentina): a significant sample from Western Gondwana at the end of the Triassic. Geobios 37:557–568.Google Scholar
Aresco, M. J., and Dobie, J. L. 2000. Variation in shell arching and sexual size dimorphism of river cooters, Pseudemys concinna, from two river systems in Alabama. Journal of Herpetology 34:313–317.Google Scholar
Bennett, D. H., Gibbons, J. W., and Franson, J. C. 1970. Terrestrial activity in aquatic turtles. Ecology 51:738–740.Google Scholar
Bonin, F., Devaux, B., and Dupré, A. 2006. Turtles of the world. A and C Publishers, London.CrossRefGoogle Scholar
Bonnett, X., Lagarde, F., Henen, B. T., Corbin, J., Nagy, K. A., Naulleau, G., Balhoul, K., Chastel, O., Legrand, A., and Cambag, R. 2001. Sexual dimorphism in steppe tortoises (Testudo horsfieldii): influence of the environment and sexual selection on body shape and mobility. Biological Journal of the Linnean Society 72:357–372.Google Scholar
Buhlman, K. A., Congdon, J. D., Gibbons, J. W., and Greene, J. L. 2009. Ecology of chicken turtles (Deirochelys reticularia) in a seasonal wetland ecosystem: exploiting resource and refuge environments. Herpetologica 65:39–53.Google Scholar
Christiansen, J. L., Cooper, J. A., Bickham, J. W., Gallaway, B. J., and Springer, M. D. 1985. Aspects of the natural history of the yellow mud turtle Kinosternon flavescens (Kinosternidae) in Iowa: a proposed endangered species. Southwestern Naturalist 30:413–425.Google Scholar
Claude, J., Paradis, E., Tong, H., and Auffray, J.-C. 2003. A geometric morphometric assessment of the effects of environment and cladogenesis on the evolution of the turtle shell. Biological Journal of the Linnean Society 79:485–501.Google Scholar
Degenhardt, W. G., and Christiansen, J. L. 1974. Distribution and habitats of turtles in New Mexico. Southwestern Naturalist 19:21–46.Google Scholar
Domokos, G., and Várkonyi, P. L. 2008. Geometry and self-righting of turtles. Proceedings of the Royal Society of London B 275:11–17.Google Scholar
Deutsche Stratigraphische Kommission, ed. 2005. Stratigraphie von Deutschland. IV. Keuper. Courier Forschungsinstitut Senckenberg 253:1–296.Google Scholar
Ernst, C. H. 1986. Ecology of the turtle Sternotherus odoratus, in Southern Pennsylvania. Journal of Herpetology 20:341–352.Google Scholar
Ernst, C. H., and Barbour, R. W. 1989. Turtles of the world. Smithsonian Institution Press, Washington D.C.Google Scholar
Fraas, E. 1913. Proterochersis, eine pleurodire Schildkröte aus dem Keuper. Jahreshefte des Vereins für Vaterländische Naturkunde in Württemberg 80:1–30.Google Scholar
Gaffney, E. S. 1990. The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the American Museum of Natural History 194:1–163.Google Scholar
Gibbons, J. W. 1970. Terrestrial activity and the population dynamics of aquatic turtles. American Midland Naturalist 83:404–414.CrossRefGoogle Scholar
Gibbons, J. W., Greene, J. L., and Congdon, J. D. 1983. Drought-related responses of aquatic turtle populations. Journal of Herpetology 17:242–246.Google Scholar
Goode, J. 1967. Freshwater tortoises of Australia and New Guinea. Lansdowne Press, Melbourne, Australia.Google Scholar
Hill, R. V. 2005. Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. Systematic Biology 54:530–547.Google Scholar
Iverson, J. B. 1990. Nesting and parental care in the mud turtle, Kinosternon flavescens. Canadian Journal of Zoology 68:230–233.Google Scholar
Jolicoeur, P., and Mosimann, J. E. 1960. Size and shape variation in the painted turtles: a principal component analysis. Growth 24:339–354.Google Scholar
Joyce, W. G. 2007. Phylogenetic relationships of Mesozoic turtles. Bulletin of the Peabody Museum of Natural History 48:3–102.Google Scholar
Joyce, W. G., and Gauthier, J. A. 2004. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proceedings of the Royal Society of London B 271:1–5.CrossRefGoogle ScholarPubMed
Joyce, W. G., Parham, J. F., and Gauthier, J. A. 2004. Developing a protocol for the conservation of rank-based taxon names to phylogenetically defined names, as exemplified by turtles. Journal of Paleontology 78:989–1013.Google Scholar
Joyce, W. G., Lucas, S. G., Scheyer, T. M., Heckert, A. B., and Hunt, A. P. 2009. A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell. Proceedings of the Royal Society of London B 276:507–513.Google Scholar
Kennett, R., Christian, K., and Pritchard, D. 1993. Underwater nesting by the tropical freshwater turtle, Chelodina rugosa (Testudinata: Chelidae). Australian Journal of Zoology 41:47–52.Google Scholar
Krenz, J. G., Naylor, G. J. P., Shaffer, H. B., and Janzen, F. J. 2005. Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution 37:178–191.Google Scholar
Lee, M. S. Y. 1994. The turtle's long-lost relatives. Natural History 103:63–65.Google Scholar
Lee, M. S. Y. 2001. Molecules, morphology, and the monophyly of diapsid reptiles. Contributions to Zoology 70:121–138.Google Scholar
Li, C., Wu, X.-C., Rieppel, O., Wang, L.-T., and Zhao, L.-J. 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497–501.Google Scholar
Ligon, D. B., and Stone, P. A. 2003. Radiotelemetry reveals terrestrial estivation in Sonoran mud turtles (Kinosternon sonoriense). Journal of Herpetology 37:750–754.Google Scholar
Lyson, T. R., Bever, G. S., Bhullar, B.-A. S., Joyce, W. G., and Gauthier, J. A. 2011. Transitional fossils and the origin of turtles. Biology Letters. doi: 10.1098/rsbl.2010.0371.Google Scholar
Mahmoud, I. Y. 1969. Ecology of the kinosternid turtles of Oklahoma. Southwestern Naturalist 14:31–66.Google Scholar
Mann, G. K. H., O'Riain, M. J. O., and Hofmeyr, M. D. 2006. Shaping up to fight: sexual selection influences body shape and size in the fighting tortoise (Chersina angulata). Journal of Zoology 269:373–379.Google Scholar
Morales-Verdeja, S. A., and Vogt, R. C. 1997. Terrestrial movements in relation to aestivation and the annual reproductive cycle of Kinosternon leucostomum. Copeia 1997:123–130.Google Scholar
Parham, J. F., Feldman, C. R., and Boore, J. L. 2006. The complete mitochondrial genome of the enigmatic bigheaded turtle (Platysternon): description of unusual genomic features and the reconciliation of phylogenetic hypotheses based on mitochondrial and nuclear DNA. BMC Evolutionary Biology 6:11. doi:10.1186/1471-2148-6-11.CrossRefGoogle ScholarPubMed
Parker, W. S. 1984. Immigration and dispersal of slider turtles, Pseudemys scripta, in Mississippi farm ponds. American Midland Naturalist 112:280–293.Google Scholar
R Development Core Team. 2009. A language and environment for statistical computing. http://www.R-project.org.Google Scholar
Reisz, R. R., and Head, J. J. 2008. Turtle origins out to sea. Nature 456:450–451.Google Scholar
Rieppel, O., and Reisz, R. R. 1999. The origin and early evolution of turtles. Annual Review of Ecology, Evolution, and Systematics 30:1–22.Google Scholar
Rivera, G., and Claude, J. 2008. Environmental media and shape asymmetry: a case study on turtle shells. Biological Journal of the Linnean Society 94:483–489.Google Scholar
Rivera, G., Rivera, A. R. V., Dougherty, E. E., and Blob, R. W. 2006. Aquatic turning performance of painted turtles (Chrysemys picta) and functional consequences of a rigid body design. Journal of Experimental Biology 209:4203–4213.Google Scholar
Romer, A. S. 1967. The vertebrate story. University of Chicago, Chicago.Google Scholar
Rougier, G. W., de la Fuente, M. S., and Arcucci, A. B. 1995. Late Triassic turtles from South America. Science 268:855–858.Google Scholar
Scheyer, T. M., and Sander, P. M. 2007. Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proceedings of the Royal Society of London B 274:1885–1893.Google Scholar
Seidel, M. E. 1978. Terrestrial dormancy in the turtle Kinosternon flavescens: respiratory metabolism and dehydration. Comparative Biochemistry and Physiology A 61:1–4.Google Scholar
Spinks, P. Q., Shaffer, H. B., Iverson, J. B., and McCord, W. P. 2004. Phylogenetic hypotheses for the turtle family Geoemydidae. Molecular Phylogenetics and Evolution 32:164–182.Google Scholar
Spinks, P. Q., Thomson, R. C., Lovely, G. A., and Shaffer, H. B. 2009. Assessing what is needed to resolve a molecular phylogeny: simulations and empirical data from emydid turtles. BMC Evolutionary Biology 9:5.Google Scholar
Stephens, P. R., and Wiens, J. J. 2003. Ecological diversification and phylogeny of emydid turtles. Biological Journal of the Linnean Society 79:577–610.Google Scholar
Sterli, J., de la Fuente, M. S., Guillermo, S. R., and Rougier, W. 2007. Anatomy and relationships of Palaeochersis talampayensis, a Late Triassic turtle from Argentina. Palaeontographica, Abteilung A 281:1–61.Google Scholar
Sues, H.-D., and Fraser, N. C. 2010. Triassic life on land: the great transition. Columbia University Press, New York.Google Scholar
Teska, W. R. 1976. Terrestrial movements of the mud turtle Kinosternon scorpioides in Costa Rica. Copeia 1976:579–580.CrossRefGoogle Scholar
Turtle Taxonomy Working Group. 2007. An annotated list of modern turtle terminal taxa (with comments on areas of instability and recent change). Chelonian Conservation Biology Research Monographs 4:173–199.Google Scholar
Vogt, R. C., and Guzman, S. 1988. Food partitioning in a neotropical freshwater turtle community. Copeia 1988:37–47.Google Scholar
Willemsen, R. E., and Hailey, A. 2003. Sexual dimorphism of body size and shell shape in European tortoises. Journal of Zoology 260:353–365.Google Scholar
Zardoya, R., and Meyer, A. 2001. The evolutionary position of turtles revised. Naturwissenschaften 88:193–200.Google Scholar
Zug, G. R. 1970. Buoyancy, locomotion, morphology of the pelvic girdle and hindlimbs, and the systematics of cryptodiran turtles. Miscellaneous Publications of the Museum of Zoology, University of Michigan 142:1–98.Google Scholar