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Biting mechanics determines craniofacial morphology among extant diprotodont herbivores: dietary predictions for the giant extinct short-faced kangaroo, Simosthenurus occidentalis

Published online by Cambridge University Press:  14 January 2019

D. Rex Mitchell
Affiliation:
Zoology Division, School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2351, Australia. E-mail: [email protected], [email protected]
Stephen Wroe
Affiliation:
Zoology Division, School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2351, Australia. E-mail: [email protected], [email protected]

Abstract

Large herbivores can act as keystone species that strongly influence their communities. During the Pliocene and Pleistocene, Australia was dominated by a number of large to gigantic marsupial herbivore taxa. Many of these have been understudied quantitatively with regard to their ecology; and identifying the diet of these species will improve our understanding of not only their ecologies, but also of past environments. Recent research has found that cranial morphology among kangaroos and wallabies corresponds with foraging behaviors and mechanical properties of preferred plant tissues. Here we apply shape analysis and computational biomechanics to test the hypothesis: that feeding ecology is associated with craniofacial morphology across a taxonomically broad sample of diprotodont herbivores. Based on our results we predict the diet of an extinct short-faced kangaroo, Simosthenurus occidentalis. We find that biting behaviors are reflected in craniofacial morphology, but that these are more a reflection of the hardest bites required for their lifestyle, rather than diet composition alone. A combination of a very short face, robust musculoskeletal features, and dental arrangements predict that S. occidentalis was a browser, capable of consuming particularly resistant, bulky plant matter. These features were largely conserved among other short-faced kangaroos and may have offset the unpredictable availability of quality forage during the climatically variable Pleistocene epoch, contributing to their prolific diversification during this time.

Type
Articles
Copyright
Copyright © 2019 The Paleontological Society. All rights reserved 

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Footnotes

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.44sk691

References

Literature Cited

Adams, D. C., Collyer, M. L., Kaliontzopoulou, A., and Sherratt, E.. 2016. Geomorph: software for geometric morphometric analyses. R package, Version 3.0.5. https://cran.r-project.org/package=geomorph, accessed December 2016.Google Scholar
Arman, S. D., and Prideaux, G. J.. 2015. Dietary classification of extant kangaroos and their relatives (Marsupialia: Macropodoidea). Austral Ecology 40:909922.Google Scholar
Barnes, R. F. W. 1982. Elephant feeding behaviour in Ruaha National Park, Tanzania. African Journal of Ecology 20:123136.Google Scholar
Belovsky, G. E. 1997. Optimal foraging and community structure: the allometry of herbivore food selection and competition. Evolutionary Ecology 11:641672.Google Scholar
Black, K. H., Archer, M., Hand, S. J., and Godthelp, H.. 2012. The rise of Australian marsupials: a synopsis of biostratigraphic, phylogenetic, palaeoecologic and palaeobiogeographic understanding. Pp. 9831078 in Talent, J. A., ed. Earth and life. Springer, Dordrecht, Netherlands.Google Scholar
Bodmer, R. E. 1990. Ungulate frugivores and the browser-grazer continuum. Oikos 57:319325.Google Scholar
Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., Orme, C. D. L., and Purvis, A.. 2005. Multiple causes of high extinction risk in large mammal species. Science 309:12391241.Google Scholar
Carraway, L. N., and Verts, B. J.. 1993. Aplodontia rufa. Mammalian Species 431:110.Google Scholar
Clarkson, C., Jacobs, Z., Marwick, B., Fullagar, R., Wallis, L., Smith, M., Roberts, R. G., et al. 2017. Human occupation of northern Australia by 65,000 years ago. Nature 547:306.Google Scholar
Clauss, M., Kaiser, T., and Hummel, J. 2008. The morphophysiological adaptations of browsing and grazing mammals. Pp. 4748 in Gordon, I. J. and Prins, H. H. T., eds. The ecology of browsing and grazing. Springer, Heidelberg.Google Scholar
Clauss, M., Steuer, P., Müller, D. W., Codron, D., and Hummel, J.. 2013. Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS ONE 8:e68714.Google Scholar
Covey, D. S., and Greaves, W. S.. 1994. Jaw dimensions and torsion resistance during canine biting in the Carnivora. Canadian Journal of Zoology 72:10551060.Google Scholar
Crompton, A. W., Lieberman, D. E., Owerkowicz, T., Baudinette, R. V., and Skinner, J.. 2008. Motor control of masticatory movements in the Southern hairy-nosed wombat (Lasiorhinus latifrons). Pp. 83111 in Vinyad, C., Ravosa, M. J., and Wall, C., eds. Primate craniofacial function and biology. Springer, New York.Google Scholar
Crompton, A. W., Owerkowicz, T., and Skinner, J.. 2010. Masticatory motor pattern in the koala (Phascolarctos cinereus): a comparison of jaw movements in marsupial and placental herbivores. Journal of Experimental Zoology A 313:564578.Google Scholar
Evans, M. C., Macgregor, C., and Jarman, P. J.. 2006. Diet and feeding selectivity of common wombats. Wildlife Research 33:321330.Google Scholar
Figueirido, B., Tseng, Z. J., Serrano-Alarcón, F. J., Martín-Serra, A., and Pastor, J. F.. 2014. Three-dimensional computer simulations of feeding behaviour in red and giant pandas relate skull biomechanics with dietary niche partitioning. Biology Letters 10:20140196.Google Scholar
Fitton, L. C., Prôa, M., Rowland, C., Toro-Ibacache, V., and O'higgins, P.. 2015. The impact of simplifications on the performance of a finite element model of a Macaca fascicularis cranium. Anatomical Record 298:107121.Google Scholar
Fritz, H., Duncan, P., Gordon, I. J., and Illius, A. W.. 2002. Megaherbivores influence trophic guilds structure in African ungulate communities. Oecologia 131:620625.Google Scholar
Goswami, A., Milne, N., and Wroe, S.. 2011. Biting through constraints: cranial morphology, disparity and convergence across living and fossil carnivorous mammals. Proceedings of the Royal Society of London B 278:18311839.Google Scholar
Greaves, W. S. 2012. The mammalian jaw: a mechanical analysis. Cambridge University Press, Cambridge.Google Scholar
Grosse, I. R., Dumont, E. R., Coletta, C., and Tolleson, A.. 2007. Techniques for modeling muscle-induced forces in finite element models of skeletal structures. Anatomical Record 290:10691088.Google Scholar
Helgen, K. M., Wells, R. T., Kear, B. P., Gerdtz, W. R., and Flannery, T. F.. 2006. Ecological and evolutionary significance of sizes of giant extinct kangaroos. Australian Journal of Zoology 54:293303.Google Scholar
Herring, S. W., and Herring, S. E.. 1974. The superficial masseter and gape in mammals. American Naturalist 108:561576.Google Scholar
Illius, A. W., and Gordon, I. J.. 1992. Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia, 89:428434.Google Scholar
Janis, C. M. 1990. Correlation of cranial and dental variables with dietary preferences in mammals: a comparison of macropodoids and ungulates. Memoirs of the Queensland Museum 28:349366.Google Scholar
Janis, C. M. 1995. Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. Pp. 7698 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Janis, C. M. 2008. An evolutionary history of browsing and grazing ungulates. Pp. 2145 in Gordon, I. J. and Prins, H. H. T., eds. The ecology of browsing and grazing. Ecological Studies 195. Springer, Berlin.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
Jerison, H., and Barlow, H.. 1985. Animal intelligence as encephalization [and discussion]. Philosophical Transactions of the Royal Society of London B 308:2135.Google Scholar
Johnson, C. N., and Prideaux, G. J.. 2004. Extinctions of herbivorous mammals in the late Pleistocene of Australia in relation to their feeding ecology: no evidence for environmental change as cause of extinction. Austral Ecology 29:53557.Google Scholar
Klingenberg, C. P. 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24:15–14.Google Scholar
Klingenberg, C. P., Barluenga, M., and Meyer, A.. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:19091920.Google Scholar
Lambert, J. E., Chapman, C. A., Wrangham, R. W., and Conklin-Brittain, N. L.. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology 125:363368.Google Scholar
Llamas, B., Brotherton, P., Mitchell, K. J., Templeton, J. E., Thomson, V. A., Metcalf, J. L., Armstrong, K. N., et al. 2014. Late Pleistocene Australian marsupial DNA clarifies the affinities of extinct megafaunal kangaroos and wallabies. Molecular Biology and Evolution 32:574584.Google Scholar
Maddison, W. P., and Maddison, D. R.. 2007. Mesquite: a modular system for evolutionary analysis, Version 3.31. http://mesquiteproject.org, accessed December 2016.Google Scholar
McHenry, C. R., Wroe, S., Clausen, P. D., Moreno, K., and Cunningham, E.. 2007. Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation. Proceedings of the National Academy of Sciences USA 104:1601016015.Google Scholar
Mitchell, D. R., Sherratt, E., Ledogar, J. A., and Wroe, S.. 2018. The biomechanics of foraging determines face length among kangaroos and their relatives. Proceedings of the Royal Society of London B 285:20180845.Google Scholar
Mitchell, K. J., Pratt, R. C., Watson, L. N., Gibb, G. C., Llamas, B., Kasper, M., Edson, J., et al. 2014. Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Molecular Biology and Evolution, 31:23222330.Google Scholar
Moore, B. D., and Foley, W. J.. 2000. A review of feeding and diet selection in koalas (Phascolarctos cinereus). Australian Journal of Zoology 48: 317333.Google Scholar
Murray, J. 2011. Wombats. ABDO, Edina, Minn.Google Scholar
Murray, P. F. 1992. Thinheads, thickheads and airheads—functional craniology of some diprotodontian marsupials. The Beagle, Records of the Northern Territory Museum of Arts and Sciences 9:7188.Google Scholar
Myers, T. J. 2001. Prediction of marsupial body mass. Australian Journal of Zoology 49:99118.Google Scholar
Nalla, R. K., Kinney, J. H., and Ritchie, R. O.. 2003. Mechanistic fracture criteria for the failure of human cortical bone. Natural Materials 2:164168.Google Scholar
Owen-Smith, N. 1987. Pleistocene extinctions: the pivotal role of megaherbivores. Paleobiology 13:351–62.Google Scholar
Potter, S., Cooper, S. J., Metcalfe, C. J., Taggart, D. A., and Eldridge, M. D.. 2012. Phylogenetic relationships of rock-wallabies, Petrogale (Marsupialia: Macropodidae) and their biogeographic history within Australia. Molecular Phylogenetics and Evolution 62:640652.Google Scholar
Prideaux, G. 2004. Systematics and evolution of the sthenurine kangaroos. Geological Sciences, Vol. 146. University of California Press, Oakland, Calif.Google Scholar
Prideaux, G. J., and Warburton, N. M.. 2010. An osteology-based appraisal of the phylogeny and evolution of kangaroos and wallabies (Macropodidae: Marsupialia). Zoological Journal of the Linnean Society 159:954987.Google Scholar
Prideaux, G. J., Ayliffe, L. K., DeSantis, L. R., Schubert, B. W., Murray, P. F., Gagan, M. K., and Cerling, T. E.. 2009. Extinction implications of a chenopod browse diet for a giant Pleistocene kangaroo. Proceedings of the National Academy of Sciences USA 106:1164611650.Google Scholar
R Development Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.Google Scholar
Richardson, K. 2012. Australia's amazing kangaroos: their conservation, unique biology and coexistence with humans. CSIRO Publishing, Collingwood, Australia.Google Scholar
Rohlf, F. J., and Slice, D.. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39:4059.Google Scholar
Samuels, J. X., and Van Valkenburgh, B.. 2009. Craniodental adaptations for digging in extinct burrowing beavers. Journal of Vertebrate Paleontology 29:254268.Google Scholar
Sanson, G. D. 1989. Morphological adaptations of teeth to diets and feeding in the Macropodoidea. Pp. 151168 in Grigg, G., Jarman, P., and Hume, I., eds. Kangaroos, wallabies and rat-kangaroos. Surrey Beatty, Chipping Norton, NSW, Australia.Google Scholar
Sharp, A. C. 2015. Comparative finite element analysis of the cranial performance of four herbivorous marsupials. Journal of Morphology 276:12301243.Google Scholar
Shipley, L. A. 1999. Grazers and browsers: how digestive morphology affects diet selection. Pp. 2027 in Launchbaugh, K. L., Sanders, K. D., and Mosley, J. C., eds. Grazing behavior of livestock and wildlife. University of Idaho, Moscow.Google Scholar
Shockey, B. J., and Anaya, F.. 2011. Grazing in a new late Oligocene mylodontid sloth and a mylodontid radiation as a component of the Eocene–Oligocene faunal turnover and the early spread of grasslands/savannas in South America. Journal of Mammalian Evolution 18:101115.Google Scholar
Stein, B. R. 2000. Morphology of subterranean rodents. Pp. 1961 in Lacey, E. A., Patton, J. L., and Cameron, G. N., eds. Life underground: the biology of subterranean rodents. University of Chicago Press, Chicago.Google Scholar
Strait, D. S., Weber, G. W., Neubauer, S., Chalk, J., Richmond, B. G., Lucas, P. W., Spencer, M. A., et al. 2009. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proceedings of the National Academy of Sciences USA 106:21242129.Google Scholar
Strait, D. S., Grosse, I. R., Dechow, P. C., Smith, A. L., Wang, Q., Weber, G. W., Neubauer, S., et al. 2010. The structural rigidity of the cranium of Australopithecus africanus: implications for diet, dietary adaptations, and the allometry of feeding biomechanics. Anatomical Record 293:583593.Google Scholar
Stokke, S., and Toit, J. T.. 2000. Sex and size related differences in the dry season feeding patterns of elephants in Chobe National Park, Botswana. Ecography 23:7080.Google Scholar
Therrien, F. 2005. Feeding behaviour and bite force of sabretoothed predators. Zoological Jounal of the Linnean Society 145:393426.Google Scholar
Vincent, J. F. 1982. The mechanical design of grass. Journal of Materials Science 17:856860.Google Scholar
Walmsley, C. W., McCurry, M. R., Clausen, P. D., and McHenry, C. R.. 2013. Beware the black box: investigating the sensitivity of FEA simulations to modelling factors in comparative biomechanics. PeerJ 1:e204.Google Scholar
Warburton, N. M. 2009. Comparative jaw muscle anatomy in kangaroos, wallabies, and rat-kangaroos (Marsupialia: Macropodoidea). Anatomical Record 292:875884.Google Scholar
Wells, R. T., and Tedford, R. H.. 1995. Sthenurus (Macropodidae, Marsupialia) from the Pleistocene of Lake Callabonna, South Australia. Bulletin of the American Natural History Museum 225.Google Scholar
Wroe, S., Field, J. H., Archer, M., Grayson, D. K., Price, G. J., Louys, J., Faith, J. T., et al. 2013. Climate change frames debate over the extinction of megafauna in Sahul (Pleistocene Australia–New Guinea). Proceedings of the National Academy of Sciences USA 110:87778781.Google Scholar
Wroe, S., Parr, W. C. H., Ledogar, J. A., Bourke, J., Evans, S. P., Fiorenza, L., Benazzi, S., et al. 2018. Computer simulations show that Neanderthal facial morphology represents adaptation to cold and high energy demands, but not heavy biting. Proceedings of the Royal Society of London B 285:20180085.Google Scholar
Young, H. S., McCauley, D. J., Helgen, K. M., Goheen, J. R., Otárola-Castillo, E., Palmer, T. M., Pringle, R. M., et al. 2013. Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. Journal of Ecology 101:10301041.Google Scholar
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., and Fink, W. L.. 2004. Geometric morphometrics for biologists: a primer. Elsevier, San Diego, Calif.Google Scholar