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

  • D. Rex Mitchell (a1) and Stephen Wroe (a1)

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.

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

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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.
Arman, S. D., and Prideaux, G. J.. 2015. Dietary classification of extant kangaroos and their relatives (Marsupialia: Macropodoidea). Austral Ecology 40:909922.
Barnes, R. F. W. 1982. Elephant feeding behaviour in Ruaha National Park, Tanzania. African Journal of Ecology 20:123136.
Belovsky, G. E. 1997. Optimal foraging and community structure: the allometry of herbivore food selection and competition. Evolutionary Ecology 11:641672.
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.
Bodmer, R. E. 1990. Ungulate frugivores and the browser-grazer continuum. Oikos 57:319325.
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.
Carraway, L. N., and Verts, B. J.. 1993. Aplodontia rufa. Mammalian Species 431:110.
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.
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.
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.
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.
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.
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.
Evans, M. C., Macgregor, C., and Jarman, P. J.. 2006. Diet and feeding selectivity of common wombats. Wildlife Research 33:321330.
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.
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.
Fritz, H., Duncan, P., Gordon, I. J., and Illius, A. W.. 2002. Megaherbivores influence trophic guilds structure in African ungulate communities. Oecologia 131:620625.
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.
Greaves, W. S. 2012. The mammalian jaw: a mechanical analysis. Cambridge University Press, Cambridge.
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.
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.
Herring, S. W., and Herring, S. E.. 1974. The superficial masseter and gape in mammals. American Naturalist 108:561576.
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.
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.
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.
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.
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.
Jerison, H., and Barlow, H.. 1985. Animal intelligence as encephalization [and discussion]. Philosophical Transactions of the Royal Society of London B 308:2135.
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.
Klingenberg, C. P. 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24:15–14.
Klingenberg, C. P., Barluenga, M., and Meyer, A.. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:19091920.
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.
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.
Maddison, W. P., and Maddison, D. R.. 2007. Mesquite: a modular system for evolutionary analysis, Version 3.31. http://mesquiteproject.org, accessed December 2016.
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.
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.
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.
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.
Murray, J. 2011. Wombats. ABDO, Edina, Minn.
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.
Myers, T. J. 2001. Prediction of marsupial body mass. Australian Journal of Zoology 49:99118.
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.
Owen-Smith, N. 1987. Pleistocene extinctions: the pivotal role of megaherbivores. Paleobiology 13:351–62.
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.
Prideaux, G. 2004. Systematics and evolution of the sthenurine kangaroos. Geological Sciences, Vol. 146. University of California Press, Oakland, Calif.
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.
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.
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.
Richardson, K. 2012. Australia's amazing kangaroos: their conservation, unique biology and coexistence with humans. CSIRO Publishing, Collingwood, Australia.
Rohlf, F. J., and Slice, D.. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39:4059.
Samuels, J. X., and Van Valkenburgh, B.. 2009. Craniodental adaptations for digging in extinct burrowing beavers. Journal of Vertebrate Paleontology 29:254268.
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.
Sharp, A. C. 2015. Comparative finite element analysis of the cranial performance of four herbivorous marsupials. Journal of Morphology 276:12301243.
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.
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.
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.
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.
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.
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.
Therrien, F. 2005. Feeding behaviour and bite force of sabretoothed predators. Zoological Jounal of the Linnean Society 145:393426.
Vincent, J. F. 1982. The mechanical design of grass. Journal of Materials Science 17:856860.
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.
Warburton, N. M. 2009. Comparative jaw muscle anatomy in kangaroos, wallabies, and rat-kangaroos (Marsupialia: Macropodoidea). Anatomical Record 292:875884.
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.
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.
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.
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.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., and Fink, W. L.. 2004. Geometric morphometrics for biologists: a primer. Elsevier, San Diego, Calif.

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

  • D. Rex Mitchell (a1) and Stephen Wroe (a1)

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