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The evolution of the bone-cracking model in carnivorans: cranial functional morphology of the Plio-Pleistocene cursorial hyaenid Chasmaporthetes lunensis (Mammalia: Carnivora)

Published online by Cambridge University Press:  08 April 2016

Zhijie Jack Tseng ,
Mauricio Antón  and
Manuel J. Salesa
Zhijie Jack Tseng
Affiliation:
Integrative and Evolutionary Biology Program, Department of Biological Sciences, 3616 Trousdale Parkway, University of Southern California, Los Angeles, California 90089 Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007. E-mail: jack.tseng@usc.edu
Mauricio Antón
Affiliation:
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal, 2, 28006 Madrid, Spain
Manuel J. Salesa
Affiliation:
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal, 2, 28006 Madrid, Spain
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Abstract

Fossil species of the family Hyaenidae represent a wide range of ecomorphological diversity not observed in living representatives of this carnivoran group. Among them, the cursorial meat-and-bone specialists are of particular interest not only because they were the most cursorial of the hyaenids, but also because they were the only members of this family to spread into the New World. Here we conduct a functional morphological analysis of the cranium of the cursorial meat-and-bone specialist Chasmaporthetes lunensis by using finite element modeling to compare it with the living Crocuta crocuta, a well-known bone-cracking carnivoran. As found with previous finite element studies on hyaenid crania, the cranium of C. lunensis is not differentially adapted for stress dissipation between the bone-cracking and meat-shearing teeth. A smaller occlusal surface on the more slender P3 cusp of C. lunensis allowed this species to use less bite force to crack a comparably-sized bone relative to C. crocuta, but higher muscle masses in the latter probably allow it to process larger food items. We use two indices, the stress slope and the bone-cracking index, to show that C. lunensis has a well-adapted cranium for stress dissipation given its size, but the main stresses placed on its cranium might have been more from subduing prey and less from cracking bones. Throughout the Cenozoic, other carnivores besides hyaenids convergently evolved similar morphologies, including domed frontal regions, suggesting an adaptive value for a repetitive mosaic of features. Our analyses add support to the hypothesis that bone-cracking adaptations are a complex model that has evolved convergently several times across different carnivoran families, and these predictable morphologies may evolve along a common gradient of functionality that is likely to be under strong adaptive control.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 1 , Winter 2011 , pp. 140 - 156
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Antón, M., Turner, A., Salesa, M. J., and Morales, J. 2006. A complete skull of Chasmaporthetes lunensis (Carnivora, Hyaenidae) from the Spanish Pliocene site of La Puebla de Valverde (Teruel). Estudios Geológicos 62(1):375–388.CrossRefGoogle Scholar
Ashby, M. F., Gibson, L. J., Wegst, U., and Olive, R. 1995. The mechanical properties of natural materials. I. Material property charts. Proceedings of the Royal Society of London A 450:123–140.Google Scholar
Ashman, R. B., Rosinia, G., Cowin, S. C., and Fontenot, M. G. 1985. The bone tissue of the canine mandible is elastically isotropic. Journal of Biomechanics 18:717–721.Google Scholar
Bazant, Z. P., and Li, Z. 1995. Modulus of rupture: size effect due to fracture initiation in boundary layer. Journal of Structural Engineering 121:739–746.CrossRefGoogle Scholar
Berta, A. 1981. The Plio-Pleistocene hyaena Chasmaporthetes ossifragus from Florida. Journal of Vertebrate Paleontology 1:341–356.Google Scholar
Biknevicius, A. R., and Ruff, C. B. 1992. The structure of the mandibular corpus and its relationship to feeding behaviors in extant carnivorans. Journal of Zoology 228:479–507.CrossRefGoogle Scholar
Binder, W. J., and Van Valkenburgh, B. 2000. Development of bite strength and feeding behaviour in juvenile spotted hyenas (Crocuta crocuta). Journal of the Zoological Society of London 252:273–283.CrossRefGoogle Scholar
Cowin, S. C. 1989. Bone mechanics. CRC Press, Boca Raton, Fla. Google Scholar
Dessem, D. 1989. Interactions between jaw-muscle recruitment and jaw-joint forces in Canis familiaris . Journal of Anatomy 164:101–121.Google ScholarPubMed
Dumont, E.R., Piccirillo, J., and Grosse, I.R. 2005. Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. Anatomical Record Part A 283A:319–330.CrossRefGoogle Scholar
Erickson, G. M., Catanese, J. III, and Keaveny, T. M. 2002. Evolution of the biomechanical material properties of the femur. Anatomical Record 268:115–124.CrossRefGoogle ScholarPubMed
Ewer, R. F. 1973. The carnivores. Cornell University Press, Ithaca, N.Y. Google Scholar
Ferretti, M. P. 1999. Tooth enamel structure in the hyaenid Chasmaporthetes lunensis lunensis from the Late Pliocene of Italy, with implications for feeding behavior. Journal of Vertebrate Paleontology 19:767–770.CrossRefGoogle Scholar
Ferretti, M. P. 2007. Evolution of bone-cracking adaptations in hyaenids (Mammalia, Carnivora). Swiss Journal of Geoscience 100:41–52.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 290:1069–1088.Google Scholar
Hay, O. P. 1921. Descriptions of species of Pleistocene Vertebrata, types or specimens most of which are preserved in the United States National Museum. Proceedings of the United States National Museum 59:599–642.CrossRefGoogle Scholar
Khomenko, I. P. 1932. Hyaena borissiaki n. sp. iz russil'onskoj fauny Bessarabii. Travaux de l'Institut Paléozoologique de l'Academie des Sciences de l'U.R.S.S. 1:81–134.Google Scholar
Kruuk, H. 1972. The spotted hyena: a study of predation and social behavior. University of Chicago Press, Chicago.Google Scholar
Kurtén, B., and Werdelin, L. 1988. A review of the genus Chasmaporthetes Hay, 1921 (Carnivora, Hyaenidae). Journal of Vertebrate Paleontology 8(1):46–66.CrossRefGoogle Scholar
Lauder, G. V. 1995. On the inference of function from structure. Pp. 1–18 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Lucas, P. W., Prinz, J. F., Agrawal, K. R., and Bruce, I. C. 2002. Food physics and oral physiology. Food Quality and Preference 13:203–213.Google Scholar
McHenry, C., 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 104:16010–16015.CrossRefGoogle ScholarPubMed
Nowak, R. M. 1999. Walker's carnivores of the world. The Johns Hopkins University Press, Baltimore.Google Scholar
Rensberger, J. M. 1995. Determination of stresses in mammalian dental enamel and their relevance to the interpretation of feeding behaviors in extinct taxa. Pp. 151–172 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Rensberger, J. M., and Stefen, C. 2006. Functional differentiations of the microstructure in the upper carnassial enamel of the spotted hyena. Palaeontographica Abteilung A 278:149–162.CrossRefGoogle Scholar
Schaub, S. 1941. Ein neues Hyaenidengenus von der Montagne de Perrier. Eclogae Geologicae Helvetiae 34:279–286.Google Scholar
Slater, G. J., and Van Valkenburgh, B. 2009. Allometry and performance: the evolution of skull form and function in felids. Journal of Evolutionary Biology 22:2278–2287.Google Scholar
Slater, G. J., Dumont, E. R., and Van Valkenburgh, B. 2009. Implications of predatory specialization for cranial form and function in canids. Journal of Zoology 278:181–188.Google Scholar
Stefen, C., and Rensberger, J. M. 1999. The specialized structure of hyaenid enamel: description and development within the lineage-including Percrocuta . Scanning Microscopy 13:363–80.Google Scholar
Tanner, J. B., Dumont, E. R., Sakai, S. T., Lundrigan, B. L., and Holekamp, K. E. 2008. Of arcs and vaults: the biomechanics of bone-cracking in spotted hyenas (Crocuta crocuta). Biological Journal of the Linnean Society 95:246–255.Google Scholar
Thomason, J. J. 1991. Cranial strength in relation to estimate biting forces in some mammals. Canadian Journal of Zoology 69:2326–2333.Google Scholar
Tseng, Z. J. 2009. Cranial function in a late Miocene Dinocrocuta gigantea (Mammalia: Carnivora) revealed by comparative finite element analysis. Biological Journal of the Linnean Society 96:51–67.CrossRefGoogle Scholar
Tseng, Z. J., and Binder, W. J. 2010. Mandibular biomechanics of Crocuta crocuta, Canis lupus, and the late Miocene Dinocrocuta gigantea (Carnivora, Mammalia). Zoological Journal of Linnean Society 158:683–696.CrossRefGoogle Scholar
Tseng, Z.J., and Wang, X. In press. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). Journal of Morphology.Google Scholar
Turner, A., Anton, M., and Werdelin, L. 2008. Taxonomy and evolutionary patterns in the fossil Hyaenidae of Europe. Geobios 41(5):677–687.Google Scholar
Van Valkenburgh, B. 1988. Incidence of tooth breakage among large, predatory mammals. American Naturalist, 131:291–302.CrossRefGoogle Scholar
Van Valkenburgh, B. 1990. Skeletal and dental predictors of body mass in carnivores. Pp. 181–205 in Damuth, J. and MacFadden, B. J., eds. Body Size in Mammalian Paleobiology: Estimation and Biological Implications. Cambridge University Press, Cambridge.Google Scholar
Van Valkenburgh, B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47:147–163.Google Scholar
Werdelin, L. 1989. Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387–401.CrossRefGoogle Scholar
Werdelin, L. 1996. Chapter 17. Carnivoran ecomorphology: a phylogenetic perspective. Pp. 582–624 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, New York.Google Scholar
Werdelin, L., and Solounias, N. 1991. The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata 30:1–104.Google Scholar
Werdelin, L. 1996. The evolutionary history of hyaenas in Europe and western Asia during the Miocene. Pp. 290–306 in Bernor, R. L., Rietschel, S., and Mittmann, W., eds. The Evolution of Western Eurasian Miocene Mammal Faunas. Columbia University Press, New York.Google Scholar
Wroe, S. 2008. Cranial mechanics compared in extinct marsupial and extant African lions using a finite-element approach. Journal of Zoology 274:332–339.CrossRefGoogle Scholar
Wroe, S., Clausen, P. D., McHenry, C., Moreno, K., and Cunningham, E. 2007a. Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap. Proceedings of the Royal Society B: Biological Sciences 274:2819–2828.CrossRefGoogle ScholarPubMed
Wroe, S., Moreno, K., Clausen, P., McHenry, C., and Curnoe, D. 2007b. High-resolution three-dimensional computer simulation of hominid cranial mechanics. Anatomical Records 290:1248–1255.Google Scholar