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Assessing niche conservatism using a multiproxy approach: dietary ecology of extinct and extant spotted hyenas

Published online by Cambridge University Press:  02 February 2017

Larisa R. G. DeSantis
Department of Earth and Environmental Sciences, Vanderbilt University, Nashville, Tennessee 37240, U.S.A. E-mail:
Zhijie Jack Tseng
Division of Paleontology, American Museum of Natural History, New York, New York 10024, U.S.A., and Department of Pathology and Anatomical Sciences, State University of New York at Buffalo, Buffalo, New York, U.S.A.
Jinyi Liu
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China
Aaron Hurst
Department of Earth and Environmental Sciences, Vanderbilt University, Nashville, Tennessee 37240, U.S.A. E-mail:
Blaine W. Schubert
Don Sundquist Center of Excellence in Paleontology and Department of Geosciences, East Tennessee State University, Johnson City, Tennessee 37614, U.S.A.
Qigao Jiangzuo
Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China


A central premise of bioclimatic envelope modeling is the assumption of niche conservatism. Whereas such assumptions are testable in modern populations, it is unclear whether niche conservatism holds over deeper time spans and over very large geographic ranges. Hyaenids occupied a diversity of ecological niches over time and space, and until the end-Pleistocene they occurred in Europe and most of Asia, with Asian populations of Crocuta suggested as being genetically distinct from their closest living relatives. Further, little is known regarding whether and how the dietary ecology of extinct populations of Crocuta differed from those of their extant African counterparts. Here, we use a multiproxy approach to assess an assumption of conserved dietary ecology in late Pleistocene extant spotted hyenas via finite element analysis, dental microwear texture analysis, and a novel dental macrowear method (i.e., whether teeth are minimally, moderately, or extremely worn, as defined by degree of dentin exposure) proposed here. Results from finite element simulations of the masticatory apparatus of Chinese and African Crocuta demonstrate lower skull stiffness and higher stress in the orbital region of the former when biting with carnassial teeth, suggesting that Chinese Crocuta could not process prey with the same degree of efficiency as extant Crocuta crocuta. Dental microwear texture data further support this interpretation, as Chinese Crocuta have intermediate and indistinguishable complexity values (indicative of hard-object feeding) between the extant African lion (Panthera leo) and extant hyenas (C. crocuta, Hyaena hyaena, and Parahyaena brunnea), being most similar to the omnivorous P. brunnea. The use of dental macrowear to infer dietary behavior may also be possible in extinct taxa, as evinced by dietary correlations between extant African feliforms and dental macrowear assignments. Collectively, this multiproxy analysis suggests that Chinese Crocuta may have exhibited dietary behavior distinct from that of living C. crocuta, and assumptions of niche conservatism may mask significant dietary variation in species broadly distributed in time and space.

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Literature Cited

Anyonge, W. 1996. Microwear on canines and killing behavior in large carnivores: saber function in Smilodon fatalis . Journal of Mammalogy 77:10591067.CrossRefGoogle Scholar
Araújo, M. B., and Townsend Peterson, A.. 2012. Uses and misuses of bioclimatic envelope modeling. Ecology 93:15271539.CrossRefGoogle ScholarPubMed
Arman, S. D., Ungar, P. S., Brown, C. A., DeSantis, L. R. G., Schmidt, C., and Prideaux, G. J.. 2016. Minimizing inter-microscope variability in dental microwear texture analysis. Surface Topography: Metrology and Properties 4(2): 024007.CrossRefGoogle Scholar
Bennett, M. B., and Taylor, G. C.. 1995. Scaling of elastic strain energy in kangaroos and the benefits of being big. Nature 378:5659.CrossRefGoogle ScholarPubMed
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 228:479507.CrossRefGoogle Scholar
Binder, W. J., and Van Valkenburgh, B.. 2010. A comparison of tooth wear and breakage in Rancho La Brea sabertooth cats and dire wolves across time. Journal of Vertebrate Paleontology 30:255261.CrossRefGoogle Scholar
Bourke, J., Wroe, S., Moreno, K., McHenry, C., and Clausen, P. D.. 2008. Effects of gape and tooth position on bite force and skull stress in the dingo (Canis lupus dingo) using a 3-dimensional finite element approach. PLoS ONE 3:e2200.CrossRefGoogle Scholar
Bright, J. A. 2014. A review of paleontological finite element models and their validity. Journal of Paleontology 88:760769.CrossRefGoogle Scholar
Cabin, R. J., and Mitchell, R. J.. 2000. To Bonferroni or not to Bonferroni: when and how are the questions. Bulletin of the Ecological Society of America 81:246248.Google Scholar
DeSantis, L. R. G. 2016. Dental microwear textures: reconstructing diets of fossil mammals. Surface Topography: Metrology and Properties 4(2): 023002.CrossRefGoogle Scholar
DeSantis, L. R. G., and Haupt, R. J.. 2014. Cougars’ key to survival through the late Pleistocene extinction: Insights from dental microwear texture analysis. Biology Letters 10:20140203.CrossRefGoogle ScholarPubMed
DeSantis, L. R. G., and MacFadden, B.. 2007. Identifying forested environments in deep time using fossil tapirs: evidence from evolutionary morphology and stable isotopes. Courier-Forschungsinstitut Senckenberg 258:147157.Google Scholar
DeSantis, L. R. G., Feranec, R. S., and MacFadden, B. J.. 2009. Effects of global warming on ancient mammalian communities and their environments. PLoS ONE 4:e5750.CrossRefGoogle ScholarPubMed
DeSantis, L. R. G., Beavins Tracy, R. A., Koontz, C. S., Roseberry, J. C., and Velasco, M. C.. 2012a. Mammalian niche conservation through deep time. PLoS ONE 7:e35624.CrossRefGoogle Scholar
DeSantis, L. R. G., Schubert, B. W., Scott, J. R., and Ungar, P. S.. 2012b. Implications of diet for the extinction of saber-toothed cats and American lions. PLoS ONE 7:e52453.CrossRefGoogle ScholarPubMed
DeSantis, L. R. G., Scott, J. R., Schubert, B. W., Donohue, S. L., McCray, B. M., Van Stolk, C. A., Wilburn, A. A., Greshko, M. A., and O’Hara, M. C.. 2013. Direct comparisons of 2D and 3D dental microwear proxies in extant herbivorous and carnivorous mammals. PLoS ONE 8:e71428.CrossRefGoogle Scholar
DeSantis, L. R. G., Schubert, B. W., Schmitt-Linville, E., Ungar, P. S., Donohue, S. L., and Haupt, R. L.. 2015. Dental microwear textures of carnivorans from the La Brea Tar Pits, California and potential extinction implications. Contributions in Science, Los Angeles County Museum of Natural History 42:3752.Google Scholar
Dessem, D., and Druzinsky, R. E.. 1992. Jaw-muscle activity in ferrets, Mustela putorius furo . Journal of Morphology 213:275286.CrossRefGoogle Scholar
Donohue, S. L., DeSantis, L. R. G., Schubert, B. W., and Ungar, P. S.. 2013. Was the giant short-faced bear a hyper-scavenger? A new approach to the dietary study of ursids using dental microwear textures. PLoS ONE 8:e77531.CrossRefGoogle Scholar
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 283A:319330.CrossRefGoogle Scholar
Dumont, E. R., Grosse, I., and Slater, G. J.. 2009. Requirements for comparing the performance of finite element models of biological structures. Journal of Theoretical Biology 256:96103.CrossRefGoogle Scholar
Dumont, E. R., Davis, J. L., Grosse, I., and Burrows, A. M.. 2011. Finite element analysis of performance in the skulls of marmosets and tamarins. Journal of Anatomy 218:151162.CrossRefGoogle ScholarPubMed
Dunn, O. J. 1964. Multiple comparisons using rank sums. Technometrics 6:241252.CrossRefGoogle Scholar
Estes, R. D. 1991. The behaviour guide to African mammals: including hoofed mammals, carnivores, primates. Berkeley: University of Calfornia Press.Google Scholar
Fortelius, M., and Solounias, N.. 2000. Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets. American Museum Novitates 3301.Google Scholar
Goillot, C., Blondel, C., and Peigné, S.. 2009. Relationships between dental microwear and diet in Carnivora (Mammalia)—implications for the reconstruction of the diet of extinct taxa. Palaeogeography, Palaeoclimatology, Palaeoecology 271:1323.CrossRefGoogle Scholar
Grosse, I., 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.CrossRefGoogle Scholar
Hadly, E. A., Spaeth, P. A., and Li, C.. 2009. Niche conservatism above the species level. Proceedings of the National Academy of Sciences USA 106:1970719714.CrossRefGoogle ScholarPubMed
Hayward, M. W. 2006. Prey preferences of the spotted hyaena (Crocuta crocuta) and degree of dietary overlap with the lion (Panthera leo). Journal of Zoology 270:606614.CrossRefGoogle Scholar
Hayward, M. W., and Kerley, G. I. H.. 2005. Prey preferences of the lion (Panthera leo). Journal of Zoology 267:309322.CrossRefGoogle Scholar
Hayward, M. W., Hofmeyr, M., O’Brien, J., and Kerley, G. I. H.. 2006. Prey preferences of the cheetah (Acinonyx jubatus) (Felidae: Carnivora): morphological limitations or the need to capture rapidly consumable prey before kleptoparasites arrive? Journal of Zoology 270:615627.CrossRefGoogle Scholar
Jones, D. B., and DeSantis, L. R. G.. 2016. Dietary ecology of the extinct cave bear: evidence of omnivory as inferred from dental microwear textures. Acta Palaeontologica Polonica 61:735741.CrossRefGoogle Scholar
Kruuk, H. 1972. The spotted hyena: a study of predation and social behavior. Chicago: University of Chicago Press.Google Scholar
Liu, J., Wagner, J., Chen, P., Sheng, G., Chen, J., Jiangzuo, Q., and Liu, S.. 2015. Mass mortality of a large population of the spotted hyenas (Crocuta ultima) at the Lingxiandong Cave, Qinhuangdao, Hebei Province: a hyena communal den with its palaeoecological and taphonomical interpretation. Quaternary Sciences 35:607621.Google Scholar
Loffredo, L. F., and DeSantis, L. R. G.. 2014. Cautionary lessons from assessing dental mesowear observer variability and integrating paleoecological proxies of an extreme generalist Cormohipparion emsliei . Palaeogeography, Palaeoclimatology, Palaeoecology 395:4252.CrossRefGoogle Scholar
Losos, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:9951007.CrossRefGoogle ScholarPubMed
Mihlbachler, M. C., Rivals, F., Solounias, N., and Semprebon, G. M.. 2011. Dietary change and evolution of horses in North America. Science 331:11781181.CrossRefGoogle ScholarPubMed
Mills, M. G. L. 1978. Foraging behaviour of the brown hyaena (Hyaena brunnea Thunberg, 1820) in the southern Kalahari. Zeitschrift für Tierpsychologie 48:113141.CrossRefGoogle Scholar
Mills, M. G. L. 1989. The comparative behavioral ecology of hyenas: the importance of diet and food dispersion. Pp. 125142 in J. L. Gittleman, ed. Carnivore behavior, ecology, and evolution. New York: Springer.CrossRefGoogle Scholar
Mills, M. G. L. 1990. Kalahari hyenas: comparative behavioral ecology of two species. Caldwell, N.J.: Blackburn.CrossRefGoogle Scholar
Mills, M. G. L., and Mills, M. E.. 1978. The diet of the brown hyaena Hyaena brunnea in the southern Kalahari. Koedoe 21:125149.CrossRefGoogle Scholar
Münzel, S. C., Rivals, F., Pacher, M., Döppes, D., Rabeder, G., Conard, N. J., and Bocherens, H.. 2014. Behavioural ecology of Late Pleistocene bears (Ursus spelaeus, Ursus ingressus): insight from stable isotopes (C, N, O) and tooth microwear. Quaternary International 339:148163.CrossRefGoogle Scholar
Nakagawa, S. 2004. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behavioral Ecology 15:10441045.CrossRefGoogle Scholar
Nalla, R. K., Kinney, J. H., and Ritchie, R. O.. 2003. Mechanistic failure criteria for the failure of human cortical bone. Nature Materials 2:164168.CrossRefGoogle ScholarPubMed
Nowak, R. M. 1999. Walker’s mammals of the world, 6th edn. Baltimore, Md.: Johns Hopkins University Press.Google Scholar
Nowak, R. M. 2005. Walker’s carnivores of the world, 7th edn. Baltimore, Md.: Johns Hopkins University Press.Google Scholar
Olifiers, N., de Cassia Bianchi, R., D’Andrea, P. S., Mourao, G., and Gompper, M. E.. 2010. Estimating age of carnivores from the Pantanal region of Brazil. Wildlife Biology 16:389399.CrossRefGoogle Scholar
Owens, M. J., and Owens, D. D.. 1978. Feeding ecology and its influence on social organization in brown hyenas (Hyaena brunnea, Thunberg) of the central Kalahari Desert. African Journal of Ecology 16:113135.CrossRefGoogle Scholar
Owens, M. J., and Owens, D. D.. 1979. Communal denning and clan associations in brown hyenas (Hyaena brunnea, Thunberg) of the central Kalahari Desert. African Journal of Ecology 17:3544.CrossRefGoogle Scholar
Pei, W. C. 1940. The Upper Cave fauna of Choukoutien. Palaeontologia Sinica, new series C 10:1100.Google Scholar
Peigné, S., Goillot, C., Germonpré, M., Blondel, C., Bignon, O., and Merceron, G.. 2009. Predormancy omnivory in European cave bears evidenced by a dental microwear analysis of Ursus spelaeus from Goyet, Belgium. Proceedings of the National Academy of Sciences USA 106:1539015393.CrossRefGoogle ScholarPubMed
Peterson, A. T. 2011. Ecological niche conservatism: a time-structured review of evidence. Journal of Biogeography 38:817827.CrossRefGoogle Scholar
Pollock, C. M., and Shadwick, R. E.. 1994. Allometry of muscle, tendon, and elastic energy of storage capacity in mammals. American Journal of Physiology 266:10221031.Google ScholarPubMed
Rayfield, E. J. 2007. Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annual Review of Earth and Planetary Science 35:541576.CrossRefGoogle Scholar
Rivals, F., Mihlbachler, M. C., and Solounias, N.. 2007. Effect of ontogenetic-age distribution in fossil and modern samples on the interpretation of ungulate paleodiets using the mesowear method. Journal of Vertebrate Paleontology 27:763767.CrossRefGoogle Scholar
Robson, S. K., and Young, W. G.. 1990. A comparison of tooth microwear between an extinct marsupial predator, the Tasmanian tiger Thylacinus cynocephalus (Thylacinidae) and an extant scavenger, the Tasmanian devil Sarcophilus harrisii (Dasyuridae, Marsupialia). Australian Journal of Zoology 37:575589.CrossRefGoogle Scholar
Schaller, G. B. 1972. The Serengeti lion: a study of predator–prey relations. Chicago: University of Chicago Press.Google Scholar
Schubert, B. W., Ungar, P. S., and DeSantis, L. R. G.. 2010. Carnassial microwear and dietary behavior in large carnivorans. Journal of Zoology 280:257263.CrossRefGoogle Scholar
Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Grine, F. E., Teaford, M. F., and Walker, A.. 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693695.CrossRefGoogle Scholar
Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Childs, B. E., Teaford, M. F., and Walker, A.. 2006. Dental microwear texture analysis: technical considerations. Journal of Human Evolution 51:339349.CrossRefGoogle ScholarPubMed
Sheng, G., Soubrier, J., Liu, J. Y., Werdelin, L., Llmas, B., Thomson, V., Tuke, J., Wu, L., Hou, X., Chen, Q., Lai, X., and Cooper, A.. 2014. Pleistocene Chinese cave hyenas and the recent Eurasian history of the spotted hyena, Crocuta crocuta . Molecular Ecology 23:522533.CrossRefGoogle Scholar
Stander, P. E. 1997. Field age determination of leopards by tooth wear. African Journal of Ecology 35:156161.CrossRefGoogle Scholar
Taylor, M. E., and Hannam, A. G.. 1987. Tooth microwear and diet in the African Viverridae. Canadian Journal of Zoology 65:16961702.CrossRefGoogle Scholar
Teaford, M. F. 1988. A review of dental microwear and diet in modern mammals. Scanning Microscopy 2:11491166.Google ScholarPubMed
Tseng, Z. J. 2013. Testing adaptive hypotheses of convergence with functional landscapes: a case study of bone-cracking hypercarnivores. PLoS ONE 8:e65305.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 the Linnean Society 158:683696.CrossRefGoogle Scholar
Tseng, Z. J., and Chang, C.-H.. 2007. A study of new material of Crocuta crocuta ultima (Carnivora: Hyaenidae) from the Quaternary of Taiwan. Collection and Research 20:919.Google Scholar
Tseng, Z. J., and Flynn, J. J.. 2015a. Are cranial biomechanical simulation data linked to known diets in extant taxa? A method for applying diet-biomechanics linkage models to infer feeding capability of extinct species. PLoS ONE 10:e0124020.CrossRefGoogle Scholar
Tseng, Z. J., and Flynn, J. J.. 2015b. Convergence analysis of a finite element skull model of Herpestes javanicus (Carnivora, Mammalia): implications for robust comparative inferences of biomechanical function. Journal of Theoretical Biology 365:112148.CrossRefGoogle ScholarPubMed
Tseng, Z. J., and Wang, X.. 2010. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). Journal of Morphology 271:13861398.CrossRefGoogle Scholar
Tseng, Z. J., Antón, M., and Salesa, M. J.. 2011. The evolution of the bone-cracking model in carnivorans: cranial functional morphology of the Plio-Pleistocene cursorial hyaenid Chasmaporthetes lunensis (Mammalia: Carnivora). Paleobiology 37:140156.CrossRefGoogle Scholar
Ungar, P. S., Brown, C. A., Bergstrom, T. S., and Walkers, A.. 2003. Quantification of dental microwear by tandem scanning confocal microscopy and scale-sensitive fractal analyses. Scanning 25:185193.CrossRefGoogle ScholarPubMed
Ungar, P. S., Scott, J. R., Schubert, B. W., and Stynder, D. D.. 2010. Carnivoran dental microwear textures: comparability of carnassial facets and functional differentiation of the postcanine teeth. Mammalia 74:219224.CrossRefGoogle Scholar
Ungar, P., Ragni, A., and DeSantis, L.. 2014. Comparability of dental microwear texture data between studies. Journal of Vertebrate Paleontology, Program and Abstracts 2014:244.Google Scholar
Van Valkenburgh, B. 1988. Incidence of tooth breakage among large, predatory mammals. American Naturalist 131:291302.CrossRefGoogle Scholar
Van Valkenburgh, B. 1996. Feeding behavior in free-ranging, large African carnivores. Journal of Mammalogy 77:240254.CrossRefGoogle Scholar
Van Valkenburgh, B. 1999. Major patterns in the history of carnivorous mammals. Annual Review of Earth and Planetary Sciences 27:463493.CrossRefGoogle Scholar
Van Valkenburgh, B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrated and Comparative Biology 47:147163.CrossRefGoogle ScholarPubMed
Van Valkenburgh, B. 2009. Costs of carnivory: tooth fracture in Pleistocene and Recent carnivorans. Biological Journal of the Linnean Society 96:6881.CrossRefGoogle Scholar
Van Valkenburgh, B., and Hertel, F.. 1993. Tough times at La Brea: tooth breakage in large carnivores of the Late Pleistocene. Science 261:456459.CrossRefGoogle Scholar
Van Valkenburgh, B., Teaford, M. F., and Walker, A.. 1990. Molar microwear and diet in large carnivores: inferences concerning diet in the sabretooth cat, Smilodon fatalis . Journal of Zoology 222:319340.CrossRefGoogle Scholar
Wagner, A. P. 2006. Behavioral ecology of the striped hyena (Hyaena hyaena). Ph.D. thesis, Montana State University, Bozeman.Google Scholar
Werdelin, L. 1989. Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387401.CrossRefGoogle Scholar
Werdelin, L. 1996. Carnivoran ecomorphology: a phylogenetic perspective. Pp. 582624 in J. L. Gittleman, ed. Carnivore behavior, ecology, and evolution, Vol. 2. New York: Cornell University Press.Google Scholar
Werdelin, L., and Solounias, N.. 1991. The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata 30:1104.Google Scholar
Werdelin, L., and Solounias, N.. 1996. The evolutionary history of hyenas in Europe and western Asia during the Miocene. Pp. 290306 in R. L. Bernor, V. Fahlbusch, and S. Rietschel, eds. Later Neogene European biotic evolution and stratigraphic correlation. New York: Columbia University Press.Google Scholar
Wiens, J. J., and Graham, C. H.. 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Reviews of Ecology, Evolution, and Systematics 36:519539.CrossRefGoogle Scholar
Wroe, S. 2008. Cranial mechanics compared in extinct marsupial and extant African lions using a finite-element approach. Journal of Zoology 274:332339.CrossRefGoogle Scholar