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

  • Larisa R. G. DeSantis (a1), Zhijie Jack Tseng (a2), Jinyi Liu (a3), Aaron Hurst (a1), Blaine W. Schubert (a4) and Qigao Jiangzuo (a3)...
Abstract
Abstract

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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Anyonge W. 1996. Microwear on canines and killing behavior in large carnivores: saber function in Smilodon fatalis . Journal of Mammalogy 77:10591067.
Araújo M. B., and Townsend Peterson A.. 2012. Uses and misuses of bioclimatic envelope modeling. Ecology 93:15271539.
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.
Bennett M. B., and Taylor G. C.. 1995. Scaling of elastic strain energy in kangaroos and the benefits of being big. Nature 378:5659.
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.
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.
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.
Bright J. A. 2014. A review of paleontological finite element models and their validity. Journal of Paleontology 88:760769.
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.
DeSantis L. R. G. 2016. Dental microwear textures: reconstructing diets of fossil mammals. Surface Topography: Metrology and Properties 4(2): 023002.
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.
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.
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.
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.
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.
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.
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.
Dessem D., and Druzinsky R. E.. 1992. Jaw-muscle activity in ferrets, Mustela putorius furo . Journal of Morphology 213:275286.
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.
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.
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.
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.
Dunn O. J. 1964. Multiple comparisons using rank sums. Technometrics 6:241252.
Estes R. D. 1991. The behaviour guide to African mammals: including hoofed mammals, carnivores, primates. Berkeley: University of Calfornia Press.
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.
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.
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.
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.
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.
Hayward M. W., and Kerley G. I. H.. 2005. Prey preferences of the lion (Panthera leo). Journal of Zoology 267:309322.
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.
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.
Kruuk H. 1972. The spotted hyena: a study of predation and social behavior. Chicago: University of Chicago Press.
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.
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.
Losos J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:9951007.
Mihlbachler M. C., Rivals F., Solounias N., and Semprebon G. M.. 2011. Dietary change and evolution of horses in North America. Science 331:11781181.
Mills M. G. L. 1978. Foraging behaviour of the brown hyaena (Hyaena brunnea Thunberg, 1820) in the southern Kalahari. Zeitschrift für Tierpsychologie 48:113141.
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.
Mills M. G. L. 1990. Kalahari hyenas: comparative behavioral ecology of two species. Caldwell, N.J.: Blackburn.
Mills M. G. L., and Mills M. E.. 1978. The diet of the brown hyaena Hyaena brunnea in the southern Kalahari. Koedoe 21:125149.
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.
Nakagawa S. 2004. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behavioral Ecology 15:10441045.
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.
Nowak R. M. 1999. Walker’s mammals of the world, 6th edn. Baltimore, Md.: Johns Hopkins University Press.
Nowak R. M. 2005. Walker’s carnivores of the world, 7th edn. Baltimore, Md.: Johns Hopkins University Press.
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.
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.
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.
Pei W. C. 1940. The Upper Cave fauna of Choukoutien. Palaeontologia Sinica, new series C 10:1100.
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.
Peterson A. T. 2011. Ecological niche conservatism: a time-structured review of evidence. Journal of Biogeography 38:817827.
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.
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.
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.
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.
Schaller G. B. 1972. The Serengeti lion: a study of predator–prey relations. Chicago: University of Chicago Press.
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.
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.
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.
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.
Stander P. E. 1997. Field age determination of leopards by tooth wear. African Journal of Ecology 35:156161.
Taylor M. E., and Hannam A. G.. 1987. Tooth microwear and diet in the African Viverridae. Canadian Journal of Zoology 65:16961702.
Teaford M. F. 1988. A review of dental microwear and diet in modern mammals. Scanning Microscopy 2:11491166.
Tseng Z. J. 2013. Testing adaptive hypotheses of convergence with functional landscapes: a case study of bone-cracking hypercarnivores. PLoS ONE 8:e65305.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Van Valkenburgh B. 1988. Incidence of tooth breakage among large, predatory mammals. American Naturalist 131:291302.
Van Valkenburgh B. 1996. Feeding behavior in free-ranging, large African carnivores. Journal of Mammalogy 77:240254.
Van Valkenburgh B. 1999. Major patterns in the history of carnivorous mammals. Annual Review of Earth and Planetary Sciences 27:463493.
Van Valkenburgh B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrated and Comparative Biology 47:147163.
Van Valkenburgh B. 2009. Costs of carnivory: tooth fracture in Pleistocene and Recent carnivorans. Biological Journal of the Linnean Society 96:6881.
Van Valkenburgh B., and Hertel F.. 1993. Tough times at La Brea: tooth breakage in large carnivores of the Late Pleistocene. Science 261:456459.
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.
Wagner A. P. 2006. Behavioral ecology of the striped hyena (Hyaena hyaena). Ph.D. thesis, Montana State University, Bozeman.
Werdelin L. 1989. Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387401.
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.
Werdelin L., and Solounias N.. 1991. The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata 30:1104.
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.
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.
Wroe S. 2008. Cranial mechanics compared in extinct marsupial and extant African lions using a finite-element approach. Journal of Zoology 274:332339.
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