Skip to main content

Advertisement

Log in

Functional morphology of the cave bear (Ursus spelaeus) mandible: a 3D geometric morphometric analysis

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

The diet of the fossil cave bears (Ursus spelaeus group) has been debated extensively. Thought traditionally to be herbivorous, more recent studies have proposed more meat in the cave bear diet. To test this, the mandibular morphology of cave bears was analysed using 3D geometric morphometrics and compared to that of extant Ursidae. Landmarks for 3D digitisation of the mandible were chosen to reflect functional morphology relating to the temporalis and masseter muscles. Extant and extinct Pleistocene Ursidae were digitised with a MicroScribe G2. Generalised Procrustes superimposition was performed, and data were allometrically and phylogenetically corrected. Principal component analysis (PCA), two-block partial least squares analysis (2B-PLS), regression analysis and discriminant function analysis were performed. PCA and 2B-PLS differentiate between known dietary niches in extant Ursidae. The lineage of the cave bear runs parallel to that of the panda (Ailuropoda melanoleuca) in morphospace, implying the development of morphological adaptations for eating foliage. A regression of shape onto foliage content in the diet and a discriminant function analysis also indicate that the cave bear diet consisted primarily of foliage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams, D. C. (2014). A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Systematic Biology, 63(5), 685–697.

    Article  PubMed  Google Scholar 

  • Anyonge, W., & Baker, A. (2006). Craniofacial morphology and feeding behavior in Canis dirus, the extinct Pleistocene dire wolf. Journal of Zoology, 269(3), 309–316.

    Article  Google Scholar 

  • Arribas, A., & Palmqvist, P. (1999). On the ecological connection between sabre-tooths and hominids: faunal dispersal events in the Lower Pleistocene and a review of the evidence for the first human arrival in Europe. Journal of Archaeological Science, 26(5), 571–585.

    Article  Google Scholar 

  • Athen, K. (2006). Biostatistical investigation of long bones and metapodial bones of Ursus spelaeus and Ursus deningeri. Scientific Annals, School of Geology Aristotle University of Thessaloniki, 98, 159–162.

    Google Scholar 

  • Athen, K. (2007). Biometrische Untersuchungen des Stylopodiums, Zygopodiums und Metapodiums pleistozäner Ursiden im Hinblick auf die Evolution des Höhlenbären und die Klassifizierung des Fundmaterials Einhornhöhle/Harz. Ph. D. thesis, Eberhard-Karls-Universität, Tübingen.

  • Augeri, D. M. (1995). On the biogeographic ecology of the Malayan sun bear. Cambridge: University of Cambridge.

    Google Scholar 

  • Azzaroli, A. (1983). Quaternary mammals and the “end-Villafranchian” dispersal event—a turning point in the history of Eurasia. Palaeogeography, Palaeoclimatology, Palaeoecology, 44(1–2), 117–139. doi:10.1016/0031-0182(83)90008-1.

    Article  Google Scholar 

  • Baca, M., Stankovic, A., Stefaniak, K., Marciszak, A., Hofreiter, M., Nadachowski, A., et al. (2012). Genetic analysis of cave bear specimens from Niedźwiedzia Cave, Sudetes, Poland. Palaeontologia Electronica, 15(2), 21A.

    Google Scholar 

  • Bargali, H. S., Akhtar, N., & Chauhan, N. P. S. (2009). Feeding ecology of sloth bears in a disturbed area in central India. Ursus, 15(2), 212–217. doi:10.2192/1537-6176(2004)015<0212:feosbi>2.0.co;2.

    Article  Google Scholar 

  • Baryshnikov, G. (2007). Ursidae (Fauna of Russia and neighbouring countries, new ser. 147 ). Saint Petersburg: Nauka. (in Russian)

  • Biknevicius, A. R., Van Valkenburgh, B., & Walker, J. (1996). Incisor size and shape: implications for feeding behaviors in saber-toothed “cats”. Journal of Vertebrate Paleontology, 16(3), 510–521.

    Article  Google Scholar 

  • Binder, W. J., & Van Valkenburgh, B. (2000). Development of bite strength and feeding behaviour in juvenile spotted hyenas (Crocuta crocuta). Journal of Zoology, 252, 273–283.

    Article  Google Scholar 

  • Bininda-Emonds, O. R. P., Gittleman, J. L., & Purvis, A. (1999). Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biological Reviews, 74(2), 143–175.

    Article  CAS  PubMed  Google Scholar 

  • Bocherens, H., Fizet, M., & Mariotti, A. (1994). Diet, physiology and ecology of fossil mammals as inferred from stable carbon and nitrogen isotope biogeochemistry: implications for Pleistocene bears. Palaeogeography, Palaeoclimatology, Palaeoecology, 107(3–4), 213–225.

    Article  Google Scholar 

  • Bocherens, H., Billiou, D., Patou-Mathis, M., Bonjean, D., Otte, M., & Mariotti, A. (1997). Paleobiological implications of the isotopic signatures (13C,15N) of fossil mammal collagen in Scladina cave (Sclayn, Belgium). Quaternary Research, 48(3), 370–380.

    Article  Google Scholar 

  • Bocherens, H., Stiller, M., Hobson, K. A., Pacher, M., Rabeder, G., Burns, J. A., et al. (2011). Niche partitioning between two sympatric genetically distinct cave bears (Ursus spelaeus and Ursus ingressus) and brown bear (Ursus arctos) from Austria: isotopic evidence from fossil bones. Quaternary International, 245(2), 238–248.

    Article  Google Scholar 

  • Bocherens, H., Bridault, A., Drucker, D. G., Hofreiter, M., Münzel, S. C., Stiller, M., et al. (2014). The last of its kind? Radiocarbon, ancient DNA and stable isotope evidence from a late cave bear (Ursus spelaeus ROSENMÜLLER, 1794) from Rochedane (France). Quaternary International, 339–340, 179–188.

    Article  Google Scholar 

  • Bojarska, K., & Selva, N. (2012). Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors. Mammal Review, 42(2), 120–143. doi:10.1111/j.1365-2907.2011.00192.x.

    Article  Google Scholar 

  • Bon, C., Caudy, N., de Dieuleveult, M., Fosse, P., Philippe, M., Maksud, F., et al. (2008). Deciphering the complete mitochondrial genome and phylogeny of the extinct cave bear in the Paleolithic painted cave of Chauvet. Proceedings of the National Academy of Sciences of the United States of America, 105(45), 17447–17452. doi:10.1073/pnas.0806143105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bookstein, F. L. (1991). Morphometric tools for landmark data geometry and biology. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bruner, E., & Costantini, D. (2009). Head morphology and degree of variation in Lacerta bilineata, Podarcis muralis and Podarcis sicula. International Journal of Morphology, 27(3), 667–676.

    Article  Google Scholar 

  • Cahill, J. A., Green, R. E., Fulton, T. L., Stiller, M., Jay, F., Ovsyanikov, N., et al. (2013). Genomic evidence for island population conversion resolves conflicting theories of polar bear evolution. PLoS Genetics, 9(3), e1003345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christiansen, P. (2007a). Canine morphology in the larger Felidae: implications for feeding ecology. Biological Journal of the Linnean Society, 91(4), 573–592.

    Article  Google Scholar 

  • Christiansen, P. (2007b). Comparative bite forces and canine bending strength in feline and sabretooth felids: implications for predatory ecology. Zoological Journal of the Linnean Society, 151, 423–437.

    Article  Google Scholar 

  • Christiansen, P. (2007c). Evolutionary implications of bite mechanics and feeding ecology in bears. Journal of Zoology, 272(4), 423–443.

    Article  Google Scholar 

  • Christiansen, P. (2008). Feeding ecology and morphology of the upper canines in bears (Carnivora: Ursidae). Journal of Morphology, 269(7), 896–908.

    Article  PubMed  Google Scholar 

  • Christiansen, P., & Adolfssen, J. S. (2005). Bite forces, canine strength and skull allometry in carnivores (Mammalia, Carnivora). Journal of Zoology, 266, 133–151.

    Article  Google Scholar 

  • Clark, P. U., Archer, D., Pollard, D., Blum, J. D., Rial, J. A., Brovkin, V., et al. (2006). The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quaternary Science Reviews, 25(23–24), 3150–3184.

    Article  Google Scholar 

  • Cox, P. G. (2008). A quantitative analysis of the Eutherian orbit: correlations with masticatory apparatus. Biological Reviews, 83(1), 35–69. doi:10.1111/j.1469-185X.2007.00031.x.

    PubMed  Google Scholar 

  • Davis, D. D. (1955). Masticatory apparatus in the spectacled bear. Fieldiana: Zoology, 37, 25–46.

    Google Scholar 

  • Desdevises, Y., Legendre, P., Azouzi, L., & Morand, S. (2003). Quantifying phylogenetically structured environmental variation. Evolution, 57(11), 2647–2652.

    Article  PubMed  Google Scholar 

  • Emerson, S. B., & Radinsky, L. (1980). Functional-analysis of sabertooth cranial morphology. Paleobiology, 6(3), 295–312.

    Google Scholar 

  • Enloe, J. G., David, F., & Baryshnikov, G. (2000). Hyenas and hunters: zooarchaeological investigations at Prolom II Cave, Crimea. International Journal of Osteoarchaeology, 10(5), 310–324.

    Article  Google Scholar 

  • Evans, A. R., Martin, T., Fortelius, M., & Jernvall, J. (2006a). Reconstructing dental occlusion in 3D: from carnivorans to Asfaltomylos. Journal of Vertebrate Paleontology, 26(3), 59A–59A.

    Google Scholar 

  • Evans, A. R., Wilson, G. P., Fortelius, M., & Jernvall, J. (2006b). High-level similarity of dentitions in carnivorans and rodents. Nature, 445, 78–81.

    Article  PubMed  CAS  Google Scholar 

  • Ewer, R. G. (1973). The carnivores. Ithaca: Cornell University Press.

    Google Scholar 

  • Figueirido, B., Palmqvist, P., & Pérez-Claros, J. A. (2009). Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics. Journal of Zoology, 277(1), 70–80.

    Article  Google Scholar 

  • Figueirido, B., Serrano-Alarcón, F. J., & Palmqvist, P. (2012). Geometric morphometrics shows differences and similarities in skull shape between the red and giant pandas. Journal of Zoology, 286(4), 293–302. doi:10.1111/j.1469-7998.2011.00879.x.

    Article  Google Scholar 

  • Flynn, J. J., & Nedbal, M. A. (1998). Phylogeny of the Carnivora (Mammalia): congruence vs incompatibility among multiple data sets. Molecular Phylogenetics and Evolution, 9(3), 414–426. doi:10.1006/mpev.1998.0504.

    Article  CAS  PubMed  Google Scholar 

  • Fredriksson, G. M., Wich, S. A., & Trisno. (2006). Frugivory in sun bears (Helarctos malayanus) is linked to El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biological Journal of the Linnean Society, 89(3), 489–508.

    Article  Google Scholar 

  • Fulton, T. L., & Strobeck, C. (2006). Molecular phylogeny of the Arctoidea (Carnivora): effect of missing data on supertree and supermatrix analyses of multiple gene data sets. Molecular Phylogenetics and Evolution, 41(1), 165–181. doi:10.1016/j.ympev.2006.05.025.

    Article  CAS  PubMed  Google Scholar 

  • Ginsburg, L., & Morales, J. (1998). Les Hemicyoninae (Ursidae, Carnivora, Mammalia) et les formes apparentées du Miocène inférieur et moyen d’Europe occidentale. Annales de Paleontologie, 84(1), 71–123. doi:10.1016/s0753-3969(98)80003-7.

    Article  Google Scholar 

  • Gittleman, J. L. (1985). Carnivore body size—ecological and taxonomic correlates. Oecologia, 67(4), 540–554.

    Article  Google Scholar 

  • Grandal-d’Anglade, A., & Vidal Romaní, J. R. (1997). A population study on the cave bear (Ursus spelaeus Ros.-Hein.) from Cova Eirós (Triacastela, Galicia, Spain). Geobios, 30(5), 723–731.

    Article  Google Scholar 

  • Hänni, C., Laudet, V., Stehelin, D., & Taberlet, P. (1994). Tracking the origins of the cave bear (Ursus spelaeus) by mitochondrial DNA sequencing. Proceedings of the National Academy of Sciences of the United States of America, 91(25), 12336–12340.

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrero, S. (1972). Aspects of evolution and adaptation in American black bears (Ursus americanus Pallus) and brown and grizzly bears (Ursus arctos Linn.) of North America. Bears - Their Biology and Management, 23, 221–231.

    Article  Google Scholar 

  • Hilderbrand, G. V., Farley, S. D., Robbins, C. T., Hanley, T. A., Titus, K., & Servheen, C. (1996). Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology, 74, 2080–2088.

    Article  Google Scholar 

  • Hofreiter, M., Capelli, C., Krings, M., Waits, L., Conard, N., Münzel, S., et al. (2002). Ancient DNA analyses reveal high mitochondrial DNA sequence diversity and parallel morphological evolution of Late Pleistocene cave bears. Molecular Biology and Evolution, 19(8), 1244–1250.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, R. M. (1999). Ursidae. In C. M. Janis, K. M. Scott, & L. L. Jacobs (Eds.), Evolution of tertiary mammals of North America (pp. 174–195). New York: Cambridge University Press.

    Google Scholar 

  • Hunt, R. M. (2004). A paleontologist’s perspective on the origin and relationships of the giant panda. In D. G. Lindburg & K. Baragona (Eds.), Giant pandas: biology and conservation (p. 308). Berkely: University of California Press.

    Google Scholar 

  • Ives, A. R., Midford, P. E., & Garland, T., Jr. (2007). Within-species measurement error in phylogenetic comparative methods. Systematic Biology, 56, 252–270.

    Article  PubMed  Google Scholar 

  • Jin, C., Ciochon, R. L., Dong, W., Hunt, R. M., Liu, J., Jaeger, M., et al. (2007). The first skull of the earliest giant panda. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 10932–10937. doi:10.1073/pnas.0704198104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin, K., Xue, C., Wu, X., Qian, J., Zhu, Y., Yang, Z., et al. (2011). Why does the giant panda eat bamboo? A comparative analysis of appetite-reward-related genes among mammals. PLoS ONE, 6(7), e22602. doi:10.1371/journal.pone.0022602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi, A. R., Garshelis, D. L., & Smith, J. L. D. (1997). Seasonal and habitat-related diets of sloth bears in Nepal. Journal of Mammalogy, 78(2), 584–597.

    Article  Google Scholar 

  • Klingenberg, C. P. (2010a). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 353–357, doi:10.1111/j.1755-0998.2010.02924.x.

  • Klingenberg, C. P. (2010b). New Procrustes Fit. http://www.flywings.org.uk/MorphoJ_guide/frameset.htm?index.htm. Accessed September 16th 2010.

  • Klingenberg, C. P. (2010c). Regression. http://www.flywings.org.uk/MorphoJ_guide/frameset.htm?index.htm. Accessed June 1st 2010.

  • Kosintsev, P. (2007). Late Pleistocene large mammal faunas from the Urals. Quaternary International, 160, 112–120. doi:10.1016/j.quaint.2006.09.012.

    Article  Google Scholar 

  • Krause, J., Unger, T., Nocon, A., Malaspinas, A.-S., Koloktronis, S.-O., Stiller, M., et al. (2008). Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. Evolutionary Biology, 8(220), 1–12.

    Google Scholar 

  • Kupczik, K., & Stynder, D. D. (2012). Tooth root morphology as an indicator for dietary specialisation in carnivores (Mammalia: Carnivora). Biological Journal of the Linnean Society, 105(2), 456–471.

    Article  Google Scholar 

  • Kurt, F. (1990). Malayan Sun Bear. In S. P. Parker (Ed.), Grzimek’s encyclopedia of mammals (Vol. 3, p. 504). New York: McGraw-Hill Publishing Company.

    Google Scholar 

  • Laurie, A., & Seidensticker, J. (1977). Behavioural ecology of the Sloth bear (Melursus ursinus). Journal of Zoology, 182(2), 187–204.

    Article  Google Scholar 

  • Lisiecki, L. E., & Raymo, M. E. (2007). Plio-Pleistocene climate evolution: trends and transitions in glacial cycle dynamics. Quaternary Science Reviews, 26(1–2), 56–69.

    Article  Google Scholar 

  • Martin, L. D. (1989). Fossil history of the terrestrial Carnivora. In J. L. Gittleman (Ed.), Carnivore behaviour, ecology and evolution (pp. 536–568). London: Chapman and Hall.

    Chapter  Google Scholar 

  • Martínez-Navarro, B., & Palmqvist, P. (1996). Presence of the African saber-toothed felid Megantereon whitei (Broom, 1937) (Mammalia, Carnivora, Machairodontinae) in Apollonia-1 (Mygdonia Basin, Macedonia, Greece). Journal of Archaeological Science, 23(6), 869–872.

    Article  Google Scholar 

  • Mattson, D. J. (1998). Diet and morphology of extant and recently extinct northern bears. Ursus, 10, 479–496.

    Google Scholar 

  • McLellan, B., & Reiner, D. C. (1994). A review of bear evolution. Bears - Their Biology and Management, 85–96.

  • McNulty, K. P. (2004). A geometric morphometric assessment of hominoid crania: conservative African apes and their liberal implications. Annals of Anatomy - Anatomischer Anzeiger, 186(5–6), 429–433.

    Article  PubMed  Google Scholar 

  • Meijaard, E. (1998). Ursus (Helarctos) malayanus, the neglected Malayan sun bear. Nederlandse Commissie voor Internationale Natuurbescherming. Mededelingen, 34, 1-62.

  • Meloro, C. (2007). Plio-Pleistocene large carnivores from the Italian pensinsula: functional morphology and macroecology. Ph. D. thesis, Università degli Studi di Napoli “Federico II”, Napoli.

  • Meloro, C. (2011). Feeding habits of Plio-Pleistocene large carnivores as revealed by the mandibular geometry. Journal of Vertebrate Paleontology, 31(2), 428–446.

    Article  Google Scholar 

  • Meloro, C., Raia, P., Piras, P., Barbera, C., & O’Higgins, P. (2008). The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zoological Journal of the Linnean Society, 154, 832–845.

    Article  Google Scholar 

  • Meloro, C., Clauss, M., & Raia, P. (2015a). Ecomorphology of Carnivora challenges convergent evolution. Organisms Diversity & Evolution, 1–10, doi:10.1007/s13127-015-0227-5.

  • Meloro, C., Hudson, A., & Rook, L. (2015b). Feeding habits of extant and fossil canids as determined by their skull geometry. Journal of Zoology, 295(3), 178–188.

    Article  Google Scholar 

  • Mutsvangwa, T. E. M., Meintjes, E. M., Viljoen, D. L., & Douglas, T. S. (2010). Morphometric analysis and classification of the facial phenotype associated with fetal alcohol syndrome in 5- and 12-year-old children. American Journal of Medical Genetics Part A, 152A, 32–41.

    Article  PubMed  Google Scholar 

  • Nawaz, M. A. (2008). Ecology, Genetics and Conservation of Himalayan Brown Bears. Ph. D. thesis, Norwegian University of Life Sciences, Ås.

  • Nelson, R. A., Folk, G. E., Pfeiffer, E. W., Craighead, J. J., Jonkel, C. J., & Steiger, D. L. (1983). Behavior, biochemistry, and hibernation in black, grizzly, and polar bears. International Conference on Bear Research and Management, 5, 284–290.

    Google Scholar 

  • Oldfield, C. C., McHenry, C. R., Clausen, P. D., Chamoli, U., Parr, W. C. H., Stynder, D. D., et al. (2012). Finite element analysis of ursid cranial mechanics and the prediction of feeding behaviour in the extinct giant Agriotherium. Journal of Zoology, 286(2), 163–170.

    Article  Google Scholar 

  • Osborn, H. F. (2010). The age of mammals in Europe, Asia and North America. New York: MacMillan Co.

    Google Scholar 

  • Pacher, M., & Stuart, A. J. (2008). Extinction chronology and palaeobiology of the cave bear (Ursus spelaeus). Boreas, 38, 189–206.

    Article  Google Scholar 

  • Palmqvist, P., Gröcke, D. R., Arribas, A., & Fariña, R. A. (2003). Paleoecological reconstruction of a Lower Pleistocene large mammal community using biogeochemical (δ13C, δ15N, δ18O, Sr: Zn) and ecomorphological approaches. Paleobiology, 29(2), 205–229.

    Article  Google Scholar 

  • Palmqvist, P., Pérez-Claros, J. A., Janis, C. M., Figueirido, B., Torregrosa, V., & Gröcke, D. R. (2008a). Biogeochemical and ecomorphological inferences on prey selection and resource partitioning among mammalian carnivores in an Early Pleistocene community. Palaios, 23(11), 724–737. doi:10.2110/palo.2007.p07-073r.

    Article  Google Scholar 

  • Palmqvist, P., Pérez-Claros, J. A., Janis, C. M., & Gröcke, D. R. (2008b). Tracing the ecophysiology of ungulates and predator–prey relationships in an early Pleistocene large mammal community. Palaeogeography, Palaeoclimatology, Palaeoecology, 266(1–2), 95–111.

    Article  Google Scholar 

  • Peigné, S., Goillot, C., Germonpré, M., Blondel, C., Bignon, O., & 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, 106(36), 15390–15393. doi:10.1073/pnas.0907373106.

    Article  Google Scholar 

  • Pierce, G. J., Hastie, L. C., Guerra, A., Thorpe, R. S., Howard, F. G., & Boyle, P. R. (1994). Morphometric variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fisheries Research, 21, 127–148.

    Article  Google Scholar 

  • Pilgrim, G. E. (1932). The fossil carnivora of India. Palaeontologia Indica, 18, 1–232.

    Google Scholar 

  • Pinto Llona, A. C. (2006). Comparative dental microwear analysis of cave bears Ursus spelaeus Rosenmüller, 1794 and brown bear Ursus arctos Linnaeus, 1758. Scientific Annals, School of Geology Aristotle University of Thessaloniki, 98, 103–108.

    Google Scholar 

  • Popowics, T. E. (2003). Postcanine dental form in the mustelidae and viverridae (Carnivora: Mammalia). Journal of Morphology, 256(3), 322–341. doi:10.1002/jmor.10091.

    Article  PubMed  Google Scholar 

  • Prevosti, F. J., Turazzini, G. F., Ercoli, M. D., & Hingst-Zaher, E. (2012). Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics. Zoological Journal of the Linnean Society, 164(4), 836–855. doi:10.1111/j.1096-3642.2011.00785.x.

    Article  Google Scholar 

  • Quilès, J. (2002). Les Ursidae du Pléistocène moyen et supérieur en Midi méditerranéen: Apports paléontologiques et archéozoologique. Ph. D. thesis, Muséum National d’Histoire Naturelle, Paris.

  • Quilès, J., Petrea, C., Moldovan, O., Zilhao, J., Rodrigo, R., Rougier, H., et al. (2006). Cave bears (Ursus spelaeus) from the Peştera cu Oase (Banat, Romania): paleobiology and taphonomy. Comptes Rendus Palevol, 5(8), 927–934. doi:10.1016/j.crpv.2006.09.005.

    Article  Google Scholar 

  • Rabal-Garcés, R., Cuenca-Bescos, G., Ignacio Canudo, J., & De Torres, T. (2012). Was the European cave bear an occasional scavenger? Lethaia, 45(1), 96–108. doi:10.1111/j.1502-3931.2011.00260.x.

    Article  Google Scholar 

  • Rabeder, G., & Hofreiter, M. (2004). Der neue Stammbaum der alpinen Höhlenbären. Die Höhle, 55(1–4), 58–77.

    Google Scholar 

  • Rabeder, G., Hofreiter, M., Nagel, D., & Withalm, G. (2004). New taxa of Alpine cave bears (Ursidae, Carnivora). Cahiers scientifiques Muséum Lyon, 2, 49–67.

    Google Scholar 

  • Rabeder, G., Debeljak, I., Hofreiter, M., & Withalm, G. (2008). Morphological responses of cave bears (Ursus spelaeus group) to high-alpine habitats. Die Höhle, 59(1–4), 59–72.

    Google Scholar 

  • Rabeder, G., Pacher, M., & Withalm, G. (2010). Early Pleistocene bear remains from Deutsch-Altenburg (Vol. 17). Wien: Verlag der Österreichischen Akademie der Wissenschaften.

    Google Scholar 

  • Raia, P. (2004). Morphological correlates of tough food consumption in large land carnivores. Italian Journal of Zoology, 71(1), 45–50.

    Article  Google Scholar 

  • Revell, L. J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    Article  Google Scholar 

  • Richards, M. P., Pacher, M., Stiller, M., Quilès, J., Hofreiter, M., Constantin, S., et al. (2008). Isotopic evidence for omnivory among European cave bears: Late Pleistocene Ursus spelaeus from the Peştera cu Oase, Romania. Proceedings of the National Academy of Sciences of the United States of America, 105(2), 600–604. doi:10.1073/pnas.0711063105.

  • Robu, M., Fortin, J. K., Richards, M. P., Schwartz, C. C., Wynn, J. G., Robbins, C. T., et al. (2013). Isotopic evidence for dietary flexibility among European Late Pleistocene cave bears (Ursus spelaeus). Canadian Journal of Zoology, 91(4), 227–234. doi:10.1139/cjz-2012-0222.

    Article  CAS  Google Scholar 

  • Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least squares to study covariation in shape. Systematic Biology, 49(4), 740–753.

    Article  CAS  PubMed  Google Scholar 

  • Rossi, M., & Santi, G. (2001). Archaic and recent Ursus spelaeus forms from Lombardy and Venetia Region (North Italy). Cadernos do Laboratorio Xeolóxico de Laxe, 26, 317–323.

    Google Scholar 

  • Sacco, T., & Van Valkenburgh, B. (2004). Ecomorphological indicators of feeding behaviour in the bears (Carnivora: Ursidae). Journal of Zoology, 263, 41–54.

    Article  Google Scholar 

  • Schmitz, L., & Motani, R. (2011). Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science, 332(6030), 705–708.

    Article  CAS  PubMed  Google Scholar 

  • Seetah, T. K., Cardini, A., & Miracle, P. T. (2012). Can morphospace shed light on cave bear spatial-temporal variation? Population dynamics of Ursus spelaeus from Romualdova pećina and Vindija, (Croatia). Journal of Archaeological Science, 39(2), 500–510.

    Article  Google Scholar 

  • Senshu, T., Ohya, A., Ide, K., Mikogai, J., Morita, M., Nakao, T., et al. (2007). Studies on the digestion in the Giant Panda, Ailuropoda melanoleuca, fed feedstuffs including bamboo. Mammal Study, 32(4), 139–149. doi:10.3106/1348-6160(2007)32[139:sotdit]2.0.co;2.

    Article  Google Scholar 

  • Slater, G. J., Dumont, E., & Van Valkenburgh, B. (2007). Implications of craniofacial form for performance of the canid skull during prey killing and feeding. Journal of Vertebrate Paleontology, 27(3), 148A–148A.

    Google Scholar 

  • Slater, G. J., Figueirido, B., Louis, L., Yang, P., & Van Valkenburgh, B. (2010). Biomechanical consequences of rapid evolution in the polar bear lineage. PLoS ONE, 5(11), e13870.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • SPSS Inc. (2009). PASW Statistics 17.0. (17.0.3 ed.). Chigago: SPSS Inc.

  • Stiller, M., Molak, M., Prost, S., Rabeder, G., Baryshnikov, G., Rosendahl, W., et al. (2014). Mitochondrial DNA diversity and evolution of the Pleistocene cave bear complex. Quaternary International, 339–340, 224–231.

    Article  Google Scholar 

  • Stiner, M. C., Achyuthan, H., Arsebuk, G., Howell, F. C., Josephson, S. C., Juell, K. E., et al. (1998). Reconstructing cave bear paleoecology from skeletons: a cross-disciplinary study of Middle Pleistocene bears from Yarimburgaz cave, Turkey. Paleobiology, 24(1), 74–98.

    Google Scholar 

  • Stirling, I., & Archibald, W. R. (1977). Aspects of predation of seals by polar bears. Journal of the Fisheries Research Board of Canada, 34(8), 1126–1129. doi:10.1139/f77-169.

    Article  Google Scholar 

  • Stynder, D. D., & Kupczik, K. (2013). Tooth root morphology in the early Pliocene African bear Agriotherium africanum (Mammalia, Carnivora, Ursidae) and its implications for feeding ecology. Journal of Mammalian Evolution, 20(3), 227–237.

    Article  Google Scholar 

  • Tagle, D. A., Miyamoto, M. M., Goodman, M., Hofmann, O., Braunitzer, G., Göltenboth, R., et al. (1986). Hemoglobin of pandas: phylogenetic relationships of carnivores as ascertained with protein sequence data. Naturwissenschaften, 73(8), 512–514.

    Article  CAS  PubMed  Google Scholar 

  • Talbot, S. L., & Shields, G. F. (1996). A phylogeny of the bears (Ursidae) inferred from complete sequences of three mitochondrial genes. Molecular Phylogenetics and Evolution, 5(3), 567–575. doi:10.1006/mpev.1996.0051.

    Article  CAS  PubMed  Google Scholar 

  • Therrien, F. (2005). Mandibular force profiles of extant carnivorans and implications for the feeding behaviour of extinct predators. Journal of Zoology, 267, 249–270.

    Article  Google Scholar 

  • Trajano, E., & Ferrarezzi, H. (1995). A fossil bear from northeastern Brazil, with a phylogenetic analysis of the South American extinct Tremarctinae (Ursidae). Journal of Vertebrate Paleontology, 14(4), 552–561. doi:10.1080/02724634.1995.10011577.

    Article  Google Scholar 

  • van Heteren, A. H., MacLarnon, A., Rae, T. C., & Soligo, C. (2009). Cave bears and their closest living relatives: a 3D geometric morphometrical approach to the functional morphology of the cave bear Ursus spelaeus. Slovenský Kras Acta Carsologica Slovaca, 47(supplement 1), 33–46.

    Google Scholar 

  • van Heteren, A. H., MacLarnon, A. M., Soligo, C., & Rae, T. C. (2012). 3D geometric morphometrical analyses of intraspecific variation in the mandible of Ursus spelaeus from the Alpine region. Braunschweiger Naturkundliche Schriften, 11, 111–128.

    Google Scholar 

  • van Heteren, A. H., MacLarnon, A. M., Soligo, C., & Rae, T. C. (2014). Functional morphology of the cave bear (Ursus spelaeus) cranium: a three-dimensional geometric morphometric analysis. Quaternary International, 339–340, 209–216.

    Article  Google Scholar 

  • Van Valkenburgh, B. (2007). Deja vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology, 47(1), 147–163.

    Article  PubMed  Google Scholar 

  • Van Valkenburgh, B., & Hertel, F. (1993). Tough times at La-Brea—tooth breakage in large carnivores of the Late Pleistocene. Science, 261(5120), 456–459.

    Article  Google Scholar 

  • Werdelin, L. (1989). Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia, Canidae). Paleobiology, 15(4), 387–401.

    Google Scholar 

  • Werdelin, L., & Solounias, N. (1991). The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata, 30, 1–104.

    Google Scholar 

  • Wong, S. T. (2002). The ecology of Malayan sun bears (Helarctos malayanus) in the lowland tropical rainforest of Sabah, Malaysian Borneo. M. Sc. thesis, University of Montana, Montana.

  • Wozencraft, W. C. (1989). Phylogeny of the recent carnivora. In J. L. Gittleman (Ed.), Carnivore behaviour, ecology and evolution (pp. 495–535). London: Chapman and Hall.

    Chapter  Google Scholar 

  • Yoganand, K., Rice, C. G., & Johnsing, A. J. T. (2012). Sloth bear. In A. J. T. Johnsing & N. Manjrekar (Eds.), Mammals of South Asia (Vol. 1, pp. 328–456). Telangana: Orient Blackswan.

    Google Scholar 

  • Zhang, Y.-P., & Shi, L.-M. (1991). Riddle of the giant panda. Nature, 352(6336), 573–573. doi:10.1038/352573a0.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Specimens were studied in the following museums: Haus der Natur, Salzburg, Austria; Musée de Préhistoire de Tautavel; Museum für Naturkunde, Leibnitz-Institut für Evolutions- und Biodiversitätsforschung and der Humboldt Universtität, Berlin, Germany; Landesmuseum Joanneum, Graz, Austria; Museum of Zoology and Natural History “La Specola”, Firenze, Italy; Natural History Museum, London, United Kingdom; Natural History Museum, University of Oslo, Oslo, Norway; Naturhistorisches Museum Wien, Vienna, Austria; Royal Belgian Institute of Natural Sciences, Brussels, Belgium; Staatliches Museum für Naturkunde Stuttgart, Museum am Löwentor, Germany; Universität Tübingen, Tübingen, Germany; Universität Wien, Vienna, Austria; Université de Liège, Liège, Belgium. The authors would like to thank the curators at these institutions for granting permission to study the fossils. The authors are also grateful to G. Rabeder, E. Heiss and two anonymous reviewers for helpful comments on earlier versions of this manuscript, as well as C. Meloro and J. Smaers for advice on statistics. This research received support from the SYNTHESYS Project http://www.synthesys.info/ which is financed by European Community Research Infrastructure Action under the FP6 ‘Structuring the European Research Area’ Programme. This research was partly funded by internal grant 37913 and a 3-year bursary from the University of Roehampton.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anneke H. van Heteren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Information 1

List of specimens used in the analyses. (PDF 285 kb)

Supplementary Information 2

Statistics pertaining to the allometric correction. (PDF 337 kb)

Supplementary Information 3

Form spaces. (PDF 351 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van Heteren, A.H., MacLarnon, A., Soligo, C. et al. Functional morphology of the cave bear (Ursus spelaeus) mandible: a 3D geometric morphometric analysis. Org Divers Evol 16, 299–314 (2016). https://doi.org/10.1007/s13127-015-0238-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-015-0238-2

Keywords

Navigation