A three-dimensional analysis of tooth-root morphology in living bears and implications for feeding behaviour in the extinct cave bear

References

• Abel O, Kyrle G. 1931. Die Drachenhöhle bei Mixnitz. Speläol Monogr. 7–9. 953pp. Wien.
   Google Scholar
• Andrews P, Turner A. 1992. Life and death of the Westbury bears. Ann Zool Fennici. 28(3–4):139–149.
   Web of Science ®Google Scholar
• Astúa D. 2009. Evolution of scapula size and shape in didelphid marsupials (Didelphimorphia: Didelphidae). Evolution. 63(9):2438–2456.
   PubMed Web of Science ®Google Scholar
• Bocherens H, Drucker DG, Billiou D, Geneste JM, Van Der Plicht J. 2006. Bears and Humans in Chauvet Cave (Vallon-Pont-d’Arc. Ardèche France): insights stable isotopes radiocarbon dating bone collagen. J Hum Evol. 50(3):370-376.
   Google Scholar
• Bocherens H, Stiller M, Hobson KA, Pacher M, Rabeder G, Burns JA, Hofreiter M 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. Quatern Int. 245(2):238–248.
   Web of Science ®Google Scholar
• Bocherens H. 2018. Isotopic insights on cave bear palaeodiet. Hist Bio. doi:10.1080/08912963.2018.1465419
   PubMed Web of Science ®Google Scholar
• Bocherens H, Billiou D, Patou-Mathis M, Otte M, Bonjean D, Toussaint M, Mariotti A. 1999. Palaeoenvironmental and Palaeodietary Implications of Isotopic Biogeochemistry of Late Interglacial Neandertal and Mammal Bones in Scladina Cave (Belgium). J Archaeol Sci. 26:599–607.
   Web of Science ®Google Scholar
• Bocherens H, Mariotti A. 1997. Comments on: Diet, physiology and ecology of fossil mammals as inferred from stable carbon and nitrogen isotope biochemistry: Implications for Pleistocene bears by Bocherenset al. -Repy Palaeogeogr Palaeocl 128:362–364.
   Google Scholar
• Christiansen P. 2008. Evolution of skull and mandible shape in cats (Carnivora: Felidae). PLoS One. 3(7):e2807.
   PubMed Web of Science ®Google Scholar
• Christiansen P, Wroe S. 2007. Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology. 88(2):347–358.
   PubMed Web of Science ®Google Scholar
• DeMaster DP, Stirling I. 1981. Ursus maritimus. Polar bear. Mamm Sp. 145:1–7.
   Google Scholar
• Derocher AE, Andersen M, Wiig Ø, Aars J. 2010. Sexual dimorphism and the mating ecology of polar bears (Ursus maritimus) at Svalbard. Behav Ecol Sociobiol. 64(6):939-946.
   Google Scholar
• Diedrich CG. 2012. An Ice Age spotted hyena Crocuta crocuta spelaea (Goldfuss 1823) population, their excrements and prey from the late Pleistocene hyena den of the Sloup Cave in the Moravian Karst, Czech Republic. Hist Biol. 24(2):161–185.
   Web of Science ®Google Scholar
• Döppes D, Pacher M, Rabeder G, Lindauer S, Freidrich R, Kromer B, Rosendahl W. 2016. Unexpected! New AMS dating from Austrian cave bear sites. Cranium. 33:26–30.
   Google Scholar
• Döppes D, Rabeder G, Frischauf C, Kavcik-Graumann N, Kromer B, Lindauer S, Friedrich R, Rosendahl W. 2018. Extinction pattern of Alpine cave bears - new data and climatological interpretation. Hist Biol. doi:10.1080/08912963.2018.1487422
   PubMed Web of Science ®Google Scholar
• Döppes D, Rabeder G, Stiller M. 2011. Was the Middle Würmian in the High Alps warmer than today? Quatern Int. 245(2):193–200.
   Web of Science ®Google Scholar
• Döppes D, Rosendahl W. 2009. Numerically dated palaeontological cave sites of Alpine region from Late Middle Pleistocene to Early Late Pleistocene. Preistoria Alpina. 44:45–48.
   Google Scholar
• Ehrenberg K. 1929. Die Ergebnisse der Ausgrabungen in der Schreiberwandhöhle am Dachstein. Paläont Z. 11(3):261–268.
   Google Scholar
• Figueirido B, Palmqvist P, Pérez-Claros JA. 2009. Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: An approach based on geometric morphometrics. J Zool. 277:70–80.
   Web of Science ®Google Scholar
• Figueirido B, Serrano-Alarcón FJ, Slater GJ, Palmqvist P. 2010. Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory. J Evolution Biol. 23(12):2579–2594.
   PubMed Web of Science ®Google Scholar
• Figueirido B, Soibelzon LH. 2010. Inferring palaeoecology in extinct tremarctine bears (Carnivora, Ursidae) using geometric morphometrics. Lethaia. 43(2):209–222.
   Web of Science ®Google Scholar
• Figueirido B, Tseng ZJ, Martín-Serra A. 2013. Skull shape evolution in durophagous carnivorans. Evolution. 67(7):1975–1993.
   PubMed Web of Science ®Google Scholar
• Fortes GG, Grandal-d’Anglade A, Kolbe B, Fernandes D, Meleg IN, García-Vázquez A, Frischauf C. 2016. Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears. Mol Ecol. 25(19):4907–4918.
   PubMed Web of Science ®Google Scholar
• Frischauf C, Liedl P, Rabeder G. 2014. Revision der fossilen Fauna der Drachenhöhle (Mixnitz, Steiermark). Die Höhle. 66(1–4):47–55.
   Google Scholar
• García N, Arsuaga JL, Torres T. 1997. The carnivore remains from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain). J Hum Evol. 33(2–3):155–174.
   PubMed Web of Science ®Google Scholar
• García N, Santos E, Arsuaga JL, Carretero JM. 2006. High-resolution X-ray computed tomography applied to the study of some endocranial traits in cave and brown bears. Scientific Annals School of Geology Aristotle University of Thessaloniki. 98:(141–146):141.
   Google Scholar
• Gidaszewski NA, Baylac M, Klingenberg CP. 2009. Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evol Biol. 9(1):110.
   PubMedGoogle Scholar
• Grandal-d’Anglade A, López-González F. 2005. Sexual dimorphism and ontogenetic variation in the skull of the cave bear (Ursus spelaeus Rosenmüller) of the European Upper Pleistocene. Geobios. 38(3):325-337.
   Web of Science ®Google Scholar
• Grandal-d’Anglade A. 2010. Bite force of the extinct Pleistocene Cave bear Ursus spelaeus Rosenmüller from Europe. Comptes Rendus Palevol. 9(1–2):31-37.
   Web of Science ®Google Scholar
• Grandal-d’Anglade A, Pérez-Rama M, García-Vázquez A, González-Fortes GM. 2018. The cave bear’s hibernation: reconstructing the physiology and behaviour of an extinct animal. Hist Biol. doi:10.1080/08912963.2018.1468441
   PubMed Web of Science ®Google Scholar
• Hofreiter M, Münzel S, Conard N, Pollack J, Weiss G, Pääbo S. 2007. Sudden replacement of cave bear mitochondrial DNA in the Late Pleistocene. Curr Biol. 17(4):R122–R123.
   Web of Science ®Google Scholar
• Hofreiter M, Rabeder G, Jaenicke V, Withalm G, Nagel D, Paunovic M, Jambrsi G, Pääbo S. 2004. Evidence for reproductive isolation between cave bear populations. Curr Biol 14(1):40–43.
   PubMed Web of Science ®Google Scholar
• Horacek M, Frischauf C, Pacher M, Rabeder G. 2012. Stable isotopic analyses of cave bear bones from the Conturines cave (2800 m, South Tyrol, Italy). Braunschweiger Naturkundliche Schriften. 11(1):47–52.
   Google Scholar
• Kadlec J, Hercman H, Beneš V, Šroubek P, J F D, Granger D. 2001. Cenozoic history of the Moravian Karst (northern segment): cave sediments and karst morphology. Acta Mus Moraviae Sci geol. 86:111–160.
   Google Scholar
• Ø H, Harper DAT, Ryan PD. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron. 4:9.
   Google Scholar
• Kavcik-Graumann N, Nagel D, Rabeder G, Ridush B, Withalm G 2016. The bears of Illinka cave near Odessa (Ukraine). In: Cranium. ICBS Proceedings. 1–25.
   Google Scholar
• Kikinis R, Pieper SD, Vosburgh K. 2014. 3D Slicer: a platform for subject-specific image analysis. visualization. and clinical support. Intraoperative Imaging Image-Guided Therapy. Ferenc A Jolesz Editor. 3(19):277–289.
   Google Scholar
• Klingenberg CP, Gidaszewski NA. 2010. Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biol. 59(3):245–261.
   PubMed Web of Science ®Google Scholar
• Knapp M. 2018. From a molecules’ perspective – contributions of ancient DNA research to understanding cave bear biology. Hist Bio. doi:10.1080/08912963.2018.1434168
   PubMed Web of Science ®Google Scholar
• Knapp M, Rohland N, Weinstock J, Baryshnikov G, Sher A, Nagel D, Hofreiter M. 2009. First DNA sequences from Asian cave bear fossils reveal deep divergences and complex phylogeographic patterns. Mol Ecol. 18(6):1225-1238.
   PubMed Web of Science ®Google Scholar
• Krause J, Unger T, Noçon A, Malaspinas AS, Kolokotronis SO, Stiller MBray SC. 2008. Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. BMC Evol Biol. 8(1):220.
   PubMedGoogle Scholar
• Kupczik K, Dean MC. 2008. Comparative observations on the tooth root morphology of Gigantopithecus blacki. J Hum Evol. 54(2):196–204.
   PubMed Web of Science ®Google Scholar
• Kupczik K, Hublin JJ. 2010. Mandibular molar root morphology in Neanderthals and Late Pleistocene and recent Homo sapiens. J Hum Evol. 59(5):525–541.
   PubMed Web of Science ®Google Scholar
• Kupczik K, Stynder DD. 2012. Tooth root morphology as an indicator for dietary specialisation in carnivores (Mammalia: Carnivora). Biol J Linn Soc. 105(2):456–471.
   Web of Science ®Google Scholar
• Kurtén B. 1955. Sex dimorphism and size trends in the cave bear, Ursus spelaeus Rosenmüller and Heinroth. Acta Zool. Fennica. 90:1-48.
   Google Scholar
• Kurtén B. 1967. Pleistocene bears of North America. II: Genus Arctodus. short-faced bears. Acta Zool. Fennica. 117:1–60.
   Google Scholar
• Maddison WP. 1991. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Systematic Biology. 40(3):304–314.
   Google Scholar
• Maddison WP, Maddison DR. 2018. Mesquite: a modular system for evolutionary analysis. Version 3.51 http://www.mesquiteproject.org.
   Google Scholar
• Martín-Serra A, Figueirido B, Palmqvist P. 2014a. A three-dimensional analysis of morphological evolution and locomotor performance of the carnivoran forelimb. PLoS One. 9(1):e85574.
   PubMed Web of Science ®Google Scholar
• Martín-Serra A, Figueirido B, Palmqvist P. 2014b. A three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb. BMC Evol Biol. 14(1):129.
   PubMedGoogle Scholar
• Mattson DJ. 1998. Diet and morphology of extant and recently extinct northern bears. Ursus. 10:479–496.
   Google Scholar
• Nagel D, Lindenbauer J, Kavcik-Graumann N, Rabeder G. 2018 (in press). Subtropical steppe inhabitants in the Late Pleistocene cave faunas of eastern Middle Europe. Slovensk: Kras -Acta Carsologica Slovaka.
   Google Scholar
• Pacher M, Stuart AJ. 2009. Extinction chronology and palaeobiology of the cave bear (Ursus spelaeus). Boreas. 38(2):189-206.
   Google Scholar
• Peigné S, Merceron G. 2017. Palaeoecology of cave bears as evidenced by dental wear analysis: a review of methods and recent findings. Hist Biol. 1–13.
   Web of Science ®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. P Natl Acad Sci. 106(36):15390-15393.
   Google Scholar
• Pérez-Rama M, Fernández-Mosquera D, Grandal-d’Anglade A. 2011. Effects of hibernation on the stable isotope signatures of adult and neonate cave bears. Quaternaire. 4:79–88.
   Google Scholar
• Pinto Llona AC, Andrews PJ, Etxebarría F. 2005. Taphonomy and Palaeoecology of Quaternary Bears from Cantabrian Spain. Oviedo: Fundación Oso de Asturias.
   Google Scholar
• Polly PD, MacLeod N. 2008. Locomotion in fossil Carnivora: an application of eigensurface analysis for morphometric comparison of 3D surfaces. Palaeontol Electron. 11(2):10–13.
   Web of Science ®Google Scholar
• Quilès J, Petrea C, Moldovan O, Zilhão J, Rodrigo R, Rougier H, Trinkaus E. 2006. Cave bears (Ursus spelaeus) from the Peştera cu Oase (Banat, Romania): Paleobiology and taphonomy. C R Palevol. 5(8):927-934.
   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. 59:59–72.
   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. 2004a. New taxa of alpine cave bears (Ursidae, Carnivora). Cahiers scientifiques Hors série. 2:49–67.
   Google Scholar
• Rabeder G, Hofreiter M, Withalm G. 2004b. The Systematic Position of the Cave Bear from Potočka zijalka (Slovenia). Mitt Komm Quartärforsch Österr Akad. Wiss.13:197–200.
   Google Scholar
• Richards MP, Pacher M, Stiller M, Quilès J, Hofreiter M, Constantin S, Trinkaus E. 2008. Isotopic evidence for omnivory among European cave bears: Late Pleistocene Ursus spelaeus from the Peştera cu Oase, Romania. Proc Natl Acad Sci. 105(2):600-604.
   Google Scholar
• Robu M, Wynn JG, Mirea IC, Petculescu A, Kenesz M, Puşcaş CM, Vlaicu M, Trinkaus E, Constantin S, O’Regan H. 2018. The diverse dietary profiles of MIS 3 cave bears from the Romanian Carpathians: insights from stable isotope (δ13C and δ15N) analysis. Palaeontology. 61:209–219.
   Web of Science ®Google Scholar
• Sacco T, Van Valkenburgh B. 2004. Ecomorphological indicators of feeding behaviour in the bears (Carnivora: Ursidae). J Zoo. 263(1):41–54.
   Google Scholar
• Schulz E, Piotrowski V, Clauss M, Mau M, Merceron G, Kaiser TM. 2013. Dietary Abrasiveness Is Associated with Variability of Microwear and Dental Surface Texture in Rabbits. PLoS ONE. 8(2):e56167.
   PubMed Web of Science ®Google Scholar
• Self CJ. 2015a. Dental root size in bats with diets of different hardness. J Morphol. 276(9):1065–1074.
   PubMed Web of Science ®Google Scholar
• Self CJ. 2015b. Cricetid rodents: Is molar root morphology an indicator of diet?. Zoomorphology. 134(2):309–316.
   Web of Science ®Google Scholar
• Spencer MA. 2003. Tooth-root form and function in platyrrhine seed-eaters. Am J Phys Anthropol.122. (4):325–335.
   PubMed Web of Science ®Google Scholar
• Spötl C, Reimer PJ, Rabeder G, Ramsey CB. 2018. Radiocarbon constraints on the age of the world’s highest-elevation cave-bear population, Conturines Cave (Dolomites, Northern Italy). Radiocarbon. 60(1):299–307.
   Web of Science ®Google Scholar
• Stiller M, Molak M, Prost S, Rabeder G, Baryshnikov G, Rosendahl W, Germonpré M. 2014. Mitochondrial DNA diversity and evolution of the Pleistocene cave bear complex. Quatern Int. 339:224-231.
   Web of Science ®Google Scholar
• Stynder DD, Kupczik K. 2013. Tooth root morphology in the early Pliocene African bear Agriotherium africanum (Mammalia. Carnivora. Ursidae) and its implications for feeding ecology. J Mammal Evol. 20(3):227–237.
   Web of Science ®Google Scholar
• Terlato G, Bocherens H, Romandini M, Nannini N, Hobson KA, Peresani M. 2018. Chronological and Isotopic data support a revision for the timing of cave bear extinction in Mediterranean Europe. Hist Bio. doi:10.1080/08912963.2018.1448395
   PubMed Web of Science ®Google Scholar
• Thomason JJ. 1991. Cranial strength in relation to estimated biting forces in some mammals. Can J Zool. 69:2326–2333.
   Web of Science ®Google Scholar
• Van Heteren AH, Arlegi M, Santos E, Arsuaga JL, Gómez-Olivencia A. 2018. Cranial and mandibular morphology of Middle Pleistocene cave bears (Ursus deningeri): implications for diet and evolution. Historical Biology. doi:10.1080/08912963.2018.1487965
   PubMed Web of Science ®Google Scholar
• Van Heteren AH, MacLarnon A, Rae TC, 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(supplement1):33–46.
   Google Scholar
• Van Heteren AH, MacLarnon AM, Soligo C, Rae TC. 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 AH, MacLarnon AM, Soligo C, Rae TC. 2014. Functional morphology of the cave bear (Ursus spelaeus) cranium: a three-dimensional geometric morphometric analysis. Quatern Int. 339–340:209–216.
   Web of Science ®Google Scholar
• Van Heteren AH, MacLarnon AM, Soligo C, Rae TC. 2016. Functional morphology of the cave bear (Ursus spelaeus) mandible: a 3D geometric morphometric analysis. Org Divers Evol. 16:299–314.
   Web of Science ®Google Scholar
• Veitschegger K, Kolb C, Amson E, Sánchez-Villagra MR. 2018. Longevity and life history of cave bears – a review and novel data from tooth cementum and relative emergence of permanent dentition. Hist Bio. doi:10.1080/08912963.2018.1441293
   PubMed Web of Science ®Google Scholar
• Vila Taboada M, Fernández Mosquera D, López González F, Grandal D’Anglade A, Vidal Romaní JR. 1999. Paleoecological implications inferred from stable isotopic signatures (d13C. d15N) in bone collagen of Ursu spelaus ROS.-HEIN. Cadernos do Laboratori Xeolxic deLax. 24:73–87.
   Google Scholar
• Wong ST. 2002. Food habits of malayan sun bears in lowland tropical forest of Borneo. Ursus. 13:127–136.
   Web of Science ®Google Scholar
• Xia J, Zheng J, Huang D, Tian ZR, Chen L, Zhou Z, Qian L. 2015. New model to explain tooth wear with implications for microwear formation and diet reconstruction. Proc Natl Acad Sci. 112(34):10669-10672.
   Google Scholar
• Yuan B, Khechoyan D, Goldman R 2015. A new objective automatic computational framework for evaluating and visualizing the results of infant cranial surgery. Paper presented at: ASE International Conference on Biomedical Computing., Dec. 14–16; Harvard University, Cambridge, USA.
   Google Scholar