The interplay between increased tooth crown-height and chewing efficiency, and implications for Cervidae evolution

Lethaia

Volumn 49, Issue 1, 2016, Pages 117-129

  Demiguel, Daniel ^a   Azanza, Beatriz ^b   Cegoñino, José ^c   Ruiz, Inmaculada ^c   Morales, Jorge ^d  

^a INSTITUT CATALÀ DE PALEONTOLOGIA MIQUEL CRUSAFONT   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c UNIVERSITY OF ZARAGOZA   (Spain)

^d MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Biomechanics; Evolution; Finite Element Analysis; Fossil ruminants; Hypsodonty; Paleoecology

Indexed keywords

BIOMECHANICS; DEER; DIGESTION; EVOLUTION; FINITE ELEMENT METHOD; MORPHOLOGY; PALEOECOLOGY; PHENOTYPE; TOOTH;

CERVIDAE; MAMMALIA;

EID: 84956847739     PISSN: 00241164     EISSN: 15023931     Source Type: Journal    
DOI: 10.1111/let.12139     Document Type: Article

References (67)

1. Anusavice, K.J. & Tsai, Y.L. 1997: Stress distribution in ceramic crown forms as a function of thickness, elastic modulus, and supporting substrate. In Bumgardner, D. & Puckett, A.D. (eds): Proceedings of the Sixteenth Southern Biomedical Engineering Conference. Biloxi, MS, 264-267.
2. Axmacher, H. & Hofmann, R.R. 1988: Morphological characteristics of the masseter muscle of 22 ruminant species. Journal of Zoology 215, 463-473.
3. Cantalapiedra, J.L., Alcalde, G.M. & Hernández Fernández, M. 2014a: The contribution of phylogenetics to the study of ruminant evolutionary ecology. Zittleiana B 32, 1-6.
4. Cantalapiedra, J.L., FitzJohn, R.G., Kuhn, T.S., Hernández Fernández, M., DeMiguel, D., Azanza, B., Morales, J. & Mooers, A.Ø. 2014b: Dietary innovations spurred the diversification of ruminants during the Cenozoic. Proceedings of the Royal Society B 281, 20132746.
5. Clauss, M. 2013: Digestive physiology and feeding behaviour of equids - a comparative approach. In Horse Health Nutrition - European Equine Health & Nutrition Congress. Gent, Belgium, 25-33.
6. Clauss, M., Frey, R., Kiefer, B., Lechner-Doll, M., Loehlein, W., Polster, C., Rössner, G.E. & Streich, W.J. 2003: The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136, 14-27.
7. Clauss, M., Nunn, C., Fritz, J. & Hummel, J. 2009: Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 154, 376-382.
8. Codron, D., Lee-Thorp, J.A., Sponheimer, M. & Codron, J. 2007: Nutritional content of savanna plant foods: implications for browse/grazer models of ungulate diversification. European Journal of Wildlife Research 53, 100-111.
9. Crompton, A.W. & Hiiemae, K.M. 1970: Molar occlusion and mandibular movements during occlusion Didelphis marsupialis. Zoological Journal of the Linnean Society 49, 21-47.
10. Damuth, J. & Janis, C.M. 2005: Paleoecological inferences using tooth wear rates, hypsodonty and life history in ungulates. Journal of Vertebrate Paleontology 25(suppl), 49A.
11. Damuth, J. & Janis, C.M. 2011: On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biological Reviews 86, 733-758.
12. DeMiguel, D., Cegoñino, J., Azanza, B., Ruíz, I. & Morales, J. 2006: Aplicación del análisis 3D de elementos finitos en el estudio biomecánico de la dentición de mamíferos. Análisis preliminar en Procervulus ginsburgi (Cervidae, Artiodactyla). Estudios Geológicos 62, 115-122.
13. DeMiguel, D., Fortelius, M., Azanza, B. & Morales, J. 2008: Ancestral feeding state of ruminants reconsidered: earliest grazing adaptation claims a mixed condition for Cervidae. BMC Evolutionary Biology 8, 1-13.
14. DeMiguel, D., Azanza, B. & Morales, J. 2010: Trophic flexibility within the oldest Cervidae lineage to persist through the Miocene Climatic Optimum. Palaeogeography, Palaeoclimatology, Palaeoecology 289, 81-92.
15. DeMiguel, D., Azanza, B. & Morales, J. 2011: Paleoenvironments and paleoclimate of the Middle Miocene of central Spain: a reconstruction from dental wear of ruminants. Palaeogeography, Palaeoclimatology, Palaeoecology 302, 452-463.
16. DeMiguel, D., Azanza, B. & Morales, J. 2014: Key innovations in ruminant evolution: a paleontological perspective. Integrative Zoology 9, 412-433.
17. Dumont, E.R., Piccirillo, J. & Grosse, I.R. 2005: Finite-element analysis of bitting behavior and bone stress in the facial skeletons of bats. The Anatomical Record 283A, 319-330.
18. Dumont, E.R., Grosse, I.R. & Slater, G.J. 2009: Requirements for comparing the performance of finite element models of biological structures. Journal of Theoretical Biology 256, 96-103.
19. Eronen, J.T., Evans, A.R., Fortelius, M. & Jernvall, J. 2010: The impact of regional climate on the evolution of mammals: a case study using fossil horses. Evolution 64, 398-408.
20. Fortelius, M. 1985: Ungulate cheek teeth: developmental, functional and evolutionary interrelations. Acta Zoologica Fennica 180, 1-76.
21. Fortelius, M. & Solounias, N. 2000: Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets. American Museum Novitates 3301, 1-35.
22. Fritz, J., Hummel, J., Kienzle, E., Arnold, C., Nunn, C. & Clauss, M. 2009: Comparative chewing efficiency in mammalian herbivores. Oikos 118, 1623-1632.
23. Hautier, L., Clavel, J., Lazzari, V., Gomes Rodrigues, H. & Vianey-Liaud, M. 2010: Biomechanical changes and remodelling of the masticatory apparatus during mammalian evolution: the case of the Issiodoromyinae (Rodentia). Palaios 25, 6-13.
24. Heywood, J. 2010: Explaining patterns in modern ruminant diversity: contingency or constraint? Biological Journal of the Linnean Society 99, 657-672.
25. Janis, C.M. 1976: The evolutionary strategy of the Equidae and the origin of rumen and cecal digestion. Evolution 30, 757-774.
26. Janis, C.M. 1979: Mastication in the hyrax and its relevance to ungulate dental evolution. Paleobiology 5, 50-59.
27. Janis, C.M. 1988: An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preferences. Mémoirs de Musée d'Histoire naturelle, Paris (serie C) 53, 367-387.
28. Janis, C.M. 2008: An evolutionary history of browsing and grazing ungulates. In Gordon, I.J. & Prins, H.H.T. (eds): The Ecology of Browsing and Grazing, 21-45. Springer, Berlin/Heidelberg.
29. Janis, C.M. & Fortelius, M. 1988: On the means whereby mammals achieve increased functional durability of their dentitions, with special reference to limiting factors. Biology Reviews 63, 197-230.
30. Janis, C.M., Constable, E.C., Houpt, K.A., Streich, W.J. & Clauss, M. 2010: Comparative ingestive mastication in domestic horses and cattle: a pilot investigation. Journal of Animal Physiology and Animal Nutrition 94, 402-409.
31. Jardine, P.E., Janis, C.M., Sahney, S. & Benton, M.J. 2012: Grit not grass: concordant patterns of early origin of hypsodonty in Great Plains ungulates and Glires. Palaeogeography, Palaeoclimatology, Palaeoecology 365-366, 1-10.
32. Jordana, X., Marín-Moratalla, N., DeMiguel, D., Kaiser, T.M. & Köhler, M. 2012: Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proceedings of the Royal Society B 279, 3339-3346.
33. Kaiser, T.M. & Rössner, G.E. 2007: Dietary resource partitioning in ruminant communities of Miocene wetland and karst palaeoenvironments in Southern Germany. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 424-439.
34. Kupczik, K., Dobson, C.A., Fagan, M.J., Crompton, R.H., Oxnard, C.E. & O'Higgins, P. 2007: Assessing mechanical function of the zygomatic region in macaques: validation and sensitivity testing of finite element models. Journal of Anatomy 210, 41-53.
35. Lin, C.P. & Douglas, W.H. 1994: Structure-property relations and crack resistance at the bovine dentin-enamel junction. Journal of Dental Research 73, 1072-1078.
36. Lucas, P.W. 2004: Dental Functional Morphology. Cambridge University Press, Cambridge, UK.
37. Lucas, P.W., Turner, I.M., Dominy, N.J. & Yamashita, N. 2000: Mechanical defenses to herbivory. Annals of Botany 86, 913-920.
38. MacFadden, B.J. 1997: Origin and evolution of the grazing guild in New World terrestrial mammals. Trends in Ecology and Evolution 12, 182-187.
39. MacFadden, B.J. 2000: Origin and evolution of the grazing guild in Cenozoic New World terrestrial mammals. In Sues, H.-D. (ed.): Evolution of Herbivory in Terrestrial Vertebrates. Cambridge University Press, Cambridge, UK, 223-244.
40. MacFadden, B.J. & Cerling, T.E. 1994: Fossil horses, carbon isotopes and global change. Trends in Ecology and Evolution 9, 481-486.
41. McNaughton, S.J., Tarrants, J.L., McNaughton, M.M. & Davis, R.D. 1985: Silica as a defense against herbivory and a growth promotor in African grasses. Ecology 66, 528-535.
42. Mihlbachler, M.C., Rivals, F., Solounias, N. & Semprebon, G.M. 2011: Dietary change and evolution of horses in North America. Science 331, 1178-1181.
43. Osborn, H.F. 1910: The Age of Mammals in Europe, Asia and North America. MacMillan, New York.
44. Owen-Smith, N. 1987: Pleistocene extinctions: the pivotal role of megaherbivores. Paleobiology 13, 351-362.
45. Pérez-Barbería, F.J. & Gordon, I.J. 1998: The influence of molar occlusal surface area on the voluntary intake, digestion, chewing behaviour and diet selection of red deer (Cervus elaphus). Journal of Zoology 245, 307-316.
46. Rayfield, E.J. 2007: Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annual Review of Earth and Planetary Sciences 35, 541-576.
47. Rayfield, E.J., Norman, D.B., Horner, C.C., Horner, J.R., Smith, P.M., Thomason, J.J. & Upchurch, P. 2001: Cranial design and function in a large theropod dinosaur. Nature 409, 1033-1037.
48. Richmond, B.G., Wright, B.W., Grosse, I., Dechow, P.C., Ross, C.F., Spencer, M.A. & Strait, D.S. 2005: Finite element analysis in functional morphology. Anatomical Record 283A, 259-274.
49. Robbins, C.T. 1993: Wildlife Feeding and Nutrition. Academic Press, New York.
50. Ross, C.F. 2005: Finite element analysis in vertebrate biomechanics. Anatomical Record 283A, 253-258.
51. Sanson, G.D. 2006: The biomechanics of browsing and grazing. American Journal of Botany 93, 1531-1545.
52. Sanson, G.D., Kerr, S.A. & Gross, K.A. 2007: Do silica phytoliths really wear mammalian teeth? Journal of Archaeological Science 34, 526-531.
53. Schwarm, A., Ortmann, S., Wolf, C., Streich, W.J. & Clauss, M. 2009: More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 152, 504-512.
54. Shipley, L.A. 1999: Grazers and browsers: how digestive morphology affects diet selection. In Launchbaugh, K.L., Sanders, K.D. & Mosley, J.C. (eds): Grazing Behaviour of Livestock and Wildlife. Idaho Forest, Wildlife and Range Expeditions Station Bulletin, University of Idaho, Moscow, 20-27.
55. Simpson, G.G. 1953: The Major Features of Evolution. Columbia University Press, New York.
56. Solounias, N. & Moelleken, S.M.C. 1994: Differences in diet between two archaic ruminant species from Sansan, France. Historical Biology 7, 203-220.
57. Stirton, R.A. 1947: Observation of evolutionary rates in hypsodonty. Evolution 1, 32-51.
58. Strait, D.S., Weber, G.W., Neubauer, S., Chalk, J., Richmond, B.G., Lucas, P.W., Spencer, M.A., Schrein, C., Dechow, P.C., Ross, C.F., Grosse, I., Wright, B.W., Constantino, P., Wood, B.A., Lawn, B., Hylander, W.L., Wang, Q., Byron, C., Slice, D.E. & Smith, A.L. 2009: The feeding biomechanics and dietary ecology of Australopithecus africanus. Proceedings of the National Academy of Sciences 106, 2124-2129.
59. Strait, D.S., Grosse, I.R., Dechow, P.C., Smith, A.L., Wang, Q., Weber, G.W., Neubauer, S., Slice, D.E., Chalk, J., Richmond, B.G., Lucas, P.W., Spencer, M.A., Schrein, C., Wright, B.W., Byron, C. & Ross, C.F. 2010: The structural rigidity of the cranium of Australopithecus africanus: implications for diet, dietary adaptations, and the allometry of feeding biomechanics. Anatomical Record 293, 583-593.
60. Strömberg, C.A. 2006: Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology 32, 236-258.
61. Thomason, J.J. 1991: Cranial strength in relation to estimated biting forces in some mammals. Canadian Journal of Zoology 69, 2326-2333.
62. Van Valen, L. 1960: A functional index of hypsodonty. Evolution 14, 531-532.
63. White, T.E. 1959: The endocrine glands and evolution. Os cementum, hypsodonty, and diet. Contributions from the Museum of Paleontology. University of Michigan, 13, 211-265.
64. Williams, S.H. & Kay, R.F. 2001: A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution 8, 207-229.
65. Wilson, J.R. & Hacker, J.B. 1987: Comparative digestibility and anatomy of some sympatric C3 and C4 arid zone grasses. Australian Journal of Agricultural Research 38, 287-295.
66. Wroe, S., Clausen, P., Mchenry, C., Moreno, K. & Cunningham, E. 2007: Computer simulation of feeding behavior in the thylacine and dingo as a novel test for convergence and niche overlap. Proceedings of the Royal Society B 274, 2819-2828.
67. Zienkiewicz, O.C. 1971: The Finite Element Method in Engineering Science. McGraw-Hill, London.