Journal of Mammalian Evolution

, Volume 23, Issue 4, pp 369–383 | Cite as

Morphology is not Destiny: Discrepancy between Form, Function and Dietary Adaptation in Bovid Cheek Teeth

  • Juan Pablo GailerEmail author
  • Ivan Calandra
  • Ellen Schulz-Kornas
  • Thomas M. Kaiser
Original Paper


Mammal teeth have evolved morphologies that allow for the efficient mechanical processing of different foods, therefore increasing dietary energy uptake for maintenance of high metabolic demands. However, individuals masticate foods with biomechanical properties at odds with the optimal function of a given tooth morphology. Here, we investigate tooth form and function using two quantitative 3D methods at different scales on the same individuals of nine bovid species. Dental topometry quantifies the gross morphology, and therefore, reflects evolutionary adaptive patterns. Surface texture analysis infers mechanical occlusal events, which reflect the actual tooth function, and is free from the influence of morphology. We found that tough foods can be satisfactorily exploited by grazing species with enamel ridge morphologies not more complex than those found in intermediate feeders and browsers. Thus, the evolution of enamel complexity is likely determined by a balance between adaptation and constraints. Wider enamel ridges seem to be a common functional trait in bovids to compensate for severe wear from abrasive foods and/or chipping from hard foods. Our results demonstrate that supposedly essential functional adaptations in tooth morphology may not be required to process food efficiently. This emphasizes the large plasticity between “optimal” morphology and the potential function of the tooth, and underscores the need to appreciate (apparently) maladaptive structures in mammalian evolution as nevertheless effective functioning units.


3D dental topometry Bovidae Dental evolution Feeding adaptation Surface texture analysis 



The authors thank all curators and technical assistants in the collections visited for this research for access to the specimens and permission to take moulds in their facilities. We are grateful to Gina Semprebon for the kind help of correcting the English of this manuscript. This research was sponsored by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation, KA 1525/8-1) and is publication no. 83 of the DFG Research Unit 771 “Function and performance enhancement in the mammalian dentition – phylogenetic and ontogenetic impact on the masticatory apparatus.”

Supplementary material

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  1. Anders U, Koenigswald W von, Ruf I, Smith BH (2011) Generalized individual dental age stages for fossil and extant placental mammals. Palaeontol Z 85:321–339Google Scholar
  2. Archer D, Sanson G (2002) Form and function of the selenodont molar in southern African ruminants in relation to their feeding habits. J Zool 257:13–26 doi:  10.1017/S0952836902000614 CrossRefGoogle Scholar
  3. Bengtsson H (2010) R.utils: Various Programming Utilities. Downloaded on 01.06.2010
  4. Bernor RL, Armour-Chelu M (1999) Towards an evolutionary history of African hipparionine horses. In: Bromage T, Schrenk F (eds) African Biogeography, Climate Change and Early Hominid Evolution. Oxford University Press, Oxford, pp 189–215Google Scholar
  5. Bibi F (2007) Dietary niche partitioning among fossil bovids in the late Miocene C3 habitats: consilience of functional morphology and stable isotope analysis. Palaeogeogr Palaeoclimatol Palaeoecol 253:529–538CrossRefGoogle Scholar
  6. Bibi F (2007) Origin, paleoecology, and paleobiogeography of early Bovini. Palaeogeogr Palaeoclimatol Palaeoecol 248:60–72CrossRefGoogle Scholar
  7. Bjorndal KA, Bolten AB, Moore JE (1990) Digestive fermentation in herbivores: effect of food particle size. Physiol Zool 63:710–721CrossRefGoogle Scholar
  8. Butler PM (1939) Studies of the mammalian dentition. - Differentiation of the postcanine dentition. Proc Zool Soc Lond B109:1–36CrossRefGoogle Scholar
  9. Calandra I, Schulz E, Pinnow M, Krohn S, Kaiser TM (2012) Teasing apart the contributions of hard items on 3D dental microtextures in primates. J Hum Evol 63:85–98CrossRefPubMedGoogle Scholar
  10. Cerling TE, Harris JM, Passey BH (2003) Diets of East African Bovidae based on stable isotope analysis. J Mammal 84:456–470CrossRefGoogle Scholar
  11. Clauss M, Kaiser T, Hummel J (2008) The morphophysiological adaptations of browsing and grazing mammals. In: Gordon IJ, Prins HHT (eds) The Ecology of Browsing and Grazing. Springer, Berlin Heidelberg, pp 47–88CrossRefGoogle Scholar
  12. Currie HA, Perry CC (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 100:1383–1389CrossRefPubMedPubMedCentralGoogle Scholar
  13. Damuth J, Janis CM (2011) On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biol Rev Cambridge Philos Soc 86:733–758 doi:  10.1111/j.1469-185X.2011.00176.x CrossRefPubMedGoogle Scholar
  14. Dunnett CW (1980) Pairwise multiple comparisons in the unequal variance case. J Am Statist Assoc 75:796–800CrossRefGoogle Scholar
  15. Estes RD (1991) The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates. Russel Friedmann, South AfricaGoogle Scholar
  16. Evans AR, Wilson GP, Fortelius M, Jernvall J (2007) High-level similarity of dentitions in carnivorans and rodents. Nature 445:78–81CrossRefPubMedGoogle Scholar
  17. Fortelius M (1985) Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zool Fenn 180:1–76Google Scholar
  18. Gagnon M, Chew AE (2000) Dietary preferences in extant African Bovidae. J Mammal 81:490–511CrossRefGoogle Scholar
  19. Gailer JP, Kaiser TM (2014) Common solutions to resolve different dietary challenges in the ruminant dentition: the functionality of bovid postcanine teeth as a masticatory unit. J Morphol 275:328–341CrossRefPubMedGoogle Scholar
  20. Gould SJ, Vrba ES (1982) Exaptation-a missing term in the science of form. Paleobiology 8:4–15CrossRefGoogle Scholar
  21. Greaves WS (1991) A relationship between premolar loss and jaw elongation in selenodont artiodactyls. Zool J Linn Soc 101:121–129CrossRefGoogle Scholar
  22. Harris JM, Leakey MG, Cerling TE (2003) Early Pliocene tetrapod remains from Kanapoi, Lake Turkana, Kenya. In: Harris JM, Leakey MG (eds) Geology and Vertebrate Paleontology of the Early Pliocene Site of Kanapoi, Northern Kenya. Natural History Museum of Los Angeles County, Los Angeles, pp 39–113Google Scholar
  23. Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen van Vuuren B, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335:32–50CrossRefPubMedGoogle Scholar
  24. Hernandez Fernandez M, Vrba ES (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev Cambridge Philos Soc 80:269–302CrossRefPubMedGoogle Scholar
  25. Heywood JJN (2010) Functional anatomy of bovid upper molar occlusal surfaces with respect to diet. J Zool 281:1–11CrossRefGoogle Scholar
  26. Hiiemae KM, Crompton AW (1985) Mastication, food transport, and swallowing. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional Vertebrate Morphology. The Belknap Press of Harvard University Press, Cambridge, pp 262–290Google Scholar
  27. Hillson S (2005) Teeth. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  28. Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96:1027–1046CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hofmann RR, Stewart DRM (1972) Grazer or browser: a classification based on the stomage structure and feeding habits of East African ruminants. Mammalia 36:226–240CrossRefGoogle Scholar
  30. Højsgaard S, Wright K, Leidi AA (2010) doBy: Groupwise Computations of Summary Statistics, General Linear Contrasts and Other Utilities. Downloaded on 01.06.2010
  31. Houte de Lange SM (1978) Zur Futterwahl des Alpensteinbockes (Capra Ibex L.). Z Jagdwiss 24:113–138 doi:  10.1007/bf01905544 Google Scholar
  32. International Organization for Standardization (2010) ISO/FDIS 25178–2 – Geometrical product specifications (GPS) – Surface texture: Areal – Part 2: Terms, definitions and surface texture parameters.Google Scholar
  33. Janis CM (1988) An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preference. In: Russell DE, Santoro J-P, Sigogneau-Russell D (eds) Teeth Revisited: Proceedings of the VIIth International Symposium on Dental Morphology, Paris, 1986. Mem Mus Natl Hist Nat Paris, pp 367–387Google Scholar
  34. Jardine PE, Janis CM, Sahney S, Benton MJ (2012) Grit not grass: concordant patterns of early origin of hypsodonty in Great Plains ungulates and Glires. Palaeogeogr Palaeoclimatol Palaeoecol 365–366:1–10CrossRefGoogle Scholar
  35. Jarman PJ (1971) Diets of large mammals in the woodlands around Lake Kariba, Rhodesia. Oecologia 8:157–178CrossRefGoogle Scholar
  36. Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48:215–266CrossRefGoogle Scholar
  37. Kaiser TM, Brinkmann G (2006) Measuring dental wear equilibriums — the use of industrial surface texture parameters to infer the diets of fossil mammals. Palaeogeogr Palaeoclimatol Palaeoecol 239:221–240CrossRefGoogle Scholar
  38. Kaiser TM, Clauss M, Schulz-Kornas E (2016) A set of hypotheses on tribology of mammalian herbivore teeth. Surf Topogr Metrol Prop 4:014003 doi:  10.1088/2051-672X/4/1/014003
  39. Kaiser TM, Fickel J, Streich WJ, Hummel J, Clauss M (2010) Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. J Zool 281:12–25Google Scholar
  40. Kaiser TM, Fortelius M (2003) Differential mesowear in occluding upper and lower molars: opening mesowear analysis for lower molars and premolars in hypsodont horses. J Morphol 258:67–83Google Scholar
  41. Kaufman PB, Dayanandan P, Takeoka Y, Bigelow JD, Jones JD, Iler R (1981) Silica in shots in higher plants. In: Simpson TL, Volcani BE (eds) Silicon and Siliceous Structures in Biological Systems. Springer-Verlag, New York, pp 409–449CrossRefGoogle Scholar
  42. Kavanagh KD, Evans AR, Jernvall J (2007) Predicting evolutionary patterns of mammalian teeth from development. Nature 449:427–432 doi:  10.1038/nature06153 CrossRefPubMedGoogle Scholar
  43. Kingdon J (2001) The Kingdon Field Guide to African Mammals. Academic Press, San DiegoGoogle Scholar
  44. Le Fur S, Fara E, Mackaye HT, Vignaud P, Brunet M (2009) The mammal assemblage of the hominid site TM266 (late Miocene, Chad Basin): ecological structure and paleoenvironmental implications. Naturwissenschaften 96:565–574 doi:  10.1007/s00114-008-0504-7 CrossRefPubMedGoogle Scholar
  45. Lent PC (1988) Ovibus moschatus. Mammal Species 302:1–9CrossRefGoogle Scholar
  46. Liem KF (1980) Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am Zool 20:295–314CrossRefGoogle Scholar
  47. Lucas PW (2004) Dental Functional Morphology: How Teeth Work. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  48. Lucas PW, Constantino PJ, Chalk J, Ziscovici C, Wright BW, Fragaszy DM., Hill DA, Lee JJ-W, Chai H, Darvell BW, Lee PKD, Yuen TDB (2009) Indentation as technique to assess the mechanical properties of fallback foods. Am J Phys Anthropol 140:643–652Google Scholar
  49. Lucas PW, Constantino P, Wood B, Lawn B (2008) Dental enamel as a dietary indicator in mammals. Bioessays 30:374–385Google Scholar
  50. Lucas PW, Turner IM, Dominy NJ, Yamashita N (2000) Mechanical defences to herbivory. Ann Bot 86:913–920 doi:  10.1006/anbo.2000.1261
  51. Luciani TJ (2009) RSvgDevice: An R SVG Graphics Device. Downloaded on 01.06.2010
  52. McKitrick MC (1993) Phylogenetic constraint in evolutionary theory: has it any explanatory power? Annu Rev Ecol Syst 24:307–330CrossRefGoogle Scholar
  53. Mendoza M, Palmqvist P (2008) Hypsodonty in ungulates: an adaptation for grass consumption or for foraging in open habitat? J Zool 274:134–142CrossRefGoogle Scholar
  54. Mihlbachler MC, Campbell D, Ayoub M, Chen C, Ghani I (2015) Comparative dental microwear of ruminant and perissodactyl molars: implications for paleodietary analysis of rare and extinct ungulate clades. Paleobiology FirstView:1–19 doi:  10.1017/pab.2015.33
  55. Moser BK, Stevens GR, Watts CL (1989) The Two-sample t Test versus Satterthwaite’s Approximate F Test. Commun Stat Theory 18:3963–3975CrossRefGoogle Scholar
  56. Oakes EJ, Harmsen R, Eberl C (1992) Sex, age, and seasonal differences in the diets and activity budgets of muskoxen (Ovibos moschatus). Can J Zool 70:605–616CrossRefGoogle Scholar
  57. Pampush JD, Duque AC, Burrows BR, Daegling DJ, Kenney WF, McGraw WS (2013) Homoplasy and thick enamel in primates. J Hum Evol 64:216–224CrossRefPubMedGoogle Scholar
  58. Pérez-Barbería FJ, Elston DA, Gordon IJ, Illius AW (2004) The evolution of phylogenetic differences in the efficiency of digestion in ruminants. Proc Zool Soc Lond B271:1081–1090Google Scholar
  59. Pérez-Barbería FJ, Gordon IJ (1998) Factors affecting food comminution during chewing in ruminants: a review. Biol J Linn Soc 63:233–256CrossRefGoogle Scholar
  60. Pérez-Barbería FJ, Gordon IJ (1999) The functional relationship between feeding type and jaw and cranial morphology in ungulates. Oecologia 118:157–165CrossRefGoogle Scholar
  61. Pérez-Barbería FJ, Gordon IJ (2001) Relationships between oral morphology and feeding style in the Ungulata: a phylogenetically controlled evaluation. Proc Zool Soc Lond B268:1023–1032CrossRefGoogle Scholar
  62. Pond KR, Ellis WC, Akin DE (1984) Ingestive mastication and fragmentation of forages. J Anim Sci 58:1567–1574CrossRefGoogle Scholar
  63. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Downloaded on 28.04.2010
  64. Rensberger JM (1973) An occlusion model for mastication and dental wear in herbivorous mammals. J Paleontol 47:515–528Google Scholar
  65. Richmond KE, Sussman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr Opin Plant Biol 6:268–272CrossRefPubMedGoogle Scholar
  66. Robinson BW, Wilson DS (1998) Optimal foraging, specialization, and a solution to Liem’s paradox. Am Nat 151:223–235 doi: 10.1086/286113 CrossRefPubMedGoogle Scholar
  67. Salazar-Ciudad I, Jernvall J (2004) How different types of pattern formation mechanisms affect the evolution of form and development. Evol Dev 6:6–16CrossRefPubMedGoogle Scholar
  68. Salazar-Ciudad I, Jernvall J, Newman SA (2003) Mechanisms of pattern formation in development and evolution. Development 130:2027–2037 doi:  10.1242/dev.00425 CrossRefPubMedGoogle Scholar
  69. Sanson G (2006) The biomechanics of browsing and grazing. Am J Bot 93:1531–1545 doi:  10.3732/ajb.93.10.1531 CrossRefPubMedGoogle Scholar
  70. Schmidt-Kittler N (1984) Pattern analysis of occlusal surfaces in hypsodont herbivores and its bearing on morpho-functional studies. Proc Konink Nederl Akad Wetensch B87:453–480Google Scholar
  71. Schmidt-Kittler N (2002) Feeding specializations in rodents. Senckenb Lethaea 82:141–152CrossRefGoogle Scholar
  72. Schulz E, Calandra I, Kaiser TM (2010) Applying tribology to teeth of hoofed mammals. Scanning 32:162–182CrossRefPubMedGoogle Scholar
  73. Schulz E, Calandra I, Kaiser TM (2013) Feeding ecology and chewing mechanics in hoofed mammals: 3D tribology of enamel wear. Wear 300:169–179CrossRefGoogle Scholar
  74. 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:e56167CrossRefPubMedPubMedCentralGoogle Scholar
  75. Scott JR (2012) Dental microwear texture analysis of extant African Bovidae. Mammalia 76:157–174CrossRefGoogle Scholar
  76. Skinner JD, Smithers RHN (1990) The Mammals of the Southern African Subregion. University of Pretoria, PretoriaGoogle Scholar
  77. Sponheimer M, Lee-Thorp JA, DeRuiter DJ, Smith JM, Van der Merwe NJ, Reed K, Grant CC, Ayliffe LK, Robinson TF, Heidelberger C, Marcus W (2003) Diets of southern African Bovidae: stable isotope evidence. J Mammal 84:471–479CrossRefGoogle Scholar
  78. Strait DS, Constantino P, Lucas PW, Richmond BG, Spencer MA, Dechow PC, Ross CF, Grosse IR, Wright BW, Wood BA, Weber GW, Wang Q, Byron C, Slice DE, Chalk J, Smith AL, Smith LC, Wood S, Berthaume M, Benazzi S, Dzialo C, Tamvada K, Ledogar JA (2013) Viewpoints: diet and dietary adaptations in early hominins. Am J Phys Anthropol 151:339–355CrossRefPubMedGoogle Scholar
  79. Suter HP (2010) xlsReadWrite: Natively Read and Write Excel Files. Downloaded on 01.06.2010
  80. Turnbull WD (1970) Mammalian masticatory apparatus. Fieldiana: Geology 18:147–356Google Scholar
  81. Ungar PS, Grine FE, Teaford MF (2008) Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS ONE 3:e2044CrossRefPubMedPubMedCentralGoogle Scholar
  82. Welch BL (1938) The significance of the difference between two means when the population variances are unequal. Biometrika 29:350–362CrossRefGoogle Scholar
  83. Wilcox RR (2003) Applying Contemporary Statistical Techniques. Academic Press, San DiegoGoogle Scholar
  84. Wilcox RR (2005) Introduction to Robust Estimation and Hypothesis Testing, 2nd edn. Elsevier Academic Press, Burlington, San Diego, LondonGoogle Scholar
  85. Wilcox RR, Charlin VL, Thompson KL (1986) New monte carlo results on the robustness of the anova f, w and f statistics. Commun Stat Simulat 15:933–943 doi:  10.1080/03610918608812553
  86. Wilcox RR, Schönbrodt FD (2010) The WRS Package for Robust Statistics in R. Downloaded on 27.04.2011
  87. Williams SH, Kay RF (2001) A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. J Mammal Evol 8:207–229 doi:  10.1023/A:1012231829141
  88. Winkler DE, Schulz E, Calandra I, Gailer JP, Landwehr C, Kaiser TM (2013) Indications for a dietary change in the extinct bovid genus Myotragus (Plio-Holocene, Mallorca, Spain). Geobios 46:143–150CrossRefGoogle Scholar
  89. Yuen KK (1974) The two-sample trimmed t for unequal population variances. Biometrika 61:165–170CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Juan Pablo Gailer
    • 1
    Email author
  • Ivan Calandra
    • 2
  • Ellen Schulz-Kornas
    • 1
    • 3
  • Thomas M. Kaiser
    • 1
  1. 1.Center of Natural HistoryUniversity of HamburgHamburgGermany
  2. 2.GEGENAA – EA 3795University of Reims Champagne-ArdenneReimsFrance
  3. 3.Max Planck Institute for Evolutionary Anthropology, Max Planck Weizmann Center for Integrative Archaeology and AnthropologyLeipzigGermany

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