A Comparative Analysis of the Articular Cartilage in the Temporomandibular Joint of Gouging and Nongouging New World Monkeys

  • Amy L. Mork
  • Walter E. Horton
  • Christopher J. Vinyard
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Both laboratory and field data demonstrate that marmosets gouge trees with wide jaw gapes to elicit exudate flow. Tree gouging distinguishes marmosets from other platyrrhines and presents a natural experiment for studying the morphological consequences of this derived feeding behavior. We utilize comparative histomorphometrics to determine whether loading of the TMJ at wide jaw gapes impacts articular cartilage form in two habitual gouging species, common (Callitrix jacchus) and pygmy marmosets (Cebuella pygmaea), compared to nongouging cotton-top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus). Our histological comparisons found no difference in articular cartilage form along the posterior condyle between gouging and nongouging species. Alternatively, the anterior glenoid of gouging species was relatively larger and deeper compared to nongouging species. These findings suggest that the articular cartilage of the anterior glenoid in gouging species possesses improved load resistance ability and points to the mosaic nature of functional responses to tree gouging in the marmoset masticatory apparatus.


Articular Cartilage Squirrel Monkey Posterior Condyle Condylar Cartilage Anterior Glenoid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Anne Burrows and Leanne Nash for inviting us to contribute to this volume, and Anne for asking us to participate in the symposium “The Evolution of Exudativory in Primates” held at the XXII Congress of the International Primatological Society in Edinburgh, Scotland (Aug. 2008). We are grateful to Elizabeth Curran (NEPRC), Amanda Trainor (WPRC), Suzette Tardiff (SFBR), Donna Layne (SFBR), and Susan Gibson (SMBRR) for supplying the specimens used in this analysis. We thank A. Burrows, T. Smith, S. Ward, and D. McBurney for suggestions and advice throughout this project. N. Robl assisted in collecting the histological data. This research was supported by NSF (BCS-0412153) and (BCS-0412153) and the NEOUCOM Department of Anatomy.


  1. Benjamin M, Ralphs JR (2004) Biology of fibrocartilage cells. Int Rev Cytol 233:1–45.PubMedCrossRefGoogle Scholar
  2. Bouvier M (1986) A biomechanical analysis of mandibular scaling in Old World monkeys. Am J Phys Anthropol 69:473–82.CrossRefGoogle Scholar
  3. Bouvier M (1987) Variation in alkaline-phosphatase activity with changing load on the mandibular condylar cartilage in the rat. Archs Oral Biol 32:671–5.CrossRefGoogle Scholar
  4. Bouvier M, Hylander WL (1982) The effect of dietary consistency on morphology of the mandibular condylar cartilage in young macaques (Macaca mulatta). In Dixon AD, Sarnat BG (eds) Factors and mechanisms influencing bone growth, Alan R Liss, New York.Google Scholar
  5. Boyd RL, Gibbs CH, Mahan PE, Richmond AF, Laskin JL (1990) Temporomandibular joint forces measured at the condyle of Macaca arctoides. Am J Orthod Dentofac Orthop 97:472–9.CrossRefGoogle Scholar
  6. Bulstra S, Drukker J, Kuijer R, Van Der Linden WB, Van Der Linden A (1993) Thionin staining of paraffin and plastic embedded sections of cartilage. Biotech Histochem 68:20–8.PubMedCrossRefGoogle Scholar
  7. Burrows AM, Smith TD (2007) Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.). Am J Primatol 69:36–45.PubMedCrossRefGoogle Scholar
  8. Carlson DS, McNamara JA, Jaul DH (1978) Histological analysis of the growth of the mandibular condyle in the rhesus monkey (Macaca mulatta). Am J Anat 151:103–18.PubMedCrossRefGoogle Scholar
  9. Chen J, Sorensen KP, Gupta T, Kilts T, Young M, Wadhwa S (2008) Altered functional loading causes differential effects in the subchondral bone and condylar cartilage in the temporomandibular joint from young mice. Osteoarth Cart 17:354–61.CrossRefGoogle Scholar
  10. Coimbra-Filho AF, Mittermeier RA (1977) Tree-gouging, exudate-eating and the “short-tusked” condition in Callithrix and Cebuella. In DG Kleiman (ed) The biology and conservation of the Callitrichidae, Smithsonian Institution Press, Washington DC.Google Scholar
  11. Colombo V, Palla S, Gallo LM (2008) Temporomandibular joint loading patterns related to joint morphology: A theoretical study. Cells Tiss Org 187:295–306.CrossRefGoogle Scholar
  12. Dijkgraaf LC, De Bont LGM, Boering G, Liem RSB (1995) Normal cartilage structure, biochemistry, and metabolism: A review of the literature. J Oral Maxillofac Surg 53:924–9.PubMedCrossRefGoogle Scholar
  13. Eng CM, Ward SR, Vinyard CJ, Taylor AB (2009) The mechanics of the masticatory apparatus facilitate muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus). J Exp Biol 212:4040–55.PubMedCrossRefGoogle Scholar
  14. Ferrari SF (1993) Ecological differentiation in the Callitrichidae. In AB Rylands (ed) Marmosets and tamarins: Systematics, behaviour, and ecology, Oxford University Press, Oxford.Google Scholar
  15. Fleagle JC (1999) Primate Adaptation and Evolution, Academic, New York.Google Scholar
  16. Freeman MAR, Kempson GE (1973) Load carriage. In Freeman MAR (ed) Adult articular cartilage, Pitman Medical, London.Google Scholar
  17. Gallo LM, Nickel JC, Iwasaki LR, Palla S (2000) Stress-field translation in the healthy human temporomandibular joint. J Dent Res 79:1740–6.PubMedCrossRefGoogle Scholar
  18. Gallo LM (2005) Modeling of temporomandibular joint function using MRI and jaw-tracking technologies – mechanics. Cells Tiss Org 180:54–68.CrossRefGoogle Scholar
  19. Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian Tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201.CrossRefGoogle Scholar
  20. Garber PA (1992) Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. Am J Phys Anthropol 88:469–82.PubMedCrossRefGoogle Scholar
  21. Garber PA, Rosenberger AA, Norconk MA (1996) Marmoset misconceptions. In Norconk MA, Rosenberger AA, Garber PA (eds) Adaptive radiations of neotropical primates, Plenum Press, New York.CrossRefGoogle Scholar
  22. Hardingham T, Bayliss M (1990) Proteoglycans of articular cartilage: changes in aging and in joint disease. Sem Arth Rheum 20:12–33.CrossRefGoogle Scholar
  23. Haskin CL, Milam SB, Cameron IL (1995) Pathogenesis of degenerative joint disease in the human temporomandibular joint. Crit Rev Oral Biol Med 6:248–77.PubMedCrossRefGoogle Scholar
  24. Herring SW, Herring SE (1974) The superficial masseter and gape in mammals. Am Nat 108:561–76.CrossRefGoogle Scholar
  25. Hinton RJ, Carlson DS (1983) Histological changes in the articular eminence and mandibular fossa during growth of the rhesus monkey (Macaca mulatta). Am J Anat 166:99–116.PubMedCrossRefGoogle Scholar
  26. Hinton RJ, McNamara JA (1984) Effect of age on the adaptive response of the adult temporomandibular joint: A study of induced protrusion in Macaca mulatta. Angle Orthod 54:154–62.PubMedGoogle Scholar
  27. Hu K, Radhakrishnan P, Patel RV, Mao JJ (2001) Regional structural and viscoelastic properties of fibrocartilage upon dynamic nanoindentation of the articular condyle. J Struct Biol 136:46–52.PubMedCrossRefGoogle Scholar
  28. Huang CY, Mow VC, Ateshian GA (2001) The role of flow-independent viscoelasticity in the biphasic tensile and compressive responses of articular cartilage. J Biomech Eng 123:410–7.PubMedCrossRefGoogle Scholar
  29. Huang Q, Opstelten D, Samman N, Tideman H (2002) Experimentally induced unilateral tooth loss: Histochemical studies of the temporomandibular joint. J Dent Res 81:209–13.PubMedCrossRefGoogle Scholar
  30. Hylander WL (1979a) An experimental analysis of temporomandibular joint reaction force in macaques. Am J Phys Anthropol 51:433–56.PubMedCrossRefGoogle Scholar
  31. Hylander WL (1979b) The functional significance of primate mandibular form. J Morphol 160:223–40.PubMedCrossRefGoogle Scholar
  32. Hylander WL, Bays R (1979) An in vivo strain-gauge analysis of the squamosal-dentary joint reaction force during mastication and incisal biting in Macaca mulatta and Macaca fascicularis. Archs Oral Biol 24:689–97.CrossRefGoogle Scholar
  33. Kanouse MC, Ramfjord SP, Nasjleti CE (1969) Condylar growth in rhesus monkeys. J Dent Res 48:1171–6.Google Scholar
  34. Kempson GE, Muir H, Swanson SAV, Freeman MAR (1970) Correlations between stiffness and the chemical constituents of cartilage on the human femoral head. Biochim Biophys Acta 215:70–7.PubMedCrossRefGoogle Scholar
  35. Kinzey WG, Rosenberger AL, Ramirez M (1975) Vertical clinging and leaping in a neotropical anthropoid. Nature 255:327–8.PubMedCrossRefGoogle Scholar
  36. Király K, Lapveteläinen T, Arokoski J, Törrönen K, Módis L, Kiviranta I, Helminen HJ (1996) Application of selected cationic dyes for the semiquantitative estimation in histological sections of articular cartilage by microspectrophotometry. Histochem J 28:577–90.PubMedCrossRefGoogle Scholar
  37. Kiviranta I, Jurvelin J, Tammi M, Säämänen AM, Helminen HJ (1987) Weight bearing controls glycosaminoglycan concentration and articular cartilage thickness in the knee joints of young beagle dogs. Arth Rheum 30:801–9.CrossRefGoogle Scholar
  38. Kiviranta I, Tammi M, Jurvelin J, Säämänen AM, Helminen HJ (1988) Moderate running exercise augments glycosaminoglycans and thickness of articular cartilage in the knee joint of young beagle dogs. J Orthop Res 6:188–95.PubMedCrossRefGoogle Scholar
  39. Klinge RF (2001) The structure of the fibrous tissue on the articular surface of the temporal bone in the monkey (Macaca mulatta). Micron 32:551–7.CrossRefGoogle Scholar
  40. Knudson CB, Knudson W (2001) Cartilage proteoglycans. Cell Develop Biol 12:69–78.CrossRefGoogle Scholar
  41. Kuettner KE, Kimura JH (1985) Proteoglycans: an overview. J Cell Biochem 27:327–36.PubMedCrossRefGoogle Scholar
  42. Kuroda S, Tanimoto K, Izawa T, Fujihara S, Koolstra JH, Tanaka E (2009) Biomechanical and biochemical characteristics of the mandibular condylar cartilage. Osteoarth Cart 17:1408–1415.Google Scholar
  43. Luder HU, Schroeder HE (1990) Light and electron microscopic morphology of the temporomandibular joint in growing and mature crab-eating monkeys (Macaca fascicularis): the condylar articular layer. Anat Embryol 181:499–511.PubMedCrossRefGoogle Scholar
  44. Luder HU, Schroeder HE (1992) Light and electron microscopic morphology of the temporomandibular joint in growing and mature crab-eating monkeys (Macaca fascicularis): the condylar calcified cartilage. Anat Embryol 185:189–99.PubMedCrossRefGoogle Scholar
  45. Milam SB, Klebe RJ, Triplett RG, Herbert D (1991) Characterization of the extracellular matrix of the primate temporomandibular joint. J Oral Maxillofac Surg 49:381–91.PubMedCrossRefGoogle Scholar
  46. Mizoguchi I, Takahashi I, Nakamura M, Sasano Y, Sato S, Kagayama M, Mitani H (1996) An immunohistochemical study of regional differences in the distribution of Type I and Type II collagens in rat mandibular condylar cartilage. Arch Oral Biol 41:863–9.PubMedCrossRefGoogle Scholar
  47. Mow VC, Ratcliffe A, Poole AR (1992) Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 13:67–97.PubMedCrossRefGoogle Scholar
  48. Mussa R, Hans MG, Enlow DH, Goldberg J (1999) Condylar cartilage response to continuous passive motion in adult guinea pigs: A pilot study. Am J Orthod Dentofacial Orthop 115:360–7.PubMedCrossRefGoogle Scholar
  49. Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yrbk Phys Anthropol 29:113–37.CrossRefGoogle Scholar
  50. Patel RV, Mao JJ (2003) Microstructural and elastic properties of the extracellular matrices of the superficial zone of neonatal articular cartilage by atomic force microscopy. Front Biosci 8:a18–a25.PubMedCrossRefGoogle Scholar
  51. Pirttiniemi P, Kantomaa T, Salo L, Tuominen M (1996) Effect of reduced articular function on deposition of type I and type II collagens in the mandibular condylar cartilage of the rat. Archs Oral Biol 41:127–31.CrossRefGoogle Scholar
  52. Presnell JK, Schriebman M, Humason GL (1997) Humason’s animal tissue techniques, John Hopkins University Press, Baltimore.Google Scholar
  53. Ravosa MJ, Kunwar R, Stock SR, Stack MS (2007) Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J Exp Biol 210:628–41.PubMedCrossRefGoogle Scholar
  54. Robinson PD, Poswillo DE (1994) Temporomandibular joint development in the marmoset – A mirror of man. J Craniofac Genet Dev Biol 14:245–51.PubMedGoogle Scholar
  55. Rosenberger AL (1978) Loss of incisor enamel in marmosets. J Mammal 59:207–8.CrossRefGoogle Scholar
  56. Rosenberger AL (1992) Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–62.PubMedCrossRefGoogle Scholar
  57. Sasaguri K, Jiang H, Chen J (1998) The effect of altered functional forces on the expression of bone-matrix proteins in developing mouse mandibular condyle. Arch Oral Biol 43:83–92.PubMedCrossRefGoogle Scholar
  58. Silver FH. (2006) Mechanosensing and mechanochemical transduction in extracellular matrix: Biological, chemical, engineering, and physiological aspects, Springer, New York.Google Scholar
  59. Singh M, Detamore MS (2009a) Biomechanical properties of the mandibular condylar cartilage and their relevance to the TMJ disc. J Biomech 42:405–17.PubMedCrossRefGoogle Scholar
  60. Singh M, Detamore MS (2009b) Stress relaxation behavior of mandibular condylar cartilage under high-strain compression. J Biomech Eng 131:0610081–5.Google Scholar
  61. Slowman SD, Brandt KD (1986) Composition and glycosaminoglycan metabolism of articular cartilage from habitually loaded and habitually unloaded sites. Arth Rheum 29:88–94.CrossRefGoogle Scholar
  62. Smith RJ, Petersen CE, Gipe DP (1983) Size and shape of the mandibular condyle in primates. J Morphol 177:59–68.PubMedCrossRefGoogle Scholar
  63. Stevenson MF, Rylands AB (1988) The marmosets, Genus Callithrix. In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behavior of neotropical primates. World Wildlife Fund, Washington DC.Google Scholar
  64. Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 64:419–49.PubMedCrossRefGoogle Scholar
  65. Tanaka H, Yamano E, Dalla-Bona DA, Watanabe M, Inubushi T, Shirakura M, Sano R, Takahashi K, van Eijden T, Tanne K (2006) Dynamic compressive properties of the mandibular condylar cartilage. J Dent Res 85:571–5.PubMedCrossRefGoogle Scholar
  66. Taylor AB (2005) A comparative analysis of temporomandibular joint morphology in the African apes. J Hum Evol 48:555–74.PubMedCrossRefGoogle Scholar
  67. Taylor AB, Vinyard CJ (2004) Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol 261:276–85.PubMedCrossRefGoogle Scholar
  68. Taylor AB, Eng CM, Anapol FC, Vinyard CJ (2009) The functional correlates of jaw-muscle fiber architecture in tree-gouging and nongouging callitrichid monkeys. Am J Phys Anthropol 139:353–67.PubMedCrossRefGoogle Scholar
  69. Tong ACK, Tideman H (2001) The microanatomy of the rhesus monkey temporomandibular joint. J Oral Maxillofac Surg 59:46–52.PubMedCrossRefGoogle Scholar
  70. Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–70.PubMedCrossRefGoogle Scholar
  71. Vinyard CJ, Wall CE, Williams SH, Mork AL, Armfield BA, Melo LCO, Valença-Montenegro MM, Valle YBM, Borstelmann de Oliveira MA, Lucas PW, Schmitt D, Taylor AB, Hylander WL (2009) The evolutionary morphology of tree gouging in marmosets. In Ford SM, Davis LC, Porter LM (eds) The smallest anthropoids: The marmoset/callimico radiation, Springer, New York.Google Scholar
  72. Wall CE (1999) A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. Am J Phys Anthropol 109:67–88.PubMedCrossRefGoogle Scholar
  73. Williams SH, Wall CE, Vinyard CJ, Hylander WL (2002) A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatol 73:197–209.PubMedCrossRefGoogle Scholar
  74. Wilson NHF, Gardner DL (1982) The postnatal development of the temporomandibular joint of the common marmoset (Callithrix jacchus). J Med Primatol 11:303–11.PubMedGoogle Scholar
  75. Yanagishita M (1993) Function of proteoglycans in the extracellular matrix. Acta Pathol Japon 43:283–93.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Amy L. Mork
    • 1
  • Walter E. Horton
  • Christopher J. Vinyard
  1. 1.Department of Anatomy and NeurobiologyNortheastern Ohio Universities College of Medicine (NEOUCOM)RootstownUSA

Personalised recommendations