Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T18:39:13.090Z Has data issue: false hasContentIssue false
  • English
  • Français

Origin of the mammalian feeding complex: models and mechanisms

Published online by Cambridge University Press:  08 April 2016

Dennis M. Bramble
Dennis M. Bramble*
Affiliation:
Department of Biology, University of Utah, Salt Lake City, Utah 84112
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper proposes a simple, unorthodox model for use in the study of vertebrate jaw mechanics. Central to the new “bifulcral model” is the assumption that the bite point may be regarded as a distinct and independent “occlusal fulcrum” equal in status to the jaw articulation or “joint fulcrum” of more traditional biomechanical models. The bifulcral model allows all mechanical forces acting on the feeding system to be evaluated in terms of their purely rotational and purely translational components defined relative to the occlusal and joint fulcra. The major benefit of this analytical approach is that it permits a new and substantially different perspective on the functional consequences of morpho-geometric organization in feeding systems. The bifulcral model clearly establishes the dynamic relationships among muscle alignment, bite point and the resultant patterns of mechanical stress at the craniomandibular joint (CMJ). It also reveals potentially important modes of competitive interaction between otherwise seemingly synergistic jaw muscles. Further, the bifulcral model encourages preliminary investigations into the possible contribution of intramuscular dynamics to the overall operational plasticity of the feeding machinery.

Specific application of the new model to structural and functional problems concerning the origin of the mammalian feeding complex lead to the following tentative conclusions. (1) Contrary to current opinion, the CMJ of most cynodont therapsids probably did not experience positive vertical loads (= compressive) when the cheek teeth were utilized for mastication. Instead, net CMJ loads were either neutral or somewhat negative (= tensile). (2) The development of a pronounced coronoid process in cynodonts was more directly related to promoting the differentiation of the masseter complex than to either improving the mechanical advantage or prehensile capacity of the temporalis muscle. (3) Differential motor activity within the complex temporalis musculature of cynodonts could have resulted in “derived lines of action” markedly different from the reconstructed lines of action employed in previous analyses of feeding mechanics in these reptiles. Such derived lines of action may have been optimal configurations for the integrated activity of the temporalis and masseter musculature. (4) Selection in cynodonts favored the evolution of a superficial masseter rather than the elaboration of the preexisting and geometrically similar pterygoideus musculature. This occurred because the masseter held the greater potential for improving bite force, motor control and facilitating the reduction of the postdentary bones of the mandible while still preserving the basic spatial economy of the cranial region. (5) The rearward growth of the condylar process of the dentary in cynodonts promoted the reduction of the postdentary unit primarily by shifting the point of load application between the dentary and postdentary units, thereby reducing bending stresses in the postdentary unit. (6) The enlarged squamosal sulcus of cynodonts was occupied mainly by a hypertrophied depressor mandibulae muscle; an auditory tube was also present in the sulcus deep to the muscle. (7) The depressor mandibulae played a major role in CMJ stabilization in therapsids; this was possibly its only function in later cynodonts. The peculiar downturned retroarticular process of the mandible in therapsids appears to have been related to this same function.

Type
Research Article
Information
Paleobiology , Volume 4 , Issue 3 , Summer 1978 , pp. 271 - 301
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adams, L. A. 1919. A memoir on the phylogeny of the jaw muscles in recent and fossil vertebrates. N.Y. Acad. Sci. Ann. 28:51–166.Google Scholar
Allin, E. F. 1975. Evolution of the mammalian middle ear. J. Morphol. 147:403–438.CrossRefGoogle ScholarPubMed
Arendsen De Wolff-Exalto, E. 1951a. On differences in the lower jaw of Animalivorous and Herbivorous mammals. I. Proc. Koninkl. Nederl. Akad van Wetensch. Ser. C. 54:237–246.Google Scholar
Arendsen De Wolff-Exalto, E. 1951b. On differences in the lower jaw of Animalivorous and Herbivorous mammals. II. Proc. Koninkl. Nederl. Akad. v. Wetensch. Ser. C. 54:405–410.Google Scholar
Barbenel, J. C. 1972. The biomechanics of the temporomandibular joint: a theoretical study. J. Biomech. 5:251–256.Google Scholar
Barghusen, H. R. 1968. The lower jaw of cynodonts (Reptilia, Therapsida) and the evolutionary origin of mammal-like adductor jaw musculature. Postilla. 118:1–49.Google Scholar
Barghusen, H. R. 1972. The origin of the mammalian jaw apparatus. Pp. 26–32. In: Schumacher, G. H., ed. Morphology of the Maxillomandibular Apparatus. VEB Georg Thieme; Leipzig.Google Scholar
Barghusen, H. R. 1973. The adductor jaw musculature of Dimetrodon (Reptilia, Pelycosauria). J. Paleontol. 47:823–834.Google Scholar
Barghusen, H. R. and Hopson, J. A. 1970. Dentary-squamosal joint and the origin of mammals. Science, N.Y. 168:573–575.Google Scholar
Bock, W. J. 1966. An approach to the functional analysis of bill shape. Auk. 81:10–51.CrossRefGoogle Scholar
Bock, W. J. 1968. Mechanics of one- and two-joint muscles. Am. Mus. Novit. 2319:1–45.Google Scholar
Bock, W. J. and Kummer, B. 1968. The avian mandible as a structural girder. J. Biomech. 1:89–96.Google Scholar
Bramble, D. M. 1971. Functional Morphology, Evolution and Paleoecology of Gopher Tortoises. 341 pp. Ph.D. Dissertation, Univ. Calif.; Berkeley, California.Google Scholar
Bramble, D. M. 1974. Occurrence and significance of the Os Transiliens in gopher tortoises. Copeia. 1974(1):102–109.CrossRefGoogle Scholar
Carroll, R. L. 1969. Problems of the origin of reptiles. Biol. Rev. 44:393–432.Google Scholar
Craddock, F. W. 1951. A review of Costen's syndrome. Br. Dent. J. 91:199.Google Scholar
Crompton, A. W. 1963a. On the lower jaw of Diarthrognathus and the origin of the mammalian lower jaw. Zool. Soc. London Proc. Ser. B. 108:735–761.Google Scholar
Crompton, A. W. 1963b. The evolution of the mammalian jaw. Evolution. 17:431–439.CrossRefGoogle Scholar
Crompton, A. W. 1972. The evolution of the jaw articulation of cynodonts. Pp. 231–251. In: Joysey, K. A. and Kemp, T. S., eds. Studies in Vertebrate Evolution. Oliver and Boyd; Edinburg.Google Scholar
Crompton, A. W. 1974. The dentitions and relationships of the Southern African Triassic mammals, Erythrotherium parringtoni and Megazostrodon rudnerae. Bull. Br. Mus. Nat. Hist. (Geol.). 24:397–437.Google Scholar
Crompton, A. W. and Hiiemäe, K. 1969. How mammalian molar teeth work. Discovery. 5:23–34.Google Scholar
Crompton, A. W. and Hiiemäe, K. 1970. Molar occlusion and mandibular movements during occlusion in the American opossum, Didelphis marsupialis. Zool. J. Linn. Soc. 49:21–47.Google Scholar
Crompton, A. W. and Hotton, N. III. 1967. Functional morphology of the masticulatory apparatus of two dicynodonts (Reptilia, Therapsida). Postilla. 109:1–51.Google Scholar
Crompton, A. W., Cook, P., Hiiemäe, K., and Thexton, A. J. 1975. Movement of the hyoid apparatus during chewing. Nature. 258:69–70.Google Scholar
Davis, D. D. 1955. Masticatory apparatus in the spectacled bear Tremarctos ornatus. Fieldiana: Zool. 37:25–46.Google Scholar
Davis, D. D. 1964. The giant panda—A morphological study of evolutionary mechanisms. Fieldiana: Zool., Mem. Ser. 3:1–339.Google Scholar
DeMar, R. and Barghusen, H. R. 1973. Mechanics and evolution of the synapsid jaw. Evolution. 26:622–637.Google Scholar
Dempster, W. T. 1961. Free-body diagrams as an approach to the mechanics of human posture and motion. Pp. 81–135. In: Evans, F. G., ed. Biomechanical Studies of the Musculoskeletal System. C. C. Thomas; Springfield, Illinois.Google Scholar
Dempster, W. T. and Duddles, R. A. 1964. Tooth statics: equilibrium of a free-body. J. Am. Dent. Assoc. 68:652–666.Google Scholar
Gans, C. 1960. Studies on amphisbaenids (Amphisbaenia, Reptilia). 1. A taxonomic revision of the Trogonophinae and a functional interpretation of the amphisbaenid adaptive pattern. Bull. Am. Mus. Nat. Hist. 119:129–203.Google Scholar
Gans, C. 1966. The functional basis of the retroarticular process in some fossil reptiles. J. Zool. (London). 150:273–277.Google Scholar
Gans, C. 1974. Biomechanics. J. B. Lippincott; Philadelphia, Pennsylvania. 261 pp.Google Scholar
Gingerich, P. D. 1971. Functional significance of mandibular translation in vertebrate jaws. Postilla. 152:1–10.Google Scholar
Greaves, W. S. 1974. Functional implications of mammalian jaw joint position. Forma et Functio. 7:363–376.Google Scholar
Gregory, W. K. 1910. The orders of mammals. Bull. Am. Mus. Nat. Hist. 27:1–524.Google Scholar
Gregory, W. K. 1913. Critique of recent work on the morphology of the vertebrate skull, especially in relation to the origin of mammals. J. Morphol. 24:1–42.Google Scholar
Herring, S. W. 1972a. Sutures—a tool in functional cranial analysis. Acta Anat. (Basel). 83:222–247.CrossRefGoogle ScholarPubMed
Herring, S. W. 1972b. The role of canine morphology in the evolutionary divergence of pigs and peccaries. J. Mammal. 53:500–512.Google Scholar
Herring, S. W. 1975. Adaptations for gape in the hippopotamus and its relatives. Forma et Functio. 8:85–100.Google Scholar
Herring, S. W. and Herring, S. E. 1974. The superficial masseter and gape in mammals. Am. Nat. 108:561–576.Google Scholar
Herring, S. W. and Scapino, R. P. 1973. Physiology of feeding in miniature pigs. J. Morphol. 141:427–460.CrossRefGoogle ScholarPubMed
Hiiemäe, K. and Crompton, A. W. 1971. A cinefluorographic study of feeding in the American opposum, Didelphis marsupialis. Pp. 299–344. In: Dahlberg, A. ed. Dental Morphology and Evolution. Univ. Chicago Press; Chicago, Illinois.Google Scholar
Hopson, J. A. 1964. Tooth replacement in cynodont, dicynodont and therocephalian reptiles. Proc. Zool. Soc. London. 142:625–654.Google Scholar
Hopson, A. J. 1966. The origin of the mammalian middle ear. Am. Zool. 6:437–450.Google Scholar
Hopson, J. A. 1969. The origin and adaptive radiation of mammal-like reptiles and nontherian mammals. Ann. N.Y. Acad. Sci. 167:199–216.Google Scholar
Hopson, J. A. 1971. Post canine replacement in the gomphodont cynodont Diademodon. Pp. 1–21. In: Kermack, D. M. and Kermack, K. A., eds. Early Mammals. Academic Press; New York.Google Scholar
Hopson, J. A. and Crompton, A. W. 1969. Origin of mammals. Pp. 15–72. In: Dobzhansky, Th., Hecht, M. K., and Steere, W. C., eds. Evolutionary Biology. Vol. III.Google Scholar
Hopson, J. A. and Kitching, J. W. 1972. A revised classification of cynodonts (Reptilia: Therapsida). Palaeontol. Africana. 14:71–85.Google Scholar
Hylander, W. L. 1975. The human mandible: lever or link? Am. J. Phys. Anthrop. 43:227–242.Google Scholar
Kallen, F. C. and Gans, C. 1972. Mastication in the Little Brown Bat, Myotis lucifugus. J. Morphol. 136:385–420.Google Scholar
Kemp, T. S. 1972a. The jaw articulation and musculature of the whaitsiid Therocephalia. Pp. 213–230. In: Joysey, K. A. and Kemp, T. S., eds. Studies in Vertebrate Evolution. Oliver and Boyd; Edinburg.Google Scholar
Kemp, T. S. 1972b. Whaitsiid Therocephalia and the origin of cynodonts. Phil. Trans. R. Soc. (London) B. 264:857–911.Google Scholar
Kermack, K. A. and Mussett, F. 1958. The jaw articulation of the Docodonta and the classification of Mesozoic mammals. Proc. R. Soc. (London) B. 148:204–215.Google Scholar
Kermack, K. A., Mussett, F., and Rigney, H. W. 1973. The lower jaw of Morganucodon. Zool. J. Linn. Soc. 53:87–175.Google Scholar
Maynard Smith, J. and Savage, R. J. G. 1959. The mechanics of mammalian jaws. School Sci. Rev. 141:289–301.Google Scholar
Olson, E. C. 1961. Jaw mechanisms: rhipidistians, amphibians, reptiles. Am. Zool. 1:205–215.Google Scholar
Ostrom, J. H. 1964. A functional analysis of the jaw mechanics in the dinosaur Triceratops. Postilla. 88:1–35.Google Scholar
Parkyn, D. G. 1963. On the statics of jaw musculature. (Appendix to Crompton, 1963a, pp. 751–753.)Google Scholar
Parrington, F. R. 1934. On the cynodont genus Galesaurus, with a note on the functional significance of the changes in the evolution of the theriodont skull. Ann. Mag. Nat. Hist. 13:38–67.Google Scholar
Parrington, F. R. 1946. On the cranial anatomy of cynodonts. Proc. Zool. Soc. (London). 116:181–197.Google Scholar
Parrington, F. R. 1955. On the cranial anatomy of some gorgonopsians and the synapsid middle ear. Proc. Zool. Soc. (London). 125:1–40.Google Scholar
Roberts, D. and Tattersall, I. 1974. Skull form and the mechanics of mandibular elevation in mammals. Am. Mus. Novit. 2536:1–9.Google Scholar
Robinson, M. 1946. Theory of reflex controlled non-lever action of the mandible. J. Am. Dent. Assoc. 33:1260–1271.Google Scholar
Romer, A. S. 1956. Osteology of the Reptiles. Univ. Chicago Press; Chicago, Illinois. 772 pp.Google Scholar
Romer, A. S. 1966. Vertebrate Paleontology. 3rd Ed.Univ. Chicago Press, Chicago, Illinois. 468 pp.Google Scholar
Romer, A. S. 1970. The Chanãres (Argentina) Triassic reptile fauna, VI. A chiniquodontid cynodont with an incipient squamosal-dentary jaw articulation. Breviora, Mus. Comp. Zool. 344:1–18.Google Scholar
Roydhouse, R. 1955. Upward force of the condyles on the cranium. J. Am. Dent. Assoc. 50:166.Google Scholar
Scapino, R. P. 1972. Adaptive radiation of mammalian jaws. Pp. 33–39. In: Schumacher, G. H., ed. Morphology of the Maxillo-mandibular Apparatus. VEB Georg. Thieme; Leipzig.Google Scholar
Schumacher, G. H. 1973. The head muscles and hyolaryngeal skeleton of turtles and crocodilians. Pp. 101–194. In: Gans, C. and Parsons, T. S., eds. Biology of the Reptilia. Vol. IX. Academic Press; New York.Google Scholar
Scott, J. H. 1955. A contribution to the study of the mandibular joint function. Br. Dent. J. 94:345.Google Scholar
Simpson, G. G. 1959. Mesozoic mammals and the polyphyletic origin of mammals. Evolution. 13:405–414.Google Scholar
Turnbull, W. D. 1970. Mammalian masticatory apparatus. Fieldiana: Geol. 18:149–356.Google Scholar
Watson, D. M. S. 1912. On some reptilian lower jaws. Ann. Mag. Nat. Hist. 20:573–587.Google Scholar
Watson, D. M. S. 1951. Paleontology and Modern Biology. Yale Univ. Press; New Haven(Silliman Memorial Lectures, 1937, with appended later comments).Google Scholar
Watson, D. M. S. 1953. Evolution of the mammalian ear. Evolution. 7:159–177.Google Scholar
Weijs, W. A. and Dantuma, R. 1975. Electromyography and mechanics of mastication in the albino rat. J. Morphol. 146:1–34.Google Scholar
Westoll, T. S. 1943. The hyomandibular of Eusthenopteron and the tetrapod middle ear. Proc. R. Soc. (London) B. 131:393–414.Google Scholar
Wilson, G. H. 1920. A manual of Dental Prosthetics. Henry Kimpton; London.Google Scholar
Zangerl, R. 1944. Contributions to the osteology of the skull of the Amphisbaenidae. Am. Midl. Nat. 31:417–454.Google Scholar