Allometry of masticatory loading parameters in mammals

Anatomical Record

Volumn 293, Issue 4, 2010, Pages 557-571

  Ravosa, Matthew J ^a   Ross, Callum F ^b   Williams, Susan H ^c   Costley, Destiny B ^a  

^a University of Missouri   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c OHIO UNIVERSITY   (United States)

Author keywords

Bite force; Body size; Bone strain; Chewing cycle; Chewing frequency; Duty factor; Loading rate time; Mandibular corpus; Masticatory stress; Scaling

Indexed keywords

ALLOMETRY; ARTICLE; BODY SIZE; BONE; BONE DEVELOPMENT; FOOD; GOAT; HORSE; LOCOMOTION; MAMMAL; MANDIBLE; MASTICATION; NONHUMAN; PARAMETER; PRIORITY JOURNAL; SKELETON;

ANIMALS; BODY SIZE; MANDIBLE; MASTICATION; SPECIES SPECIFICITY; STRESS, MECHANICAL; WEIGHT-BEARING;

CAPRA HIRCUS; EQUIDAE; MAMMALIA; PRIMATES; SUIDAE;

EID: 77950891995     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21133     Document Type: Article

References (118)

1. Alexander RM. 1977. Allometry of the limbs of antelopes (Bovidae). J Zool 183:125-146.
2. Alexander RM, Langman VA, Jayes AS. 1977. Fast locomotion in some African ungulates. J Zool 183:291-300.
3. Anderson J, Rahn H, Prange H. 1979. Scaling of supportive tissue mass. Quart Rev Biol 54:139-148.
4. Biewener AA. 1982. Bone strength in small mammals and bipedal birds: do safety factors change with body size? J Exp Biol 98:289-301.
5. Biewener AA. 1983. Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. J Exp Biol 105:147-171.
6. Biewener AA. 1991. Musculoskeletal design in relation to body size. J Biomech 24:19-29.
7. Biewener AA. 1993. Safety factors in bone strength. Calcif Tiss Int 53:568-574.
8. Biewener AA, Taylor CR. 1986. Bone strain: a determinant of gait and speed? J Exp Biol 123:383-400.
9. Biewener AA, Dial KP. 1995. In vivo strain in the humerus of pigeons (Columba livia) during flight. J Morphol 225:61-75.
10. Biewener AA, Bertram JEA. 1993. Skeletal strain patterns in relation to exercise training during growth. J Exp Biol 185:51-69.
11. Biewener AA, Swartz SM, Bertram JEA. 1986. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif Tiss Int 39:390-395.
12. Blob RW, Biewener AA. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and nonsprawling limb posture J Exp Biol 202:1023-1046.
13. Bock WJ, von Walhert G. 1965. Adaptation and the form-function complex. Evolution 19:269-299.
14. Bouvier M, Hylander WL. 1981. Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). J Morphol 167:1-12. (Pubitemid 11021544)
15. 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, editors. Factors and mechanisms influencing bone growth. New York: AR Liss. p 569-579.
16. Bouvier M, Hylander WL. 1984. The effect of dietary consistency on gross and histologic morphology in the craniofacial region of young rats. Am J Anat 170:117-126. (Pubitemid 14101477)
17. Bouvier M, Hylander WL. 1996. The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis. Arch Oral Biol 41:941-950. (Pubitemid 27066625)
18. Butcher MT, Espinoza NR, Cirilo SR, Blob RW. 2008. In vivo strains in the femur of river cooter turtles (Pseudemys concinna) during terrestrial locomotion: tests of force-platform models of loading mechanics. J Exp Biol 211:2397-2407.
19. Carrano MT, Biewener AA. 1999. Experimental alteration of limb posture in the chicken (Gallus gallus) and its bearing on the use of birds as analogs for dinosaur locomotion. J Morphol 240:237-249.
20. Carter DR, Spengler DM. 1978. Mechanical properties and composition of cortical bone. Clin Orth Rel Res 135:192-217. (Pubitemid 9046475)
21. Carter DR, Spengler DM, Frankel VH. 1977. Bone fatigue in uniaxial loading at physiologic strain rates. IRCS Med Sci 5:592.
22. Carter DR, van der Meulen MCH, Beaupre GS. 1996. Mechanical factors in bone growth and development. Bone 18:5-10.
23. Dechow PC, Carlson DS. 1990. Occlusal force and craniofacial biomechanics during growth in rhesus monkeys. Am J Phys Anthropol 83:219-238.
24. Demes B, Stern JT, Hausman MR, Larson SG, McLeod KJ, Rubin CT. 1998. Patterns of strain in the macaque ulna during functional activity. Am J Phys Anthropol 106:87-100. (Pubitemid 28196939)
25. Demes B, Qin Y-X, Stern JT, Larson SG, Rubin CT. 2001. Patterns of strain in the macaque tibia during functional activity. Am J Phys Anthropol 116:257-265. (Pubitemid 33104495)
26. Druzinsky RE. 1993. The time allometry of mammalian chewing movements: chewing frequency scales with body mass in mammals. J Theor Biol 160:427-440. (Pubitemid 23158512)
27. Emerson SB, Bramble DM. 1993. Scaling, allometry, and skull design. In: Hanken J, Hall BK, editors. The skull. Volume 3: functional and evolutionary mechanisms. Chicago: University of Chicago Press. p 384-421.
28. English AW. 1985. Limbs vs. jaws: can they be compared? Am Zool 25:351-363.
29. Fortelius M. 1985. Ungulate cheek teeth: developmental, functional and evolutionary interrelations. Acta Zool Fenn 180:1-76.
30. Gerstner GE, Gerstein JB. 2008. Chewing rate allometry among mammals. J Mammal 89:1020-1030.
31. Goodship AE, Lanyon LE, McFie H. 1979. Functional adaptation of bone to increased stress. An experimental study. J Bone Joint Surg 61:539-546. (Pubitemid 10161983)
32. Gorniak GC, Gans C. 1980. Quantitative assay of electromyograms during mastication in domestic cats (Felis catus). J Morphol 163:253-281. (Pubitemid 10047449)
33. Heglund NC, Taylor CR. 1988. Speed, stride frequency and energy cost per stride: how do they change with body size and gait? J Exp Biol 138:301-318.
34. Heglund NC, Taylor CR, McMahon TA. 1974. Scaling stride frequency and gait to animal size: mice to horses. Science 186:1112-1113.
35. Herring SW, Scapino RP. 1973. Physiology of feeding in miniature pigs. J Morphol 141:427-460.
36. Herring SW, Wineski LE. 1986. Development of the masseter muscle and oral behavior in the pig. J Exp Zool 237:191-207. (Pubitemid 16158210)
37. Herring SW, Teng S. 2000. Strain in the braincase and its sutures during function. Am J Phys Anthropol 112:575-593. (Pubitemid 30643049)
38. Herring SW, Anapol FC, Wineski LE. 1991. Motor-unit territories in the masseter muscle of infant pigs. Arch Oral Biol 36:867-873.
39. Herring SW, Pedersen SC, Huang X. 2005. Ontogeny of bone strain: the zygomatic arch in pigs. J Exp Biol 208:4509-4521. (Pubitemid 43028113)
40. Herring SW, Rafferty KL, Liu ZJ, Marshall CD. 2001. Jaw muscles and the skull in mammals: the biomechanics of mastication. Comp Biochem Physiol Part A 131:207-219.
41. Hiiemae KM. 1978. Mammalian mastication: a review of the activity of the jaw muscles and the movements they produce in chewing. In: Butler PM, Joysey KA, editors. Development, function and evolution of teeth. New York: Academic Press, p 359-398.
42. Hiraiwa T. 1978. Histochemical properties of masticatory muscles of growing rat and of matured mammals. Comp Biochem Physiol 59:231-238. (Pubitemid 8280594)
43. Hylander WL. 1979a. Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo approach to stress analysis of the mandible. J Morphol 159:253-296.
44. Hylander WL. 1979b. The functional significance of primate mandibular form. J Morphol 160:223-240. (Pubitemid 9194734)
45. Hylander WL. 1984. Stress and strain in the mandibular symphysis of primates: a test of competing hypotheses. Am J Phys Anthropol 64:1-46.
46. Hylander WL. 1985. Mandibular function and biomechanical stress and scaling. Am Zool 25:315-330.
47. Hylander WL, Johnson KR. 1997. In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. Am J Phys Anthropol 102:203-232.
48. Hylander WL, Johnson KR, Crompton AW. 1987. Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. Am J Phys Anthropol 72:287-314.
49. Hylander WL, Picq PG, Johnson KR. 1991. Masticatory-stress hypotheses and the supraorbital region of primates. Am J Phys Anthropol 86:1-36.
50. Hylander WL, Johnson KR, Crompton AW. 1992. Muscle force recruitment and biomechanical modeling: an analysis of masseter muscle function during mastication in Macaca fascicularis. Am J Phys Anthropol 88:365-387.
51. Hylander WL, Ravosa MJ, Ross CF, Johnson KR. 1998. Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force. Am J Phys Anthropol 107:257-271.
52. Hylander WL, Ravosa MJ, Ross CF, Wall CE, Johnson KR. 2000. Symphyseal fusion and jaw-adductor muscle force: an EMG study. Am J Phys Anthropol 112:469-492.
53. Indrekvan K, Husby OS, Gjerdet NR, Engesaeter LB, Langeland N. 1991. Age-dependent mechanical properties of rat femur. Measured in vivo and in vitro. Acta Orth Scand 62:248-252.
54. Keller TS, Spengler DM. 1989. Regulation of bone stress and strain in the immature and mature rat femur. J Biomech 22:1115-1127.
55. Kiltie RA. 1982. Bite force as a basis for niche differentiation between rain forest peccaries (Tayassu tajacu and T. pecari). Biotropica 14:188-195.
56. Langenbach GEJ, Van Wessel T, Brugman P, Korfage JAM, van Eijden TMGJ. 2008. Is fiber-type composition related to daily jaw muscle activity during postnatal development? Cells Tiss Org 187:307-315.
57. Lanyon LE, Baggott DG. 1976. Mechanical function as an influence on the structure and form of bone. J Bone Joint Surg 58:436-443.
58. Lanyon LE, Bourn S. 1979. The influence of mechanical function on the development and remodeling of the tibia. An experimental study in sheep. J Bone Joint Surg 61:263-273. (Pubitemid 9130299)
59. Lanyon LE, Rubin CT. 1985. Functional adaptation in skeletal structures. In: Hildebrand M, Bramble DM, Liem KF, Wake DB, editors. Functional vertebrate morphology. Cambridge: Harvard University Press. p 1-25.
60. Liu ZJ, Herring SW. 2000a. Bone surface strains and internal bony pressures at the jaw joint of the miniature pig during masticatory muscle contraction. Arch Oral Biol 45:95-112.
61. Liu ZJ, Herring SW. 2000b. Masticatory strains on osseous and ligamentous components of the temporomandibular joint in miniature pigs. J Orofac Pain 14:265-278.
62. Liu ZJ, Green JR, Moore CA, Herring SW. 2004. Time series analysis of jaw muscle contraction and tissue deformation during mastication in miniature pigs. J Oral Rehabil 31:1-17.
63. Main RP, Biewener AA. 2004. Ontogenetic patterns of limb loading, in vivo bone strains and growth in the goat radius. J Exp Biol 207:2577-2588.
64. Main RP, Biewener AA. 2007. Skeletal strain patterns and growth in the emu hindlimb during ontogeny. J Exp Biol 210:2676-2690.
65. Mao JJ. 2002. Mechanobiology of craniofacial sutures. J Dent Res 81:810-816.
66. Maxwell LC, Carlson DS, McNamara JA, Faulkner JA. 1979. Histochemical characteristics of the masseter and temporalis muscles of the rhesus monkey (Macaca mulatta). Anat Rec 193:389-402.
67. McElhaney JH. 1966. Dynamic response of bone and muscle tissue. J Appl Physiol 21:1231-1236.
68. Nakagawa N. 2009. Feeding rate as valuable information in primate feeding ecology. Primates 50:131-141.
69. Nakata S. 1981. Relationship between the development and growth of cranial bones and masticatory muscles in postnatal mice. J Dent Res 60:1440-1450. (Pubitemid 11010115)
70. Ravosa MJ. 1991a. The ontogeny of cranial sexual dimorphism in two Old World monkeys: Macaca fascicularis (Cercopithecinae) and Nasalis larvatus (Colobinae). Int J Primatol 12:403-426.
71. Ravosa MJ. 1991b. Structural allometry of the prosimian mandibular corpus and symphysis. J Hum Evol 20:3-20.
72. Ravosa MJ, Hylander WL. 1994. Function and fusion of the mandibular symphysis in primates: stiffness or strength? In: Fleagle JG, Kay RF, editors. Anthropoid origins. New York: Plenum Press. p 447-468.
73. Ravosa MJ, Hogue AS. 2004. Function and fusion of the mandibular symphysis in mammals: a comparative and experimental perspective. In: Ross CF, Kay RF, editors. Anthropoid evolution. New visions. New York: Kluwer Academic/Plenum Publishers. p 413-462.
74. Ravosa MJ, Daniel AN. Ontogeny and phyletic size change in living and fossil lemurs. Am J Primatol 72:161-172.
75. Ravosa MJ, Johnson KR, Hylander WL. 2000a. Strain in the galago facial skull. J Morphol 245:51-66.
76. Ravosa MJ, Noble VE, Hylander WL, Johnson KR, Kowalski EM. 2000b. Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. J Hum Evol 38:667-693.
77. Ravosa MJ, Vinyard CJ, Hylander WL. 2000c. Stressed out: masticatory forces and primate circumorbital form. Anat Rec 261:173-175.
78. Ravosa MJ, Kunwar R, Stock SR, Stack MS. 2007. Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J Exp Biol 210:628-641. (Pubitemid 46450810)
79. Ravosa MJ, López EK, Menegaz RA, Stock SR, Stack MS, Hamrick MW. 2008a. Adaptive plasticity in the mammalian masticatory complex: you are what, and how, you eat. In: Vinyard CJ, Ravosa MJ, Wall CE, editors. Primate craniofacial biology and function. New York: Springer Academic Publishers. p 293-328.
80. Ravosa MJ, López EK, Menegaz RA, Stock SR, Stack MS, Hamrick MW. 2008b. Using "Mighty Mouse" to understand masticatory plasticity: myostatin-deficient mice and musculoskeletal function. Integr Comp Biol 48:345-359.
81. Ravosa MJ, Ning J, Costley DB, Daniel AN, Stack MS. 2010a. Masticatory biomechanics and masseter fiber-type plasticity. J Musculoskel Neuronal Interact 10:46-55.
82. Ravosa MJ, Daniel AN, Costley, DB. 2010b. Allometry and evolution in the galago skull. Folia Primatol, in press.
83. Rawlinson SCF, Mosley JR, Suswillo RFL, Pitsillides AA, Lanyon LE. 1995. Calvarial and limb bone cells in organ and monolayer culture do not show the same early responses to dynamic mechanical strain. J Bone Min Res 10:1225-1232.
84. Reilly SM. 1995. The ontogeny of aquatic feeding behavior in Salamandra salamandra: stereotypy and isometry in feeding kinematics. J Exp Biol 198:701-708.
85. Richard BA, Wainwright PC. 1995. Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture. J Exp Biol 198:419-433.
86. Ross CF, Hylander WL. 1996. In vivo and in vitro bone strain in the owl monkey circumorbital region and the function of the postorbital septum. Am J Phys Anthropol 101:183-215.
87. Ross CF, Metzger KA. 2004. Bone strain gradients an optimization in vertebrate skulls. Ann Anat 186:387-396.
88. Ross CF, Dharia R, Herring SW, Hylander WL, Liu ZJ, Rafferty KL, Ravosa MJ, Williams SH. 2007a. How do mammals chew harder? Modulation of mandibular corpus bone strain in mammals during mastication. J Exp Biol 210:1046-1063.
89. Ross CF, Eckhardt A, Herrel A, Hylander WL, Metzger KA, Schaerlaeken V, Washington RL, Williams SH. 2007b. Modulation of intra-oral processing in mammals and lepidosaurs. Integr Comp Biol 47:118-136. (Pubitemid 351176744)
90. Ross CF, Reed DA, Washington RL, Eckhardt A, Anapol F, Shahnoor N. 2009a. Scaling of chewing cycle duration in primates. Am J Phys Anthropol 138:30-44.
91. Ross CF, Washington RL, Eckhardt A, Reed DA, Vogel E, Dominy NJ, Machanda Z. 2009b. Ecological consequences of scaling of chew cycle duration and daily feeding time in Primates. J Hum Evol 56:570-585.
92. Rubin CT, Gross T, Donahue H, Guilak F, McLeod K. 1994. Physical and environmental influences on bone formation. In: Brighton C, Friedlander G, Lane J, editors. Bone formation and regeneration. American Academy of Orthopedic Surgeons, p 61-78.
93. Rubin CT, Lanyon LE. 1982. Limb mechanics as a function of speed and fair: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol 101:187-211.
94. Rubin CT, Lanyon LE. 1984. Dynamic strain similarity in vertebrates: an alternative to allometric limb bone scaling. J Theor Biol 107:321-327.
95. Scapino RP. 1981. Morphological investigation into functions of the jaw symphysis in carnivorans. J Morphol 167:339-375.
96. Schaffler MB, Radin EL, Burr DB. 1989. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone 10:207-214.
97. Selker F, Carter DR. 1989. Scaling of long bone fracture strength with animal mass. J Biomech 22:1175-1183. (Pubitemid 20097585)
98. Swartz SM, Bertram JEA, Biewener AA. 1989. Telemetered in vivo strain analysis of locomotor mechanics of brachiating gibbons. Nature 342:270-272.
99. Swartz SM, Bennett MB, Carrier DR. 1992. Wing bone stresses in free flying bats and the evolution of skeletal design for flight. Nature 359:726-729.
100. Taylor AB, Jones KE, Kunwar R, Ravosa MJ. 2006. Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits. Anat Rec 288A:1105-1111. (Pubitemid 44521965)
101. Thexton AJ, Hiiemae KM. 1997. The effect of food consistency upon jaw movement in the macaque: a cineradiographic study. J Dent Res 76:552-560.
102. Thexton AJ, Hiiemae KM, Crompton AW. 1980. Food consistency and bite size as regulators of jaw movement during feeding in the cat. J Neurophysiol 44:456-474.
103. Turner CH. 1998. Three rules for bone adaptation to mechanical stimuli. Bone 23:399-407.
104. van der Meulen MCH, Carter DR. 1995. Developmental mechanics determine long bone allometry. J Theor Biol 172:323-327.
105. Vinyard CJ, Ravosa MJ. 1998. Ontogeny, function, and scaling of the mandibular symphysis in papionin primates. J Morphol 235:157-175.
106. Vinyard CJ, Wall CE, Williams SH, Mork AL, Garner BA, Melo LCO, Valença-Montenegro MM, Valle YBM, Monteiro da Cruz MAO, Lucas PW, Schmitt D, Taylor AB, Hylander WL. 2009. The evolutionary morphology of tree gouging in marmosets. In: Ford SM, Davis LC, Porter LM, editors. The smallest Anthropoids: the Marmoset/Callimico radiation. New York: Springer Academic Publishers. p 395-410.
107. Vinyard CJ, Yamashita N, Tan C. 2008. Linking laboratory and field approaches in studying the evolutionary physiology of biting in bamboo lemurs. Int J Primatol 29:1421-1439.
108. Wainwright PC, Richard BA. 1995. Scaling the feeding mechanism of the largemouth bass (Micropterus salmoides): motor pattern. J Exp Biol 198:1161-1171.
109. Wake MH. 1992. Morphology, the study of form and function, in modern evolutionary biology. Oxford surveys in Evolutionary Biology. Vol.8. Oxford: Oxford University Press. p 289-346.
110. Weibel ER, Taylor CR, Bolis L, editors. 1998. Principles of animal design. The optimization and symmorphosis debate. Cambridge: Cambridge University Press.
111. Weijs WA, Dantuma R. 1981. Functional anatomy of the masticatory apparatus in the rabbit (Oryctolagus cuniculus L.). Neth J Zool 31:99-147.
112. Weijs WA, Brugman P, Grimbergen CA. 1989. Jaw movements and muscle activity during mastication in growing rabbits. Anat Rec 224:407-416. (Pubitemid 19191690)
113. Williams SH, Wright BW, Truong VD, Daubert CR, Vinyard CJ. 2005. Mechanical properties of foods used in experimental studies of primate masticatory function. Am J Primatol 67:329-346.
114. Williams SH, Wall CE, Vinyard CJ, Hylander WL. 2009. Mandibular corpus bone strain in goats and alpacas: Implications for understanding the biomechanics of mandibular form in selenodont artiodactyls. J Anat 214:65-78.
115. Williams SH, Sidote J, Stover KK. 2010. Occlusal development and masseter activity in alpacas (Lama pacos). Anat Rec 293:126-134.
116. Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48:473-492.
117. Wright BW, Ulibarri L, O'Brien J, Sadler B, Prodham R, Covert HH, Nadler T. 2008. It's tough out there: variation in the Toughness of ingested leaves and feeding behavior among four colobine in Vietnam. Int J Primatol 29:1455-1466.
118. Yamashita N, Vinyard CJ, Tan CL. 2009. Food mechanical food properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. Am J Phys Anthropol 139:368-381.