The ontogeny of Holocene and late Pleistocene human postcranial strength

American Journal of Physical Anthropology

Volumn 141, Issue 1, 2010, Pages 16-37

  Cowgill, Libby W ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Femur; Growth; Humerus; Neandertal

Indexed keywords

ARTICLE; BONE STRENGTH; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIAPHYSIS; FEMUR; FOSSIL; GENETICS; GEOGRAPHIC DISTRIBUTION; GEOMETRY; HOLOCENE; HUMAN; HUMERUS; LONG BONE; NUTRITIONAL STATUS; ONTOGENY; PLEISTOCENE; SKELETON;

ADOLESCENT; AGE DETERMINATION BY SKELETON; AGE DETERMINATION BY TEETH; ANIMALS; ANTHROPOLOGY, PHYSICAL; BIOMECHANICS; BODY SIZE; BONE DENSITY; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; DIAPHYSES; EVOLUTION; FEMUR; FOSSILS; HOMINIDAE; HUMANS; HUMERUS; INFANT; POPULATION DYNAMICS;

EID: 74749089122     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21107     Document Type: Article

References (119)

1. Adams P. 1968. The effect of experimental malnutrition on the development of long bones. Nutritional aspects of the development of bone and connective tissue. In: Symposium of the Group of European Nutritionist, Cambridge. 13:69-73.
2. Akhter MP, Cullen DM, Pedersen EA, Kimmel DB, Recker RR. 1998. Bone response to in vivo mechanical loading in two breeds of mice. Calcif Tissue Int 63:442-449.
3. Akhter MP, Iwaniec UT, Covey MA, Cullen DM, Kimmel DB, Recker RR. 2000. Genetic variation in bone density, histormorphology, and strength in mice. Calcif Tiss Int 67:337-344.
4. Alexeeva TI, Bogatenkov DV, Lebedinskaya GV. 2003. Anthropology of medieval Vlakhs in comparative study: on date of Mistikhaly burial site. Moskva: Scientific World (in Russia, summery in English).
5. Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E. 1998. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J BoneMiner Res 13:500-507.
6. Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S. 2002. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274-2280.
7. Biewener AA, Bertram JEA. 1994. Structural response of growing bone to exercise and disuse. J Appl Physiol 76:946-955.
8. Biewener AA, Swartz SM, Bertram JEA. 1986. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif Tissue Int 39:390-395.
9. Biewener AA. 1992. Overview of structural mechanics. In: Biewener AA, editor. Biomechanics-structures and systems: a practical approach. Oxford: Oxford University Press. p 1-20.
10. Bradney M, Pearce G, Naughton G, Sullivan C, Bass S, Beck T, Carlson J, Seeman E. 1998. Moderate exercise during growth in perubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res 13:1814-1821.
11. Cardoso HFV. 2005. Patterns of growth and development of the human skeleton and dentition in relation to environmental quality: a biocultural analysis of a sample of 20th century Portuguese subadult documented skeletons. Ph.D. thesis. McMasters University.
12. Carter DR, Beaupré GS. 2001. Skeletal function and form: mechanobiology of skeletal development, aging and regeneration. Cambridge: Cambridge University Press.
13. Carter DR, Orr TE, Fyhrie DP, Schurman DJ. 1987. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop Relat Res 219:237-250.
14. Carter DR, Wong M. 1988. Mechanical stress and endochondral ossification in the chondroepiphysis. J Orthop Res 6:148-154.
15. Churchill SE. 1994. Human upper body evolution in the Eurasian Late Pleistocene. Ph.D. dissertation. University of New Mexico, Albuquerque.
16. Churchill SE, Formicola V, Holliday TW, Holt B, Schumann BA. 2000. The Upper Paleolithic population in Europe in an evolutionary perspective. In: Roebroeks W, Mussi M, Svoboda J, Fennema K, editors. Hunters of the Golden Age. Leiden: University of Leiden.
17. Conroy BP, Kraemer WJ,Maresh CM, Fleck SJ, Stone MH, Fry AC, Miller PD, Dalsky GP. 1993. Bone mineral density in elite junior Olympic weightlifters. Med Sci Sports Exerc 25:1103-1109.
18. Cowgill LW. 2008. The ontogeny of recent and late pleistocene human postcranial robusticity. Ph.D. dissertation. Washington University, St. Louis.
19. Cowgill LW, Hager LD. 2007. Variation in the development of postcranial robusticity: an example from Çatalhöyük, Turkey. Int J Osteoarchael 17:235-252.
20. Cowgill LW, Trinkaus E, Zeder MA. 2007. Shanidar 10: a Middle Paleolithic immature distal lower limb from Shanidar Cave, Iraqi Kurdistan. J Hum Evol 53:213-223.
21. Dickerson JWT, McCance RA. 1961. Severe undernutrition in growing and adult animals: the dimensions and chemistry of the long bones. Brit J Nutr 15:567-576.
22. Eschman PN. 1992. SLCOMM Version 1.6. Eschman Archaeological Services, Albuquerque, NM.
23. Fazekas IG, Kósa F. 1978. Forensic fetal osteology. Budapest: Akadémiai Kiadó .
24. Ferembach D, Dastugue J, Poitrat-Targowla M-J. 1962. La Nécropole E ́ pipaléolithique de Taforalt: etude des squelettes humains. Paris: Centre National de la Recherche Scientifique.
25. Formicola V, Giannecchini M. 1999. Evolutionary trends in stature in Upper Paleolithic and Mesolithic Europe. J Hum Evol 36:319-333.
26. Galusca B, Zouch M, Germain N, Bossu C, Frere D, Lang F, Lafage-Proust M-H, Thomas T, Vico L, Estour B. 2008. Constitutional thinness: unusual human phenotype of low bone quality. J Clin Endocrinol Metab 93:110-117.
27. Grimston SK, Willows ND, Hanley DA. 1993. Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc 25:1203-1210.
28. Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals we comparable to those of modern humans. Proc Natl Acad Sci USA 102:14197-14202.
29. Hall BK. 1972. Immobilization and cartilage transformation into bone in the embryonic chick. Anat Rec 173:391-404.
30. Haapasalo H. 1998. Physical activity and growing bone: development of peak bone mass with special reference to the effects of unilateral physical activity. Ann Chir Gynaecol 87: 250-252.
31. Haapasalo H, Kannus P, Sievänen H, Pasanen M, Uusi-Rasi K, Heinonen A, Oja P, Vouri I. 1998. Effect of long-term unilateral activity on bone mineral density of female junior tennis players. J Bone Miner Res 13:310-319.
32. Henderson JH, Carter DR. 2002. Mechanical induction in limb morphogenesis: the role of growth-generated strains and pressures. Bone 31:645-653.
33. Holliday TW. 1999. Body proportions in Late Pleistocene Europe and modern human origins. J Hum Evol 32:423-447.
34. Holliday TW. 2002. Body size and postcranial robusticity of European Upper Paleolithic hominins. J Hum Evol 43:513-528.
35. Holms S. 1979. A simple sequentially reductive multiple test procedure. Scand J Stat 6:65-70.
36. Holt BM. 1999. Biomechanical evidence of decreased mobility in upper Paleolithic and Mesolithic Europe. Ph.D. thesis. University of Missouri, Columbia.
37. Holt BM. 2003. Mobility in Upper Paleolithic and Mesolithic Europe: evidence from the lower limb. Am J Phys Anthropol 122:200-215.
38. Jha GJ, Deo MG, Ramalingaswami V. 1968. Bone growth in protein deficiency: a study in Rhesus monkeys. Am J Pathol 53: 1111-1123.
39. Kannus P, Haapasalo H, Sankelo M, Sievänen H, Pasanen M, Heinonen A, Oja P, Vouri I. 1995. Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med 123:27-31.
40. Karlsson MK, Johnell O, Obrant KJ. 1995. Is bone mineral density advantage maintained long-term in previous weight lifters? Calcif Tissue Int 57:325-328.
41. Khan KM, Bennell KL, Hopper JL, Flicker L, Nowson CA, Sherwin AJ, Crichton KJ, Harcourt PR, Wark JD. 1998. Selfreported ballet classes undertaken at age 10-12 years and hip bone mineral density in later life. Osteoporos Int 8:165-173.
42. Kimura T, Takahashi H. 1982. Mechanical properties of cross section of lower limb long bones in Jomon Man. J Anthrop Soc Nippon 90(Suppl):105-118.
43. Kodama Y, Umemura Y, Nagasawa S, Beamer WG, Donahue LR, Rosen CR, Baylink DJ, Farley JR. 2000. Exercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/Hej mice. Calcif Tissue Int 66:298-306.
44. Kondo O, Dodo Y. 2002a. Postcranial bones of the Neanderthal child of the burial No. 1. In: Akazawa T, Muhesen S, editors. Neanderthal Burials. Excavations of the Dederiyeh Cave, Afin, Syria. Kyoto: International Research Center for Japanese Studies. p 139-201.
45. Kondo O, Dodo Y. 2002b. Postcranial bones of the Neanderthal child of the burial No. 2. In: Akazawa T, Muhesen S, editors. Neanderthal Burials. Excavations of the Dederiyeh Cave, Afin, Syria. Kyoto: International Research Center for Japanese Studies. p 299-313.
46. Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vouri I. 2003. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquetsports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 18:352-359.
47. Kriska AM, Sandler RB, Cauley JA, LaPorte RE, Hom DL, Pambianco G. 1988. The assessment of historical phycial activity and its relation to adult bone parameters. Am J Epidemiol 127:1053-1061.
48. Lambert J, Lamothe JM, Zernicke RF, Auer RN, Reimer RA. 2005. Dietary restriction does not adversely affect bone geometry and mechanical in rapidly growing male Wistar rats. Pediatr Res 57:227-231.
49. Larsen H, Rainey F. 1948. Ipiutak and the Arctic while hunting culture. Anthrop Pap Am Mus Nat Hist 42:1-276.
50. Lieberman DE, Devlin MJ, Pearson OM. 2001. Articular area responses to mechanical loading: effects of exercise, age, and skeletal location. Am J Phys Anthropol 116:266-277.
51. Liversidge HM, Molleson T. 2004. Variation in crown and root formation and eruption of human deciduous teeth. Am J Phys Anthropol 123:172-180.
52. Lovejoy OC, Meindl RS, Ohman JC, Heiple KG, White TD. 2002. The Maka femur and its bearing on the antiquity of human walking: applying contemporary concepts of mophogenesis to the human fossil record. Am J Phys Anthropol 119:97-133.
53. Lovejoy OC, McCollum MA, Reno PL, Rosenman BA. 2003. Developmental biology and human evolution. Annu Rev Anthropol 32:85-109.
54. Macchiarelli R, Bondiolo L, Debénath A, Mazurier A, Tournepiche J-F, Birch W, Dean C. 2006. How Neandertal molar teeth grew. Nature 444:748-751.
55. McCulloch RG, Bailey DA, Whalen RL, Houson CS, Faulkner RA, Craven BR. 1992. Bone density and bone mineral content of adolescent soccer athletes and competitive swimmers. Pediatr Exerc Sci 4:319-330.
56. McKay HA, Petit MA, Schutz RW, Prior JC, Barr SI, Khan KM. 2000. Augmented trochanteric bone mineral density after modified physical education classes. J Pediatr 136:156-162.
57. Micklesfield L, Rosenberg L, Cooper D, Hoffman M, Kalla A, Stander I, Lambert E. 2003. Bone mineral density and life-time physical activity in South African Women. Calcif Tissue Int 73:463-469.
58. Moore CB. 1916 Some aboriginal sites on the Green River, Kentucky. J Phila Acad Nat Sci 16:431-487.
59. Moran MD. 2003. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403-405.
60. Moratto MJ. 1984. California archaeology. Orlando: Academic Press.
61. Moro M, Van der Meulen MCH, Kiratli BJ, Marcus R, Bachrach LK, Carter DR. 1996. Body mass is the primary determinant of midfemoral bone acquisition during adolescent growth. Bone 19:519-526.
62. Mosley JR, March BM, Lynch J, Lanyon LE. 1997. Strain magnitude related changes in whole bone architecture in growing rats. Bone 20:191-198.
63. Nagurka ML, Hayes WC. 1980. An interactive graphics package for calculating cross sectional properties of complex shapes. J Biomech 13:59-64.
64. Nakagawa S. 2004. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15: 1044-1045.
65. Nelson AJ, Thompson JL. 2000. Adolescent postcranial growth in Homo neanderthalensis. In: Minugh-Purvis N, McNarmara KJ, editors. Human evolution through developmental change. Baltimore: John Hopkins University Press. p 442-463.
66. Nordström P, Pettersson U, Lorentzon R. 1998. Type of physical activity, muscle strength, and pubertal stage as determinants of bone mineral density and bone area in adolescent boys. J Bone Miner Res 13:1141-1148.
67. Odwak H. 2000. Long bone robusticity and claviculo-humeral proportions of the Amud baby. Am J Phys Anthropol 111:241.
68. O'Neill MC, Ruff CB. 2004. Estimating human long bone crosssectional geometric properties: a comparison of noninvasive methods. J Hum Evol 47:221-235.
69. Pearson OM, Lieberman DE. 2004. The aging of Wolff 's "law": ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthropol 47:63-99.
70. Perneger TV. 1998. What's wrong with Bonferroni adjustments. Brit Med J 316:1236-1238.
71. Pettersson U, Alfredson H, Nordström P, Henriksson-Larsén K, Lorentzon R. 2000a. Bone mass in female cross-country skiers: relationship between muscle strength and different BMD sites. Calcif Tissue Int 67:199-206.
72. Pettersson U, Nordström P, Alfredson H, Henriksson-Larsén K, Lorentzon R. 2000b. Effect of high impact activity on bone mass and size in adolescent females: a comparative study between two different types of sports. Calcif Tissue Int 67: 207-214.
73. Raab DM, Smith EL, Crenshaw TD, Thomas DP. 1990. Bone mechanical properties after exercise training in young and old rats. J Appl Physiol 68:130-134.
74. Rainey F. 1971. The Ipiutak culture: excavations at point hope. Alaska: Addison-Wesley Modular Publications in Anthropology8: 1-32.
75. Ramirez Rozzi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neandertals. Nature 936-939.
76. Ramsay HL, Weaver DS, Seidler H. 2005. Bone histology in the Le Moustier Neandertal child. In: Ullrich H, editor. The Neandertal adolescent Le Moustier 1: new aspects, new results. Berlin: Staatliche Museen zu Berlin -Preussischer Kulturbesitz. p. 282-290.
77. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
78. Robbins G. 2007. Population dynamics, growth and development in Chalcolithic sites of the Deccan Peninsula, India. Ph.D. dissertation, University of Oregon, Eugene.
79. Robling AG, Turner CH. 2002. Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562-569.
80. Rodriguez JI, Garcia-Alix A, Palacios J, Paniagua R. 1988b. Changes in the long bones due to fetal immobility caused by neuromuscular disease. J Bone Joint Surg 70:1052-1060.
81. Ruff CB. 2000a. Body size, body shape and long bone strength in modern humans. J Hum Evol 38:269-290.
82. Ruff CB. 2000b. Biomechanical analyses of archaeological human skeletons. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. Wiley-Liss. p 71-102.
83. Ruff CB. 2003a. Ontogenetic adaptation to bipedalism: age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. J Hum Evol 45:317-349.
84. Ruff CB. 2003b. Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317-329.
85. Ruff CB. 2007. Body size prediction from juvenile skeletal remains. Am J Phys Anthropol 133:698-716.
86. Ruff CB, Trinkaus E, Walker A, Larsen CS. 1993. Postcranial robusticity in Homo. I. Temporal trends and mechanical interpretations. Am J Phys Anthropol 91:21-53.
87. Ruff CB, Walker A, Trinkaus E. 1994. Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 35-54.
88. Ruff CB, Holt B, Trinkaus E. 2006. Who's afraid of the Big Bad Wolff? "Wolff 's Law" and bone functional adaptation. Am J Phys Anthropol 129:484-498.
89. Sakaue K. 1998. Bilateral asymmetry of the humerus in Jomon people and modern Japanese. Anthropol Sci 105:231-246.
90. Salomon CD, Volpin G. 1972. The effects of calcium-deficient diet on breaking strength and other physical parameters of rat bones. Clin Orthop Relat Res 82:207-213.
91. Saunders SR, DeVito C. 1991. Subadult skeletons in the Raymond Dart anatomical collection: research potential. Hum Evol 6:421-434.
92. Schönau E. 1998. The development of the skeletal system in children and the influence of muscular strength. Hom Res 49: 27-31.
93. Schulz PD. 1981 Osteoarchaeology and subsistence change in prehistoric Central California. Ph.D. dissertation. Department of Anthropology, University of California, Davis.
94. Sciulli PW, Blatt SH. 2008. Evaluation of juvenile stature and body mass prediction. Am J Phys Anthropol 136:387-393.
95. Shackelford LL. 2005. Regional variation in the postcranial robusticity of Late Upper Paleolithic humans. Ph.D. dissertation. Washington University, St. Louis.
96. Slemenda CW, Johnston CC. 1993. High intensity activities in young women: site specific bone mass effects among female figure skaters. Bone Miner 20:125-132.
97. Smith BH. 1991. Standards of human tooth formation and dental age assessment. In: Kelley MA and Larsen CS, editors. Advances in dental anthropology. New York: Wiley-Liss. p 143-168.
98. Smith TM, Toussaint M, Reid DJ, Olejniczak AJ, Hublin J-J. 2007. Rapid dental development in a Middle Paleolithic Belgian Neandertal. Proc Natl Acad Sci USA 104:20220-20225.
99. Söderman K, Bergström E, Lorentzon R, Alfredson H. 2000. Bone mass and muscle strength in young female soccer players. Calcif Tissue Int 67:297-303.
100. Sokal RR, Rohlf FJ. 1995. Biometry: the principles and practice of statistics in biological research, 3rd ed. New York: WH Freeman and company.
101. Steinberg ME, Trueta J. 1981. Effects of activity on bone growth and development of the rat. Clin Orthop Relat Res 156:52-60.
102. Sumner DR, Andriacchi TP. 1996. Adaptation to differential loading: comparison of growth related changes in cross-sectional properties of the human femur and humerus. Bone 19: 121-126.
103. Teegarden D, Proulx WR, Kern M, Sedlock D, Weaver CM, Johnston CC, Lyle RM. 1996. Previous physical activity relates to bone mineral measures in young women. Med Sci Sports Exerc 28:105-113.
104. Thompson JL, Nelson AJ. 2005. The postcranial skeleton of Le Moustier 1. In: Ullrich H, editor. The Neandertal adolescent Le Moustier 1: new aspects, new results. Berlin: Staatliche Museen zu Berlin-Preussischer Kulturbesitz. p 265-281.
105. Trinkaus E. 1997. Appendicular robusticity and the paleobiology of modern human emergence. Proc Natl Acad Sci USA 94: 13367-13373.
106. Trinkaus E, Churchill S. 1999. Diaphyseal cross-sectional geometry of the near eastern Middle Paleolithic humans: the humerus. J Archaeol Sci 26:173-184.
107. Trinkaus E, Ruff CB. 1999. Diaphyseal cross-sectional geometry of Near Eastern Middle Paleolithic humans: the femur. J Archaeol Sci 26:409-424.
108. Trinkaus E, Ruff CB. 1996. Early modern human remains from eastern Asia: the Yamashita-cho 1 immature postcrania. J Hum Evol 30:299-314.
109. Trinkaus E, Ruff CB, Esteves F, Coelho JMS, Silva M, Mendova M. 2002a. The lower limb remains. In: Zilhão J, Trinkaus E, editors. Portrait of the artist as a child. Lisbon: Intituto Portuguõs de Arqueologia. p 435-465.
110. Trinkaus E, Ruff CB, Esteves F, Coelho JMS, Silva M, Mendova M. 2002b. The upper limb remains. In: Zilhão J, Trinkaus E, editors. Portrait of the artist as a child. Lisbon: Intituto Portuguõs de Arqueologia. p 466-488.
111. Trinkaus E, Smith FH, Stockton TC, Shackelford LL. 2006. The human postcranial remains from Mladec. In: Teschler-Nicola M, editor. Early modern humans at the Moravian gate: the Mladec Caves and their remains. New York: SpringerWien. p 385-446.
112. Turner CH, Hsieh Y-F, Müller R, Bouxsein ML, Rosen CJ, McCrann ME, Donahue LR, Beamer WG. 2001. Variation in bone biomechanical properties, microstructure, and density in BXH recombinant inbred mice. J Bone Miner Res 16:206-213.
113. Van Gerven DP, Hummert JR, Burr DB. 1985. Cortical bone maintenance and geometry of the tibia in Prehistoric children from Nubia's Batn et Hajar. Am J Phys Anthropol 66:275-280.
114. Van Gerven DP, Beck R, Hummert JR. 1990. Patterns of enamel hypoplasia in two medieval populations from Nubia's Batn el Hajar. Am J Phys Anthropol 82:413-420.
115. van Gerven DP, Sheridan SG; Adams WY. 1995. The Health and nutrition of a medieval nubian population: the impact of political and economic change. Am Anthropol 97:468-480.
116. Van der Meulen MC, Ashford MWJ, Kiratli BJ, Backrach LK, Carter DR. 1996. Determinates of femoral geometry and structure during adolescent growth. J Orthop Res 14:22-29.
117. Webb WS. 1946. Indian Knoll, Site Oh 2, Ohio County, Kentucky: the University of Kentucky Reports in anthropology and archaeology. Lexington: Department of Anthropology. p 111-365.
118. Winters HD. 1974. Introduction to the new edition. In: Webb WS, editor. Indian knoll. Knoxville: University the Tennessee Press.
119. Woo SL-Y, Kuei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH. 1981. The effect of prolonged physical training on the properties of long bone. J Bone Joint Surg 63:780-787.