Section: Archaeology
Topic: Archaeology

Can growth in captivity alter the calcaneal microanatomy of a wild ungulate?

Cottereau, Romain1  ; Ortiz, Katia2, 3; Locatelli, Yann2, 3, 4 ; Houssaye, Alexandra1  ; Cucchi, Thomas5  
1 CNRS, UMR 7179 Mécanismes Adaptatifs et Evolution, Muséum d’Histoire Naturelle de Paris, France
2 Réserve Zoologique de la Haute-Touche, Muséum National d’Histoire Naturelle, Obterre, France
3 Institut de Systématique, Evolution, Biodiversité, UMR 7205, Muséum National d’Histoire Naturelle CNRS UPMC EPHE, UA, Paris, France
4 Physiologie de la Reproduction et des Comportements, UMR 7247, INRAE CNRS Université de Tours IFCE, Nouzilly, France
5 UMR 7209 Archéozoologie, Archéobotanique : Sociétés, Pratiques et Environnements, Muséum d’Histoire Naturelle de Paris, France

Corresponding author(s): Cottereau, Romain (cotterom@gmail.com)

10.24072/pcjournal.210 - Peer Community Journal, Volume 3 (2023), article no. e1.

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Reduced mobility associated with captivity induces changes in biomechanical stress on the skeleton of domesticated animals. Due to bone plasticity, bone’s morphology and internal structure can respond to these new biomechanical stresses over individuals’ lifetime. In a context where documenting early process of animal domestication is challenging, this study will test the hypothesis that change in mobility patterns during a wild ungulate’s life will alter the internal structure of its limb bones and provide a proof of concept for the application of this knowledge in Zooarchaeology. Using the calcaneus as a phenotypic marker through qualitative and quantitative 3D microanatomical analyses, we relied on a comparative study across wild boars (Sus scrofa) populations from controlled experimental conditions with different mobility patterns (natural habitat, large pen, and stall) and archaeological specimens collected from middle and late Mesolithic as surrogate for the norm of reaction in European wild boar phenotype before the spread of agriculture and domestic pigs. Results provide evidence for compressive and tensile forces as the main elements affecting the variation in the cortical thickness along the calcaneus. Furthermore, changes in the internal structure of the calcaneus between mobility patterns are observed but their intensity is not directly associated with the degree of mobility restriction and only weakly impacted by the size or weight of the individuals. Despite having greater bone volume, the calcaneus of the Mesolithic wild boars displays a very similar microanatomy compared to the present-day hunted or captive wild boars. These results suggest that calcaneal microanatomy is more affected by population differences than by locomotor variation. For all these reasons, this preliminary study doesn’t support the use of microanatomy of the calcaneus as an indicator of change in locomotor behaviour induced by captivity in the archaeological record.

Published online:
DOI: 10.24072/pcjournal.210
Type: Research article

Cottereau, Romain 1; Ortiz, Katia 2, 3; Locatelli, Yann 2, 3, 4; Houssaye, Alexandra 1; Cucchi, Thomas 5

1 CNRS, UMR 7179 Mécanismes Adaptatifs et Evolution, Muséum d’Histoire Naturelle de Paris, France
2 Réserve Zoologique de la Haute-Touche, Muséum National d’Histoire Naturelle, Obterre, France
3 Institut de Systématique, Evolution, Biodiversité, UMR 7205, Muséum National d’Histoire Naturelle CNRS UPMC EPHE, UA, Paris, France
4 Physiologie de la Reproduction et des Comportements, UMR 7247, INRAE CNRS Université de Tours IFCE, Nouzilly, France
5 UMR 7209 Archéozoologie, Archéobotanique : Sociétés, Pratiques et Environnements, Muséum d’Histoire Naturelle de Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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Cottereau, Romain; Ortiz, Katia; Locatelli, Yann; Houssaye, Alexandra; Cucchi, Thomas. Can growth in captivity alter the calcaneal microanatomy of a wild ungulate?. Peer Community Journal, Volume 3 (2023), article  no. e1. doi : 10.24072/pcjournal.210. https://peercommunityjournal.org/articles/10.24072/pcjournal.210/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.archaeo.100023

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agarwal, S. C. Bone morphologies and histories: Life course approaches in bioarchaeology, American Journal of Physical Anthropology (2016), p. 159

[2] Andre, J.-P. An introduction to normal and pathological behaviour in psittacine birds, Bulletin de l'Académie Vétérinaire de France, 2007 vol.160, N°3 (2007)

[3] Barone, R. Anatomie comparée des mammifères domestiques Tome 1- ostéologie – (5e éd.). Vigot., https://www.lepointveterinaire.fr/boutique/livres/anatomie-comparee-des-mammiferes-domestiques.html, 2017 (Publication Title: Le Point Vétérinaire.fr)

[4] Barone, R. Anatomie comparée des mammifères domestiques Tome 2 -Arthologie et myologie- (4eéd.). Association centrale d’entraide vétérinaire., 2000

[5] Baskin, L.; Danell, K. Ecology of Ungulates: A Handbook of Species in Eastern Europe and Northern and Central Asia, Springer Science & Business Media, 2003

[6] Bassarova, M.; Janis, C. M.; Archer, M. The Calcaneum—On the Heels of Marsupial Locomotion, J Mammal Evol, Volume 16 (2009) no. 1, pp. 1-23 | DOI

[7] Bénévent, M.; Bressot, C. Guide pour la dissection et l'identification des principaux muscles de la carcasse chez le mouton, Annales de biologie animale, biochimie, biophysique, Volume 8 (1968) no. 2, pp. 147-193

[8] Binford, L. R. Nunamiut ethnoarchaeology, New York: Academic Press, 1978

[9] Bleefeld, A. R.; Bock, W. J. Unique anatomy of lagomorph calcaneus, Acta Palaeontologica Polonica, Volume 47 (2002) no. 1, pp. 181-183

[10] Carmeliet, G.; Bouillon, R. Space flight: a challenge for normal bone homeostasis, Critical Reviews™ in Eukaryotic Gene Expression, Volume 11 (2001) no. 1-3 (Publisher: Begel House Inc.)

[11] Carrano, M. T. Morphological indicators of foot posture in mammals: a statistical and biomechanical analysis, Zoological Journal of the Linnean Society, Volume 121 (1997) no. 1, pp. 77-104 (Publisher: Oxford University Press)

[12] Carter, D. R.; Beaupre, G. S. Skeletal Function and Form: Mechanobiology of Skeletal Development, Aging, and Regeneration, GROWTH DEVELOPMENT AND AGING, Volume 65 (2001) no. 1, pp. 57-60 (Publisher: GROWTH PUBLISHING COMP INC)

[13] Cowin, S.; Hegedus, D. Bone remodeling I: theory of adaptive elasticity, J. Elasticity (1976), p. 6

[14] Cubo, J.; Ponton, F.; Laurin, M.; De Margerie, E.; Castanet, J. Phylogenetic Signal in Bone Microstructure of Sauropsids, Systematic Biology, Volume 54 (2005) no. 4, pp. 562-574 | DOI

[15] Cucchi, T.; Domont, A.; Harbers, H.; Leduc, C.; Guidez, A.; Bridault, A.; Hongo, H.; Price, M.; Peters, J.; Briois, F.; Guilaine, J.; Vigne, J.-D. Bones geometric morphometrics illustrate 10th millennium cal. BP domestication of autochthonous Cypriot wild boar (Sus scrofa circeus nov. ssp), Sci Rep, Volume 11 (2021) no. 1, p. 11435 | DOI

[16] Curran, S. C. Expanding ecomorphological methods: geometric morphometric analysis of Cervidae post-crania, Journal of Archaeological Science, Volume 39 (2012) no. 4, pp. 1172-1182

[17] David, C. C.; Jacobs, D. J. Principal component analysis: a method for determining the essential dynamics of proteins, Protein dynamics, Springer, 2014, pp. 193-226

[18] Divé, J.; Eisenmann, V. Identification and discrimination of first phalanges from Pleistocene and modern Equus, wild and domestic, Beihefte zum Tübinger Atlas des Vorderen Orients. Reihe A, Naturwissenschaften, Volume 19 (1991) no. 2, p. 278

[19] Djukic, K.; Milovanovic, P.; Hahn, M.; Busse, B.; Amling, M.; Djuric, M. Bone microarchitecture at muscle attachment sites: The relationship between macroscopic scores of entheses and their cortical and trabecular microstructural design, American Journal of Physical Anthropology, Volume 157 (2015) no. 1, pp. 81-93 | DOI

[20] Du, T. Y.; Standen, E. M. Terrestrial acclimation and exercise lead to bone functional response in Polypterus senegalus pectoral fins, Journal of Experimental Biology, Volume 223 (2020) no. 11 | DOI

[21] Dumont, M.; Laurin, M.; Jacques, F.; Pellé, E.; Dabin, W.; de Buffrénil, V. Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study, Journal of Morphology, Volume 274 (2013) no. 5, pp. 570-584

[22] Eisenmann, V. What metapodial morphometry has to say about some Miocene Hipparions, Paleoclimate and Evolution, with Emphasis on Human Origins (1995), pp. 148-163

[23] Eisenmann, V. Comparative osteology of modern and fossil horses, half-asses, and asses, Equids in the ancient world, Volume 1 (1986), pp. 67-116

[24] Eisenmann, V.; Beckouche, S. Identification and discrimination of metapodials from Pleistocene and modern Equus, wild and domestic, Beihefte zum Tübinger Atlas des Vorderen Orients. Reihe A, Naturwissenschaften, Volume 19 (1986) no. 1, p. 117

[25] Frost, H. M. A determinant of bone architecture. The minimum effective strain., Clinical orthopaedics and related research (1983) no. 175, pp. 286-292

[26] Frost, H. M. Wolff's Law and bone's structural adaptations to mechanical usage: an overview for clinicians, The Angle Orthodontist, Volume 64 (1994) no. 3, pp. 175-188 | DOI

[27] Fyhrie, D. P.; Carter, D. R. A unifying principle relating stress to trabecular bone morphology, Journal of Orthopaedic Research, Volume 4 (1986) no. 3, pp. 304-317 | DOI

[28] Hall, B. K. Bones and cartilage: developmental and evolutionary biology, Academic Press Inc, Australia ; San Diego, Calif, 2005

[29] Hall, B. K. Epigenetic control in development and evolution, Development and evolution (1983), pp. 353-379

[30] Hall, B. K. Genetic and epigenetic control of vertebrate embryonic development, Netherlands Journal of Zoology, Volume 40 (1989) no. 1-2, pp. 352-361

[31] Hall, R. L.; Shereff, M. J. Anatomy of the calcaneus., Clinical orthopaedics and related research (1993) no. 290, pp. 27-35

[32] Hanot, P.; Herrel, A.; Claude, G.; Cornette, R. Morphological integration in the appendicular skeleton of two domestic taxa: The horse and donkey, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017), p. 20171241 | DOI

[33] Harbers, H.; Neaux, D.; Ortiz, K.; Blanc, B.; Laurens, F.; Baly, I.; Callou, C.; Schafberg, R.; Haruda, A.; Lecompte, F. The mark of captivity: plastic responses in the ankle bone of a wild ungulate (Sus scrofa), Royal Society Open Science, Volume 7 (2020) no. 3, p. 192039

[34] Harbers, H.; Zanolli, C.; Cazenave, M.; Theil, J.-C.; Ortiz, K.; Blanc, B.; Locatelli, Y.; Schafberg, R.; Lecompte, F.; Baly, I.; Laurens, F.; Callou, C.; Herrel, A.; Puymerail, L.; Cucchi, T. Investigating the impact of captivity and domestication on limb bone cortical morphology: an experimental approach using a wild boar model, Scientific Reports, Volume 10 (2020) no. 1, p. 19070 | DOI

[35] Hegedus, D. H.; Cowin, S. C. Bone remodeling II: small strain adaptive elasticity, Journal of elasticity, Volume 6 (1976) no. 4, pp. 337-352

[36] Houssaye, A.; Taverne, M.; Cornette, R. 3D quantitative comparative analysis of long bone diaphysis variations in microanatomy and cross-sectional geometry, Journal of anatomy, Volume 232 (2018) no. 5, pp. 836-849

[37] Huiskes, R.; Ruimerman, R.; van Lenthe, G. H.; Janssen, J. D. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone, Nature, Volume 405 (2000) no. 6787, pp. 704-706 | DOI

[38] Hussain, S. Evolutionary and functional anatomy of the pelvic limb in fossil and recent Equidae (Perissodactyla, Mammalia), Anatomia, Histologia, Embryologia, Volume 4 (1975) no. 3, pp. 193-222

[39] Kappelman, J. Morphology and locomotor adaptations of the bovid femur in relation to habitat, Journal of Morphology, Volume 198 (1988) no. 1, pp. 119-130

[40] Kelly, S. A.; Czech, P. P.; Wight, J. T.; Blank, K. M.; Garland, T. Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice, Journal of Morphology, Volume 267 (2006) no. 3, pp. 360-374 | DOI

[41] Keuling, O.; Stier, N.; Roth, M. Commuting, shifting or remaining?: Different spatial utilisation patterns of wild boar Sus scrofa L. in forest and field crops during summer, Mammalian Biology, Volume 74 (2009) no. 2, pp. 145-152

[42] Kivell, T. L. A review of trabecular bone functional adaptation: what have we learned from trabecular analyses in extant hominoids and what can we apply to fossils?, Journal of Anatomy, Volume 228 (2016) no. 4, pp. 569-594 | DOI

[43] Krølner, B.; Toft, B. Vertebral Bone Loss: An Unheeded Side Effect of Therapeutic Bed Rest, Clinical Science, Volume 64 (1983) no. 5, pp. 537-540 | DOI

[44] Lang, T.; LeBlanc, A.; Evans, H.; Lu, Y.; Genant, H.; Yu, A. Cortical and Trabecular Bone Mineral Loss From the Spine and Hip in Long-Duration Spaceflight, Journal of Bone and Mineral Research, Volume 19 (2004) no. 6, pp. 1006-1012 | DOI

[45] Lanyon, L. E. Analysis of surface bone strain in the calcaneus of sheep during normal locomotion: Strain analysis of the calcaneus, Journal of Biomechanics, Volume 6 (1973) no. 1, pp. 41-49 | DOI

[46] Lanyon, L. E. Control of bone architecture by functional load bearing, Journal of Bone and Mineral Research, Volume 7 (1992) no. S2, p. S369-S375 | DOI

[47] Laros, G. S.; Tipton, C. M.; Cooper, R. R.; Stimmel, P.; Davis, R.; Matthes, R. D. Influence of Physical Activity on Ligament Insertions in the Knees of Dogs, JBJS, Volume 53 (1971) no. 2, pp. 275-286

[48] Lieberman, D. E.; Devlin, M. J.; Pearson, O. M. Articular area responses to mechanical loading: effects of exercise, age, and skeletal location, American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists, Volume 116 (2001) no. 4, pp. 266-277

[49] Lovejoy, C. O.; Cohn, M. J.; White, T. D. Morphological analysis of the mammalian postcranium: a developmental perspective, Proceedings of the National Academy of Sciences, Volume 96 (1999) no. 23, pp. 13247-13252

[50] Maïmoun, L.; Sultan, C. Effects of physical activity on bone remodeling, Metabolism, Volume 60 (2011) no. 3, pp. 373-388 | DOI

[51] Maïmoun, L.; Coste, O.; Philibert, P.; Briot, K.; Mura, T.; Galtier, F.; Mariano-Goulart, D.; Paris, F.; Sultan, C. Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry, Metabolism, Volume 62 (2013) no. 8, pp. 1088-1098 | DOI

[52] Marcus, R. Mechanisms of exercise effects on bone, Principles of bone biology, Elsevier, 2002, pp. 1477-1488

[53] Marinval-Vigne, M.-C.; Mordant, D.; Auboire, G.; Augereau, A.; Bailon, S.; Dauphin, C.; Delibrias, G.; Krier, V.; Leclerc, A.-S.; Leroyer, C.; Marinval, P.; Mordant, C.; Rodriquez, P.; Vilette, P.; Vigne, J.-D. Noyen-sur-Seince, site stratifié en milieu fluviatile: Une étude multidisciplinaire intégrée, Bulletin de la Société préhistorique française, Volume 86 (1989) no. 10/12, pp. 370-379

[54] Martin, R. B. Toward a unifying theory of bone remodeling, Bone, Volume 26 (2000) no. 1, pp. 1-6 | DOI

[55] Modlesky, C. M.; Majumdar, S.; Dudley, G. A. Trabecular bone microarchitecture in female collegiate gymnasts, Osteoporos Int, Volume 19 (2008) no. 7, pp. 1011-1018 | DOI

[56] Mordant, D.; Boris, V.; Vigne, J. Noyen-sur-Seine, vingt cinq ans après, - Société Préhistorique française (2013)

[57] Neaux, D.; Blanc, B.; Ortiz, K.; Locatelli, Y.; Laurens, F.; Baly, I.; Callou, C.; Lecompte, F.; Cornette, R.; Sansalone, G.; Haruda, A.; Schafberg, R.; Vigne, J.-D.; Debat, V.; Herrel, A.; Cucchi, T. How Changes in Functional Demands Associated with Captivity Affect the Skull Shape of a Wild Boar (Sus scrofa), Evol Biol, Volume 48 (2021) no. 1, pp. 27-40 | DOI

[58] Newman, S.; Leeson, S. The effect of dietary supplementation with 1,25-dihydroxycholecalciferol or vitamin C on the characteristics of the tibia of older laying hens, Poultry Science, Volume 78 (1999) no. 1, pp. 85-90 | DOI

[59] Noyes, F.; Delucas, J.; Torvik, P. Biomechanics of Anterior Cruciate Ligament Failure: An Analysis of Strain-Rate Sensitivity and Mechanisms of Failure in Primates, The Journal of bone and joint surgery. American volume, Volume 56 (1974), p. 236-53 | DOI

[60] Palencia, P.; Vicente, J.; Barroso, P.; Barasona, J.; Soriguer, R. C.; Acevedo, P. Estimating day range from camera-trap data: the animals’ behaviour as a key parameter, Journal of Zoology, Volume 309 (2019) no. 3, pp. 182-190

[61] Parfitt, A. M. Targeted and nontargeted bone remodeling: Relationship to basic multicellular unit origination and progression, Bone (NY NY), Volume 30 (2002) no. 1, pp. 5-7

[62] Pearson, O. M.; Lieberman, D. E. The aging of Wolff's “law”: ontogeny and responses to mechanical loading in cortical bone, American journal of physical anthropology, Volume 125 (2004) no. S39, pp. 63-99

[63] Pelletier, M.; Kotiaho, A.; Niinimäki, S.; Salmi, A.-K. Identifying early stages of reindeer domestication in the archaeological record: a 3D morphological investigation on forelimb bones of modern populations from Fennoscandia, Archaeol Anthropol Sci, Volume 12 (2020) no. 8, p. 169 | DOI

[64] Pinhasi, R.; Stock, J. T. Human Bioarchaeology of the Transition to Agriculture, John Wiley & Sons, 2011

[65] Randoin, L.; Cauuseret, J. Experiments on the effect of the phosphorus, calcium, magnesium and vitamin D contents of the diet on bone development in the white rat., Bull: Soc. sci. Hyg. aliment., Volume 33 (1945), pp. 134-143

[66] R Core Team. 2017 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org.

[67] Rath, N. C.; Huff, G. R.; Huff, W. E.; Balog, J. M. Factors Regulating Bone Maturity and Strength in Poultry1, Poultry Science, Volume 79 (2000) no. 7, pp. 1024-1032 | DOI

[68] Robling, A. G.; Castillo, A. B.; Turner, C. H. Biomechanical and molecular regulation of bone remodeling, Annual review of biomedical engineering, Volume 8 (2006) no. 1, pp. 455-498 (Publisher: Palo Alto, Calif.: Annual Reviews, c1999-)

[69] Rossel, S.; Marshall, F.; Peters, J.; Pilgram, T.; Adams, M. D.; O'Connor, D. Domestication of the donkey: Timing, processes, and indicators, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 10, pp. 3715-3720 | DOI

[70] Roux, W. Der Kampf der Theile im Organismus. Ein Beitrag zur Vervollständigung der mechanischen Zweckmässigkeitslehre, 1881

[71] Ruff, C.; Holt, B.; Trinkaus, E. Who's afraid of the big bad Wolff?:“Wolff's law” and bone functional adaptation, American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists, Volume 129 (2006) no. 4, pp. 484-498

[72] Ruff, C. B. Biomechanical analyses of archaeological human skeletons, Biological anthropology of the human skeleton (2018), pp. 189-224 (Publisher: Wiley Online Library)

[73] Ruff, C. B.; Puymerail, L.; Macchiarelli, R.; Sipla, J.; Ciochon, R. L. Structure and composition of the Trinil femora: Functional and taxonomic implications, Journal of human evolution, Volume 80 (2015), pp. 147-158 (Publisher: Elsevier)

[74] Ruimerman, R.; Hilbers, P.; Van Rietbergen, B.; Huiskes, R. A theoretical framework for strain-related trabecular bone maintenance and adaptation, Journal of biomechanics, Volume 38 (2005) no. 4, pp. 931-941 (Publisher: Elsevier)

[75] Rushen, J. The" coping" hypothesis of stereotypic behaviour., Animal Behaviour (1993), p. 45

[76] Russo, L.; Massei, G.; Genov, P. V. Daily home range and activity of wild boar in a Mediterranean area free from hunting, Ethology Ecology & Evolution, Volume 9 (1997) no. 3, pp. 287-294 | DOI

[77] Schriefer, J. L.; Warden, S. J.; Saxon, L. K.; Robling, A. G.; Turner, C. H. Cellular accommodation and the response of bone to mechanical loading, Journal of Biomechanics, Volume 38 (2005) no. 9, pp. 1838-1845 | DOI

[78] Shackelford, L.; Marshall, F.; Peters, J. Identifying donkey domestication through changes in cross-sectional geometry of long bones, Journal of Archaeological Science, Volume 40 (2013) no. 12, pp. 4170-4179 | DOI

[79] Skedros, J. G.; Mason, M. W.; Bloebaum, R. D. Modeling and remodeling in a developing artiodactyl calcaneus: A model for evaluating Frost's Mechanostat hypothesis and its corollaries, The Anatomical Record, Volume 263 (2001) no. 2, pp. 167-185 | DOI

[80] Skedros, J. G.; Sorenson, S. M.; Hunt, K. J.; Holyoak, J. D. Ontogenetic structural and material variations in ovine calcanei: A model for interpreting bone adaptation, The Anatomical Record, Volume 290 (2007) no. 3, pp. 284-300 | DOI

[81] Spitz, F.; Janeau, G. Daily selection of habitat in wild boar (Sus scrofa), Journal of Zoology, Volume 237 (1995) no. 3, pp. 423-434

[82] Spitz, F.; Janeau, G. Spatial strategies: an attempt to classify daily movements of wild boar, Acta Theriologica, Volume 35 (1990) no. 1-2, pp. 129-149

[83] Su, S.; Skedros, J.; Bachus, K.; Bloebaum, R. Loading conditions and cortical bone construction of an artiodactyl calcaneus, Journal of Experimental Biology, Volume 202 (1999) no. 22, pp. 3239-3254 | DOI

[84] Taylor, D. Bone maintenance and remodeling: A control system based on fatigue damage, Journal of Orthopaedic Research, Volume 15 (1997) no. 4, pp. 601-606 | DOI

[85] Trinkaus, E.; Churchill, S. E.; Ruff, C. B. Postcranial robusticity in Homo. II: Humeral bilateral asymmetry and bone plasticity, American Journal of Physical Anthropology, Volume 93 (1994) no. 1, pp. 1-34 | DOI

[86] Turner, C. H. Toward a mathematical description of bone biology: the principle of cellular accommodation, Calcif Tissue Int, Volume 65 (1999) no. 6, pp. 466-471 | DOI

[87] Turner, C. H. Three rules for bone adaptation to mechanical stimuli, Bone, Volume 23 (1998) no. 5, pp. 399-407 (Publisher: Elsevier)

[88] Turner, C. H.; Owan, I.; Takano, Y. Mechanotransduction in bone: role of strain rate, American Journal of Physiology-Endocrinology And Metabolism, Volume 269 (1995) no. 3, p. E438-E442 (Publisher: American Physiological Society Bethesda, MD)

[89] Van der Meulen, M. C. H.; Morgan, T. G.; Yang, X.; Baldini, T. H.; Myers, E. R.; Wright, T. M.; Bostrom, M. P. G. Cancellous bone adaptation to in vivo loading in a rabbit model, Bone, Volume 38 (2006) no. 6, pp. 871-877 | DOI

[90] Vigne, J.-D.; Carrere, I.; Briois, F.; Guilaine, J. The early process of mammal domestication in the Near East: New evidence from the Pre-Neolithic and Pre-Pottery Neolithic in Cyprus, Current Anthropology, Volume 52 (2011) no. S4, p. S255-S271

[91] Vlachopoulos, D.; Barker, A. R.; Ubago-Guisado, E.; Fatouros, I. G.; Knapp, K. M.; Williams, C. A.; Gracia-Marco, L. Longitudinal Adaptations of Bone Mass, Geometry, and Metabolism in Adolescent Male Athletes: The PRO-BONE Study, Journal of Bone and Mineral Research, Volume 32 (2017) no. 11, pp. 2269-2277

[92] Wolff, J. "The Law of Bone Remodeling" (translation of the German 1892 edition by P. Maquet and R. Furlong), Springer-Verlag, Berlin Heidelberg, 1986 | DOI

[93] Woo, S.-L.; Kuei, S. C.; Amiel, D.; Gomez, M. A.; Hayes, W. C.; White, F. C.; Akeson, W. H. The effect of prolonged physical training on the properties of long bone: a study of Wolff's Law., The Journal of bone and joint surgery. American volume, Volume 63 (1981) no. 5, pp. 780-787

[94] Zanker, C. L.; Swaine, I. L. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction, Eur J Appl Physiol, Volume 83 (2000) no. 4, pp. 434-440 | DOI

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