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Linearity in the Real World: An Experimental Assessment of Nonlinearity in Terrestrial Locomotion

  • Kristian J. CarlsonEmail author
Chapter

Abstract

Amongst early human ancestors, cross-sectional geometric properties of lower limb bones are particularly useful for reconstructing mobility patterns. Experimental studies of diaphyseal loads characterizing locomotor activities, however, demonstrate disconnect with theoretical loads predicted from bone morphology alone. This complicates population-level comparisons, and makes specific behavioral inferences tenuous. Lack of a consistent definition for mobility further complicates comparisons. To contribute towards a consensus definition of mobility, here I address one specific relevant factor— what are the effects of nonlinear locomotion or turning. Mice in custom-designed cages accentuating turning (condition 1) and linear movement (condition 2) were compared with mice (control) permitted to move freely in cages. Locomotor behavior of individuals was documented multiple times per day. At the end of the experiment, limb bones were harvested, scanned with high resolution CT, and subjected to structural analyses. Comparing growing BALB/cByJ female mice from a previous experiment and growing C57BL/6J female mice (n = 30, 10 per group) in the present experiment, permits comparisons of structural effects of movement regimes on femoral cortical areas, second moments of area, polar moment of area, and shape ratios, as well as activity profiles. C57BL/6J groups differed in activity level, while BALB/cByJ groups did not. Mice in turning groups tended to have more elliptical diaphyses, while linear and control mice differed comparatively less often. Distinctive diaphyseal shapes in turning mice support the idea that nonlinear movements (e.g., turning) have recognizable effects on long bone diaphyseal structure. This suggests limb loading, likely in side-to-side orientations, is relatively high during turning compared to linear movement.

Keywords

Mobility Femur Bone functional adaptation Mediolateral Positional behavior Turning Mouse 

Notes

Acknowledgments

I am grateful to the NYIT College of Osteopathic Medicine (Old Westbury, NY) Office of Research for funding this research. I also wish to thank the Institute for Human Evolution, University of the Witwatersrand for providing the funding that permitted travel to the 2011 AAPA conference. I wish to thank Kurt Amsler, Abe Furia, Liza Nicholson, Kathleen O’Rourke, Sunny Hwang, Brian Beatty, Ryan Palevsky, and several other NYCOM students and staff for their assistance with animal care at various points over the duration of this project. I would like to thank Stefan Judex for sharing his exceptional insights into bone functional adaptations throughout this project. I am extremely grateful to Mark Dowdeswell for advice on selecting and performing statistical analyses, and for other comments on the project. I wish to thank Damiano Marchi and one anonymous reviewer for constructive comments provided on earlier versions of this chapter.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  2. Barak MM, Lieberman DE, Hublin JJ (2011) A Wolff in sheep’s clothing: trabecular bone adaptation in response to changes in joint loading orientation. Bone 49:1141–1151PubMedCrossRefGoogle Scholar
  3. Beamer WG, Donahue LR, Rosen CJ (2002) Genetics and bone: using the mouse to understand man. J Musculoskel Neuron Interact 2:225–231Google Scholar
  4. Binford LR (2001) Constructing frames of reference—an analytical method for archaeological theory building using hunter-gatherer and environmental data sets. University of California Press, Berkeley, CAGoogle Scholar
  5. Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A (1996) In vivo measurement of human tibial strains during vigorous activity. Bone 18:405–410PubMedCrossRefGoogle Scholar
  6. Carlson KJ (2005) Investigating the form-function interface in African apes, relationships between principal moments of area and positional behaviors in femoral and humeral diaphyses. Am J Phys Anthropol 127:312–334PubMedCrossRefGoogle Scholar
  7. Carlson KJ, Byron CD (2008) Building a better organismal model: the role of the mouse—introduction to the symposium. Integr Comp Biol 48:321–323PubMedCrossRefGoogle Scholar
  8. Carlson KJ, Judex S (2007) Increased non-linear locomotion alters diaphyseal bone shape. J Exp Biol 210:3117–3125PubMedCrossRefGoogle Scholar
  9. Carlson KJ, Grine FE, Pearson OM (2007) Robusticity and sexual dimorphism in the postcranium of modern hunter-gatherers from Australia. Am J Phys Anthropol 134:9–23PubMedCrossRefGoogle Scholar
  10. Carlson KJ, Lublinsky S, Judex S (2008a) Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb? Integr Comp Biol 48:385–393PubMedCrossRefGoogle Scholar
  11. Carlson KJ, Sumner DR, Morbeck ME, Nishida T, Yamanaka A, Boesch C (2008b) Role of nonbehavioral factors in adjusting long bone diaphyseal structure in free-ranging Pan troglodytes. Int J Primatol 29:1401–1420PubMedCentralPubMedCrossRefGoogle Scholar
  12. Daley MA, Biewener AA (2006) Running over rough terrain reveals limb control for intrinsic stability. Proc Natl Acad Sci U S A 103:15681–15686PubMedCentralPubMedCrossRefGoogle Scholar
  13. Daley MA, Usherwood JR, Felix G, Biewener AA (2006) Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height. J Exp Biol 209:171–187PubMedCrossRefGoogle Scholar
  14. 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 106:87–100PubMedCrossRefGoogle Scholar
  15. Demes B, Qin Y, Stern JT Jr, Larson SG, Rubin CT (2001) Patterns of strain in the macaque tibia during functional activity. Am J Phys Anthropol 116:257–265PubMedCrossRefGoogle Scholar
  16. Demes B, Carlson KJ, Franz TM (2006) Cutting corners: the dynamics of turning behaviors in two primate species. J Exp Biol 209:927–937PubMedCrossRefGoogle Scholar
  17. Flurkey K, Currer JM, Harrison DE (2007) Mouse models in aging research. In: Fox JG, Davisson MT, Quimby FW, Barthold SW, Newcomer CE, Smith AL (eds) The mouse in biomedical research. Academic, Amsterdam, pp 637–672CrossRefGoogle Scholar
  18. Green DJ, Hamrick MW, Richmond BG (2011) The effects of hypermuscularity on shoulder morphology in myostatin-deficient mice. J Anat 218:544–557PubMedCentralPubMedCrossRefGoogle Scholar
  19. Higgins RW (2014) The effects of terrain on long bone robusticity and cross-sectional shape in the lower limb bones of bovids, Neanderthals, and Upper Paleolithic modern humans. In: Carlson KJ, Marchi D (eds) Reconstructing mobility: environmental, behavioral, and morphological determinants. Springer Press, New YorkGoogle Scholar
  20. Hunt KD, Cant JGH, Gebo DL, Rose MD, Walker SE (1996) Standardized descriptions of primate locomotor and postural modes. Primates 37:363–387CrossRefGoogle Scholar
  21. Judex S, Carlson KJ (2009) Is bone’s response to mechanical signals dominated by gravitational loading? Med Sci Sports Exerc 41:2037–2043PubMedCrossRefGoogle Scholar
  22. Judex S, Donahue LR, Rubin C (2002) Genetic predisposition to low bone mass is paralleled by an enhanced sensitivity to signals anabolic to the skeleton. FASEB J 16:1280–1282PubMedGoogle Scholar
  23. Kelly RL (1995) The foraging spectrum—diversity in hunter-gatherer lifeways. Smithsonian Institution Press, WashingtonGoogle Scholar
  24. Lieberman DE, Polk JD, Demes B (2004) Predicting long bone loading from cross-sectional geometry. Am J Phys Anthropol 123:156–171PubMedCrossRefGoogle Scholar
  25. Marchi D (2008) Relationships between lower limb cross-sectional geometry and mobility: the case of a Neolithic sample from Italy. Am J Phys Anthropol 137:188–200PubMedCrossRefGoogle Scholar
  26. Marchi D, Shaw CN (2011) Variation in fibular robusticity reflects variation in mobility patterns. J Hum Evol 61:609–616PubMedCrossRefGoogle Scholar
  27. Marchi D, Sparacello V, Shaw CN (2011) Mobility and lower limb robusticity of a pastoralist Neolithic population from north-western Italy. In: Pinhasi R, Stock JT (eds) Human bioarchaeology of the transition to agriculture. Wiley-Blackwell, Oxford, pp 317–346CrossRefGoogle Scholar
  28. Milgrom C, Finestone A, Levi Y, Simkin A, Ekenman I, Mendelson S, Millgram M, Nyska M, Benjuya N, Burr D (2000) Do high impact exercises produce higher tibial strains than running? Br J Sports Med 34:195–199PubMedCentralPubMedCrossRefGoogle Scholar
  29. Moreno CA, Main RP, Biewener AA (2008) Variability in forelimb bone strains during non-steady locomotor activities in goats. J Exp Biol 211:1148–1162PubMedCrossRefGoogle Scholar
  30. Nagurka ML, Hayes WC (1980) An interactive graphics package for calculating cross-sectional properties of complex shapes. J Biomech 13:59–64PubMedCrossRefGoogle Scholar
  31. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610PubMedCrossRefGoogle Scholar
  32. Pearson OM, Lieberman DE (2004) The aging of Wolff’s “Law”: ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthropol 47:63–99CrossRefGoogle Scholar
  33. Prost JH (1965) A definitional system for the classification of primate locomotion. Am Anthropol 67:1198–1214CrossRefGoogle Scholar
  34. Ruff CB (1999) Skeletal structure and behavioral patterns of prehistoric Great Basin populations. In: Hemphill BE, Larsen CS (eds) Prehistoric lifeways in the Great Basin wetlands: bioarchaeological reconstruction and interpretation. University of Utah Press, Salt Lake City, pp 290–320Google Scholar
  35. Ruff CB (2009) Relative limb strength and locomotion in Homo habilis. Am J Phys Anthropol 138:90–100PubMedCrossRefGoogle Scholar
  36. Ruff CB, Larsen CS (2014) Long bone structural analyses and the reconstruction of past mobility: a historical review. In: Carlson KJ, Marchi D (eds) Reconstructing mobility: environmental, behavioral, and morphological determinants. Springer, New YorkGoogle Scholar
  37. Ruff CB, Runestad JA (2002) Primate limb bone structural adaptations. Annu Rev Anthropol 21:407–433CrossRefGoogle Scholar
  38. Ruff CB, Larsen CS, Hayes WC (1984) Structural changes in the femur with the transition to agriculture on the Georgia Coast. Am J Phys Anthropol 64:125–136PubMedCrossRefGoogle Scholar
  39. Ruff CB, Trinkaus E, Walker A, Larsen CS (1993) Postcranial robusticity in Homo. I. Temporal trends and mechanical interpretation. Am J Phys Anthropol 91:21–53PubMedCrossRefGoogle Scholar
  40. 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 129:484–498PubMedCrossRefGoogle Scholar
  41. Schmitt D, Zumwalt AC, Hamrick MW (2010) The relationship between bone mechanical properties and ground reaction forces in normal and hypermuscular mice. J Exp Zool A Ecol Genet Physiol 313:339–351PubMedCentralPubMedCrossRefGoogle Scholar
  42. Shaw CN, Stock JT (2009a) Intensity, repetitiveness, and directionality of habitual adolescent mobility patterns influence the tibial diaphysis morphology of athletes. Am J Phys Anthropol 140:149–159PubMedCrossRefGoogle Scholar
  43. Shaw CN, Stock JT (2009b) Habitual throwing and swimming correspond with upper limb diaphyseal strength and shape in modern human athletes. Am J Phys Anthropol 140:160–172PubMedCrossRefGoogle Scholar
  44. Sparacello V, Marchi D (2008) Mobility and subsistence economy: a diachronic comparison between two groups settled in the same geographical area (Liguria, Italy). Am J Phys Anthropol 136:485–495PubMedCrossRefGoogle Scholar
  45. Sparacello VS, Marchi D, Shaw CN (2014) The importance of considering fibular robusticity when inferring the mobility patterns of past populations. In: Carlson KJ, Marchi D (eds) Reconstructing mobility: environmental, behavioral, and morphological determinantsGoogle Scholar
  46. Stock JT, Pfeiffer SK (2001) Linking structural variability in long bone diaphyses to habitual behaviours: foragers from the Southern African Later Stone Age and the Andaman Islands. Am J Phys Anthropol 115:337–348PubMedCrossRefGoogle Scholar
  47. Stock JT, Pfeiffer SK (2004) Long bone robusticity and subsistence behaviour among Later Stone Age foragers of the forest and fynbos biomes of South Africa. J Archaeol Sci 31:999–1013CrossRefGoogle Scholar
  48. Sugiyama T, Price JS, Lanyon LS (2010) Functional adaptation to mechanical loading in both cortical and cancellous bone is controlled locally and is confined to the loaded bones. Bone 46:314–321PubMedCentralPubMedCrossRefGoogle Scholar
  49. Trinkaus E, Stringer CB, Ruff CB, Hennessy RJ, Roberts MB, Parfitt SA (1999) Diaphyseal cross-sectional geometry of the Boxgrove I Middle Pleistocene human tibia. J Hum Evol 37:1–25PubMedCrossRefGoogle Scholar
  50. Voloshina AS, Kuo AD, Daley MA, Ferris DP (2013) Biomechanics and energetics of walking on uneven terrain. J Exp Biol 216:3963–3970PubMedCrossRefGoogle Scholar
  51. Wallace IJ, Tommasini SM, Judex S, Garland T Jr, Demes B (2012) Genetic variations and physical activity as determinants of limb bone morphology: an experimental approach using a mouse model. Am J Phys Anthropol 148:24–35PubMedCrossRefGoogle Scholar
  52. Wallace IJ, Kwaczala AT, Judex S, Demes B, Carlson KJ (2013) Physical activity engendering loads from diverse directions augments the growing skeleton. J Musculoskel Neuron Interact 13:245–250Google Scholar
  53. Wergedal JE, Sheng MHC, Ackert-Bicknell CL, Beamer WG, Baylink DJ (2005) Genetic variation in femur extrinsic strength in 29 different inbred strains of mice is dependent on variations in femur cross-sectional geometry and bone density. Bone 36:111–122PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Evolutionary Studies Institute, Palaeosciences CentreUniversity of the WitwatersrandJohannesburgSouth Africa
  2. 2.School of GeosciencesUniversity of the WitwatersrandJohannesburgSouth Africa
  3. 3.Department of AnthropologyIndiana UniversityBloomingtonUSA

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