Mechanical and energetic scaling relationships of running gait through ontogeny in the ostrich (Struthio camelus)

SUMMARY It is unclear whether small animals, with their high stride frequency and crouched posture, or large animals, with more tendinous limbs, are more reliant on storage and return of elastic energy during locomotion. The ostrich has a limb structure that appears to be adapted for high-speed running with long tendons and short muscle fibres. Here we investigate biomechanics of ostrich gait through growth and, with consideration of anatomical data, identify scaling relationships with increasing body size, relating to forces acting on the musculoskeletal structures, effective mechanical advantage (EMA) and mechanical work. Kinematic and kinetic data were collected through growth from running ostriches. Joint moments scaled in a similar way to the pelvic limb segments as a result of consistent posture through growth, such that EMA was independent of body mass. Because no postural change was observed, relative loads applied to musculoskeletal tissues would be predicted to increase during growth, with greater muscle, and hence tendon, load allowing increased potential for elastic energy storage with increasing size. Mass-specific mechanical work per unit distance was independent of body mass, resulting in a small but significant increase in the contribution of elastic energy storage to locomotor economy in larger ostriches.

[1]  R. McN. Alexander,et al.  Mechanics of running of the ostrich (Struthio camelus) , 2009 .

[2]  A. R. Biknevicius,et al.  Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods. , 2007, Zoology.

[3]  R. Alexander,et al.  A dynamic similarity hypothesis for the gaits of quadrupedal mammals , 2009 .

[4]  Oded Bar-Or,et al.  Explaining differences in the metabolic cost and efficiency of treadmill locomotion in children , 2002, Journal of sports sciences.

[5]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.

[6]  G. Cavagna,et al.  Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. , 1977, The American journal of physiology.

[7]  R. M. Alexander Models and the scaling of energy costs for locomotion , 2005, Journal of Experimental Biology.

[8]  N. Schenker,et al.  Overlapping confidence intervals or standard error intervals: What do they mean in terms of statistical significance? , 2003, Journal of insect science.

[9]  D. Carrier Postnatal ontogeny of the musculo-skeletal system in the Black-tailed jack rabbit (Lepus californicus) , 2009 .

[10]  A. Biewener Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. , 1983, The Journal of experimental biology.

[11]  Alan M. Wilson,et al.  Ontogenetic scaling of locomotor kinetics and kinematics of the ostrich (Struthio camelus) , 2010, Journal of Experimental Biology.

[12]  N. Heglund,et al.  Energetics and mechanics of terrestrial locomotion. , 1982, Annual review of physiology.

[13]  R. Shadwick,et al.  Elastic energy storage in tendons: mechanical differences related to function and age. , 1990, Journal of applied physiology.

[14]  A. Biewener,et al.  Ontogenetic patterns of limb loading, in vivo bone strains and growth in the goat radius , 2004, Journal of Experimental Biology.

[15]  G. Lichtwark,et al.  Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion , 2006, Journal of Experimental Biology.

[16]  A. Biewener,et al.  In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. , 1998, The Journal of experimental biology.

[17]  L. S. Matthews,et al.  Viscoelastic properties of cat tendon: effects of time after death and preservation by freezing. , 1968, Journal of biomechanics.

[18]  Alan M. Wilson,et al.  Muscle architecture and functional anatomy of the pelvic limb of the ostrich (Struthio camelus) , 2006, Journal of anatomy.

[19]  Lei Ren,et al.  Integration of biomechanical compliance, leverage, and power in elephant limbs , 2010, Proceedings of the National Academy of Sciences.

[20]  G. Cavagna,et al.  External, internal and total work in human locomotion. , 1995, The Journal of experimental biology.

[21]  K Schmidt-Nielsen,et al.  Scaling in biology: the consequences of size. , 1975, The Journal of experimental zoology.

[22]  Sharon R Bullimore,et al.  Distorting limb design for dynamically similar locomotion , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  A. Wilson,et al.  Muscle moment arms of pelvic limb muscles of the ostrich (Struthio camelus) , 2007, Journal of anatomy.

[24]  Robilliard Jj Mechanical basis of locomotion with spring-like legs. , 2006 .

[25]  J. Young Ontogeny of muscle mechanical advantage in capuchin monkeys (Cebus albifrons and Cebus apella) , 2005 .

[26]  Pierre Boher,et al.  A transmission electron microscopy study of low‐temperature reaction at the Co‐Si interface , 1990 .

[27]  K. Hayashi,et al.  Growth-related changes in the mechanical properties of collagen fascicles from rabbit patellar tendons. , 2004, Biorheology.

[28]  A. Casinos,et al.  Limb allometry in birds , 1996 .

[29]  A. Biewener,et al.  Skeletal strain patterns and growth in the emu hindlimb during ontogeny , 2007, Journal of Experimental Biology.

[30]  Jonas Rubenson,et al.  Adaptations for economical bipedal running: the effect of limb structure on three-dimensional joint mechanics , 2011, Journal of The Royal Society Interface.

[31]  E. H. Harris,et al.  Stress-strain characteristics and tensile strength of unembalmed human tendon. , 1968, Journal of biomechanics.

[32]  Rodger Kram,et al.  Energetics of running: a new perspective , 1990, Nature.

[33]  Sharon R Bullimore,et al.  Dynamically similar locomotion in horses , 2006, Journal of Experimental Biology.

[34]  M. B. Bennett,et al.  Scaling of elastic strain energy in kangaroos and the benefits of being big , 1995, Nature.

[35]  Jonas Rubenson,et al.  Gait selection in the ostrich: mechanical and metabolic characteristics of walking and running with and without an aerial phase , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  J. Horbańczuk,et al.  Wild ostrich (Struthio camelus) ecology and physiology , 2010, Tropical Animal Health and Production.

[37]  Nicola Jones,et al.  Functional specialization and ontogenetic scaling of limb anatomy in Alligator mississippiensis , 2010, Journal of anatomy.

[38]  S. Bullimore,et al.  Scaling of elastic energy storage in mammalian limb tendons: do small mammals really lose out? , 2005, Biology Letters.

[39]  G. Cavagna,et al.  Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. , 1982, The Journal of experimental biology.

[40]  C. R. Taylor,et al.  Relating mechanics and energetics during exercise. , 1994, Advances in veterinary science and comparative medicine.

[41]  R. Alexander,et al.  Allometry of the legs of running birds , 2009 .

[42]  R. Shadwick,et al.  Allometry of muscle, tendon, and elastic energy storage capacity in mammals. , 1994, The American journal of physiology.

[43]  R. Alexander,et al.  Allometry of the leg muscles of mammals , 1981 .

[44]  A. Biewener Biomechanical consequences of scaling , 2005, Journal of Experimental Biology.

[45]  R. McN. Alexander,et al.  Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta) , 2009 .

[46]  R. McN. Alexander,et al.  Fast locomotion of some African ungulates , 2009 .

[47]  R. Shadwick,et al.  Relationship between body mass and biomechanical properties of limb tendons in adult mammals. , 1994, The American journal of physiology.

[48]  T. McMahon,et al.  The mechanics of running: how does stiffness couple with speed? , 1990, Journal of biomechanics.

[49]  R. Blickhan The spring-mass model for running and hopping. , 1989, Journal of biomechanics.

[50]  A. Biewener,et al.  Muscle-tendon stresses and elastic energy storage during locomotion in the horse. , 1998, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[51]  C. T. Farley,et al.  Running springs: speed and animal size. , 1993, The Journal of experimental biology.

[52]  G. Lichtwark,et al.  Effects of series elasticity and activation conditions on muscle power output and efficiency , 2005, Journal of Experimental Biology.

[53]  A. Biewener Scaling body support in mammals: limb posture and muscle mechanics. , 1989, Science.

[54]  A. Minetti,et al.  The relationship between mechanical work and energy expenditure of locomotion in horses. , 1999, The Journal of experimental biology.

[55]  Alan M. Wilson,et al.  Centre of mass movement and mechanical energy fluctuation during gallop locomotion in the Thoroughbred racehorse , 2006, Journal of Experimental Biology.

[56]  A. Biewener Biomechanics of mammalian terrestrial locomotion. , 1990, Science.

[57]  Andrew A Biewener,et al.  Muscle mechanical advantage of human walking and running: implications for energy cost. , 2004, Journal of applied physiology.

[58]  N. Heglund,et al.  Energetics and mechanics of terrestrial locomotion. II. Kinetic energy changes of the limbs and body as a function of speed and body size in birds and mammals. , 1982, The Journal of experimental biology.

[59]  P A Huijing,et al.  Properties of the tendinous structures and series elastic component of EDL muscle-tendon complex of the rat. , 1989, Journal of biomechanics.

[60]  Andrew A Biewener,et al.  Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control , 2007, Journal of Experimental Biology.

[61]  Denham B. Heliams,et al.  Running in ostriches (Struthio camelus): three-dimensional joint axes alignment and joint kinematics , 2007, Journal of Experimental Biology.