Molecules, muscles, and machines: Universal performance characteristics of motors

Animal- and human-made motors vary widely in size and shape, are constructed of vastly different materials, use different mechanisms, and produce an enormous range of mass-specific power. Despite these differences, there is remarkable consistency in the maximum net force produced by broad classes of animal- and human-made motors. Motors that use force production to accomplish steady translational motion of a load (myosin, kinesin, dynein, and RNA polymerase molecules, muscle cells, whole muscles, winches, linear actuators, and rockets) have maximal force outputs that scale as the two-thirds power of mass, i.e., with cross-sectional area. Motors that use cyclical motion to generate force and are more subject to multiaxial stress and vibration have maximal force outputs that scale as a single isometric function of motor mass with mass-specific net force output averaging 57 N⋅kg−1 (SD = 14). Examples of this class of motors includes flying birds, bats, and insects, swimming fish, various taxa of running animals, piston engines, electric motors, and all types of jets. Dependence of force production and stress resistance on cross-sectional area is well known, but the isometric scaling and common upper limit of mass-specific force production by cyclical motion motors has not been recognized previously and is not explained by an existing body of theory. Remarkably, this finding indicates that most of the motors used by humans and animals for transportation have a common upper limit of mass-specific net force output that is independent of materials and mechanisms.

[1]  Jack L. Kerrebrock,et al.  Aircraft Engines and Gas Turbines , 1977 .

[2]  J. Marden Short Communication: Maximum Load-Lifting and Induced Power Output of Harris' Hawks are General Functions of Flight Muscle Mass , 1990 .

[3]  Didier Sornette,et al.  Scale Invariance and Beyond , 1997 .

[4]  S. D. Senturia,et al.  Macro Power from Micro Machinery , 1997, Science.

[5]  S Fukunaga,et al.  In vitro evaluation of linear motor-driven total artificial heart. , 2008, Artificial organs.

[6]  C. Poggesi,et al.  The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. , 2000, Biophysical journal.

[7]  Marden,et al.  Maturational changes in troponin T expression, Ca2+-sensitivity and twitch contraction kinetics in dragonfly flight muscle , 1997, The Journal of experimental biology.

[8]  Marden Evolutionary adaptation of contractile performance in muscle of ectothermic winter-flying moths , 1995, The Journal of experimental biology.

[9]  C. Lindemann,et al.  Measurement of the force produced by an intact bull sperm flagellum in isometric arrest and estimation of the dynein stall force. , 2000, Biophysical journal.

[10]  H. Berg Random Walks in Biology , 2018 .

[11]  R. Marsh,et al.  Contractile properties of the striated adductor muscle in the bay scallop Argopecten irradians at several temperatures. , 1993, The Journal of experimental biology.

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

[13]  Alexander Rm,et al.  The maximum forces exerted by animals. , 1985 .

[14]  J. Marden Maximum Lift Production During Takeoff in Flying Animals , 1987 .

[15]  L. Mahadevan,et al.  Motility powered by supramolecular springs and ratchets. , 2000, Science.

[16]  J. Spudich,et al.  Single myosin molecule mechanics: piconewton forces and nanometre steps , 1994, Nature.

[17]  David Cebon,et al.  Materials Selection in Mechanical Design , 1992 .

[18]  P W Brandt,et al.  Force regulation by Ca2+ in skinned single cardiac myocytes of frog. , 1998, Biophysical journal.

[19]  Paavo V. Komi,et al.  Force-, power-, and elasticity-velocity relationships in walking, running, and jumping , 2004, European Journal of Applied Physiology and Occupational Physiology.

[20]  Michelle D. Wang,et al.  Force and velocity measured for single molecules of RNA polymerase. , 1998, Science.

[21]  P. Chai,et al.  Flight and size constraints: hovering performance of large hummingbirds under maximal loading. , 1997, The Journal of experimental biology.

[22]  R. Blickhan,et al.  Leg design in hexapedal runners. , 1991, The Journal of experimental biology.

[23]  John Tyler Bonner,et al.  On size and life , 1983 .

[24]  R. Blickhan,et al.  Muscle forces during locomotion in kangaroo rats: force platform and tendon buckle measurements compared. , 1988, The Journal of experimental biology.

[25]  S. Peters,et al.  Sexual dimorphism in forelimb muscles of the bullfrog, Rana catesbeiana: a functional analysis of isometric contractile properties. , 2000, The Journal of experimental biology.

[26]  M. Schnitzer,et al.  Force production by single kinesin motors , 2000, Nature Cell Biology.

[27]  James H. Marden,et al.  Aerial Predation and Butterfly Design: How Palatability, Mimicry, and the Need for Evasive Flight Constrain Mass Allocation , 1991, The American Naturalist.

[28]  T. Yanagida,et al.  Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. , 1999, Science.

[29]  The energetic cost of activation of white muscle fibres from the dogfish Scyliorhinus canicula , 1997, The Journal of experimental biology.

[30]  Paul W. Webb,et al.  Fast-start Performance and Body Form in Seven Species of Teleost Fish , 1978 .

[31]  R. Josephson,et al.  Power output by an asynchronous flight muscle from a beetle. , 2000, The Journal of experimental biology.

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

[33]  Toshio Yanagida,et al.  Dynein arms are oscillating force generators , 1998, Nature.

[34]  Paul W. Webb,et al.  MECHANICS OF ESCAPE RESPONSES IN CRAYFISH (ORCONECTES VIRILIS) , 1979 .

[35]  D R Carrier,et al.  Epaxial muscle function in trotting dogs. , 2001, The Journal of experimental biology.

[36]  A. Biewener,et al.  Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). , 2001, The Journal of experimental biology.

[37]  G. Ettema Elastic and length-force characteristics of the gastrocnemius of the hopping mouse (Notomys alexis) and the rat (Rattus norvegicus). , 1996, The Journal of experimental biology.

[38]  M. Dickinson,et al.  The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. , 1997, The Journal of experimental biology.