Abstract
Hunting spiders are well adapted to fast locomotion. Space saving hydraulic leg extension enables leg segments, which consist almost soley of flexor muscles. As a result, the muscle cross sectional area is high despite slender legs. Considering these morphological features in context with the spider’s segmented C-shaped legs, these specifics might influence the spider’s muscle properties. Moreover, these properties have to be known for modeling of spider locomotion. Cupiennius salei (n = 5) were fixed in a metal frame allowing exclusive flexion of the tibia–metatarsus joint of the second leg (counted from anterior). Its flexing muscles were stimulated supramaximally using needle electrodes. Accounting for the joint geometry, the force–length and the force–velocity relationships were determined. The spider muscles produce 0.07 N cm maximum isometric moment (corresponding to 25 N/cm2 maximum stress) at 160° tibia–metatarsus joint angle. When overextended to the dorsal limit at approximately 200°, the maximum isometric moments decrease to 72%, and, when flexed to the ventral hinge stop at 85°, they drop to 11%. The force–velocity relation shows the typical hyperbolic shape. The mean maximum shortening velocity is 5.7 optimum muscle lengths per second and the mean curvature (a/F iso) of the Hill-function is 0.34. The spider muscle’s properties which were determined are similar to those of other species acting as motors during locomotion (working range, curvature of Hill hyperbola, peak power at the preferred speeds), but they are relatively slow. In conjunction with the low mechanical advantage (muscle lever/load arm), the arrangement of three considerably actuated joints in series may nonetheless enable high locomotion velocities.
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References
Ahn AN, Full RJ (2002) A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. J Exp Biol 205:379–389
Ahn AN, Meijer K, Full RJ (2006) In situ muscle power differs without varying in vitro mechanical properties in two insect leg muscles innervated by the same motor neuron. J Exp Biol 209:3370–3382
Alexander RM (1985) The maximum forces exerted by animals. J Exp Biol 115:231–238
Anderson JF, Prestwich KN (1975) The fluid pressure pumps of spiders (Chelicerata, Araneae). Z Morph Tiere 81:257–277
Baratta RV, Solomonow M, Best R, Zembo M, D’Ambrosia R (1995) Force–velocity relations of nine load-moving skeletal muscles. Med Biol Eng Comput 33:537–544
Bennett AF (1985) Temperature and muscle. J Exp Biol 115:333–344
Biewener AA (1989) Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48
Biewener AA (1998) Muscle function in vivo: a comparison of muscles used for elastic energy storage savings versus muscles used to generate power. Am Zool 38:703–717
Blickhan R, Barth FG (1985) Strains in the exoskeleton of spiders. J Comp Physiol A 157:115–147
Blickhan R, Wagner H, Seyfahrt A (2003) Brain or muscles? Recent Res Devel Biomech 1:215–245
Blickhan R, Petkun S, Weihmann T, Karner M (2005) Schnelle Bewegungen bei Arthropoden: Strategien und Mechanismen. In: Pfeiffer F, Cruse H (eds) Autonomes Laufen. Springer, Berlin, pp 19–45
Blickhan R, Seyfarth A, Geyer H, Grimmer S, Wagner H, Gunther M (2007) Intelligence by mechanics. Philos Transact A Math Phys Eng Sci 365:199–220
Brown IE, Loeb GE (2000) A reductionistic approach to creating and using neuro-musculoskeletal models. In: Winters JM, Crago PE (eds) Biomechanics and neural control of posture and movement. Springer, New York
Brown IE, Cheng EJ, Loeb GE (1999) Measured and modeled properties of mammalian skeletal muscle. II. The effects of stimulus frequency on force–length and force–velocity relationships. J Muscle Res Cell Motil 20:627–643
Clarke J (1986) The comparative functional morphology of the leg joints and muscles of five spiders. Bull Brarachnol Soc 7:37–47
Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197
Curtin NA, Gardner-Medwin AR, Woledge RC (1998) Predictions of the time course of force and power output by dogfish white muscle fibres during brief tetani. J Exp Biol 201:103–114
de Haan A (1998) The influence of stimulation frequency on force–velocity characteristics of in situ rat medial gastrocnemius muscle. Exp Physiol 83:77–84
Dillon LS (1952) The myology of the araneid leg. J Morphol 90:467–480
Edman KA (2005) Contractile properties of mouse single muscle fibers, a comparison with amphibian muscle fibers. J Exp Biol 208:1905–1913
Ehlers M (1939) Untersuchungen über Formen aktiver Lokomotion bei Spinnen. Zool Jb Syst 72:373 ff
Ellis CH (1944) The mechanism of extension in the legs of spiders. Biol Bull 86:41–50
Fenn WO, Marsh BS (1935) Muscular force at different speeds of shortening. J Physiol 85:277–297
Full R, Ahn A (1995) Static forces and moments generated in the insect leg: comparison of a three-dimensional musculo-skeletal computer model with experimental measurements. J Exp Biol 198:1285–1298
Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192
Guschlbauer C, Scharstein H, Buschges A (2007) The extensor tibiae muscle of the stick insect: biomechanical properties of an insect walking leg muscle. J Exp Biol 210:1092–1108
Herzog W, Leonard TR, Renaud JM, Wallace J, Chaki G, Bornemisza S (1992) Force–length properties and functional demands of cat gastrocnemius, soleus and plantaris muscles. J Biomech 25:1329–1335
Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc London Ser B, Biol Sci 126:136–195
Josephson RK (1984) Contraction dynamics of flight and stridulatory muscles of tettigoniid insects. J Exp Biol 108:77–96
Josephson RK (1993) Contraction dynamics and power output of skeletal muscle. Annu Rev Physiol 55:527–546
Joyce GC, Rack PM, Westbury DR (1969) The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J Physiol 204:461–474
Leedham JS, Dowling JJ (1995) Force–length, torque–angle and EMG-joint angle relationships of the human in vivo biceps brachii. Eur J Appl Physiol Occup Physiol 70:421–426
Lutz GJ, Rome LC (1996) Muscle function during jumping in frogs. II. Mechanical properties of muscle: implications for system design. Am J Physiol 271:C571–578
Maganaris CN (2001) Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172:279–285
Maganaris CN (2003) Force–length characteristics of the in vivo human gastrocnemius muscle. Clin Anat 16:215–223
Maier L, Root TM, Seyfarth EA (1987) Heterogeneity of spider leg muscle: histochemistry and electrophysiology of identified fibers in the claw levator. J Comp Physiol B, Biochem Syst Environ Physiol 157:285–294
Melchers M (1967) Der Beutefang von Cupiennius salei Keyserling (Ctenidae). Z Morph Ökol Tiere 58:321–346
Mendez J, Keys A (1960) Density and composition of mammalian muscle. Metabolism 9:184–188
Moya-Larano J, Vinkovic D, De Mas E, Corcobado G, Moreno E (2008) Morphological evolution of spiders predicted by pendulum mechanics. PLoS ONE 3:e1841
Parry DA, Brown RHJ (1959) The hydraulic mechanism of the spider leg. J Exp Biol 36:423–433
Prange HD (1977) The scaling and mechanics of arthropod exoskeletons. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, pp 169–181
Ranatunga KW, Thomas PE (1990) Correlation between shortening velocity, force–velocity relation and histochemical fibre-type composition in rat muscles. J Muscle Res Cell Motil 11:240–250
Rathmayer W (1965) Neuromuscular transmission in a spider and the effect of calcium. Comp Biochem Physiol 14:673
Rathmayer W (1990) Inhibition through neurons of the common inhibitory type (CI-neurons) in crab muscle. In: Krentz WD, Tautz J, Reichert H, Mulloney B, Wiese K (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel, pp 271–278
Rathmayer W (1996) Motorische Steuerung bei Invertebraten. In: Dudel J, Menzel R, Schmidt RF (eds) Neurowissenschaft. Springer, Berlin, pp 167–190
Reinhardt L (2006) Gleichförmige Lokomotion der Jagdspinne Cupiennius salei (KEYSERLING 1877): 3D-Beinsegmentkinematik. Thesis, Friedrich-Schiller-University, Jena
Rode C, Siebert T, Herzog W, Blickhan R (2009) The effects of parallel and series elastic components on the active cat soleus force–length relationship. J Mech Med Biol 9:105–122
Rome LC, Funke RP, Alexander RM, Lutz G, Aldridge H, Scott F, Freadman M (1988) Why animals have different muscle fibre types. Nature 335:824–827
Ruhland M, Rathmayer W (1978) Die Beinmuskulatur und ihre Innervation bei der Vogelspinne Dugesiella hentzi (Ch.) (Araneae, Aviculariidae). Zoomorphology 89:33–46
Scott SH, Brown IE, Loeb GE (1996) Mechanics of feline soleus: I. Effect of fascicle length and velocity on force output. J Muscle Res Cell Motil 17:207–219
Seyfarth EA, Eckweiler W, Hammer K (1985) Proprioceptors and sensory nerves in the legs of a spider, Cupiennius salei (Arachnida, Araneida). Zoomorphology 105:190–196
Sherman RG (1985) Neural control of the heartbeat and skeletal muscle in spiders and scorpions. In: Barth FG (ed) Neurobiology of arachnids. Springer, Berlin, pp 319–336
Siebert T, Sust M, Thaller S, Tilp M, Wagner H (2007) An improved method to determine neuromuscular properties using force laws—from single muscle to applications in human movements. Hum Mov Sci 26:320–341
Siebert T, Rode C, Herzog W, Till O, Blickhan R (2008) Nonlinearities make a difference: comparison of two common Hill-type models with real muscle. Biol Cybern 98:133–143
Stewart DM, Martin AW (1974) Blood pressure in the tarantula Dugesiella hentzi. J Comp Physiol 88:141–172
Till O, Siebert T, Rode C, Blickhan R (2008) Characterization of isovelocity extension of activated muscle: a Hill-type model for eccentric contractions and a method for parameter determination. J Theor Biol 255:176–187
Wagner H, Blickhan R (1999) Stabilizing function of skeletal muscles: an analytical investigation. J Theor Biol 199:163–179
Wagner H, Blickhan R (2003) Stabilizing function of antagonistic neuromusculoskeletal systems: an analytical investigation. Biol Cybern 199:163–179
Wagner H, Siebert T, Ellerby DJ, Marsh RL, Blickhan R (2005) ISOFIT: a model-based method to measure muscle–tendon properties simultaneously. Biomech Model Mechanobiol 4:10–19
Weihmann T, Blickhan R (2006) Legs operate different during steady locomotion and escape in a wandering spider. J Biomech 39(Suppl 1):361
Wells JB (1965) Comparison of mechanical properties between slow and fast mammalian muscles. J Physiol 178:252–269
Whitehead WF, Rempel JG (1959) A study of the musculature of the black widow spider, Latrodectus mactans (Fabr.). Can J Zool 37(6):831–870
Woittiez RD, Huijing PA, Boom HB, Rozendal RH (1984) A three-dimensional muscle model: a quantified relation between form and function of skeletal muscles. J Morphol 182:95–113
Woledge RC (1998) Possible effects of fatigue on muscle efficiency. Acta Physiol Scand 162:267–273
Zebe E, Rathmayer W (1968) An electron microscopical study of spider muscles. Z Zellforsch Mikrosk Anat 92:377–387
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We thank the German Science Foundation (DFG) for support of work (Bl 236/14-2).
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Communicated by G. Heldmaier.
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Siebert, T., Weihmann, T., Rode, C. et al. Cupiennius salei: biomechanical properties of the tibia–metatarsus joint and its flexing muscles. J Comp Physiol B 180, 199–209 (2010). https://doi.org/10.1007/s00360-009-0401-1
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DOI: https://doi.org/10.1007/s00360-009-0401-1