Dynamics of mallard (Anas platyrynchos) gastrocnemius function during swimming versus terrestrial locomotion

A.A. Biewener; W.R. Corning

Summary

This study investigates how the contractile function of a muscle may be modulated to accommodate changes in locomotor mode and differences in the physical environment. In vivo recordings of lateral gastrocnemius (LG) activation, force development (measured using tendon buckle transducers) and length change (measured using sonomicrometry) were obtained from mallard ducks (Anas platyrhynchos) as they swam at steady speeds in a water tank and walked or ran on land. LG force recordings were compared with combined lateral and medial gastrocnemius (MG) muscle-tendon force recordings obtained from the contralateral limb, allowing force development by the MG to be estimated relative to that of the LG. Although similar stresses were calculated to act in the LG and MG muscles during terrestrial locomotion (126 and 115 kPa, respectively), stresses were considerably greater in the LG compared with the MG during swimming (62 versus 34 kPa, respectively). During both steady swimming and terrestrial locomotion, the LG developed force while shortening over a considerable range of its length (swimming 23.6 % versus terrestrial 37.4 %). Activation of the muscle occurred near the end of passive lengthening during the recovery stroke, just prior to muscle shortening. As a result, the muscle generated broad positive work loops during both locomotor modes. LG work during swimming (4.8 J kg(−)(1)) averaged 37 % of the work performed during terrestrial locomotion (13.1 J kg(−)(1)), consistent with the twofold greater force and 58 % greater strain of the muscle during walking and running. Because limb cycle frequency was similar for the two locomotor modes (swimming 2.65 versus terrestrial 2.61 Hz), differences in power output (swimming 12.6 W kg(−)(1)versus terrestrial 32.4 W kg(−)(1)) largely reflected difference in work per cycle. Tendon elastic energy savings was a small fraction (<5 %) of the work performed by the muscle, consistent with a fiber-tendon design of these two muscles that favors muscle work to produce limb movement with little tendon strain. These results are consistent with a higher cost of terrestrial locomotion in ducks compared with other, more cursorial birds that may operate their muscles more economically and achieve greater tendon elastic savings.

REFERENCES

1. Aigledinger, T. L. and
2. Fish, F. E.
(1995). Hydroplaning by ducklings: overcoming limitations to swimming at the water surface. J. Exp. Biol 198, 1567–.
1. Bech, C. and
2. Nomoto, S.
(1982). Cardiovascular changes associated with treadmill running in the Pekin duck. J. Exp. Biol 97, 345–.
1. Biewener, A. A.
(1983). Locomotory stresses in the limb bones of two small mammals: the ground squirrel and chipmunk. J. Exp. Biol 103, 135–.
1. Biewener, A. A.
(1998). Muscle function in vivo: the design of muscles used as springs versus muscles used to generate mechanical power. Am. Zool 38, 703–.
1. Biewener, A. A. and
2. Baudinette, R. V.
(1995). In vivo muscle force and elastic energy storage during steady-speed hopping of tammar wallabies (Macropus eugenii). J. Exp. Biol 198, 1829–.
1. Biewener, A. A. and
2. Blickhan, R.
(1988). Kangaroo rat locomotion: design for elastic energy storage or acceleration?. J. Exp. Biol 140, 243–.
1. Biewener, A. A.,
2. Corning, W. R. and
3. Tobalske, B. T.
(1998). In vivo pectoralis muscle force—length behavior during level flight in pigeons (Columba livia). J. Exp. Biol 201, 3293–.
1. Biewener, A. A. and
2. Gillis, G. B.
(1999). Dynamics of muscle function during locomotion: accommodating variable conditions. J. Exp. Biol 202, 3387–.
1. Biewener, A. A.,
2. Konieczynski, D. D. and
3. Baudinette, R. V.
(1998). In vivo muscle force—length behavior during steady-speed hopping in tammar wallabies. J. Exp. Biol 201, 1681–.
1. Biewener, A. A. and
2. Roberts, T. J.
(2000). Muscle and tendon contributions to force, work and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev 28, 99–.
1. Butler, P. J.,
2. Turner, D. L.,
3. Al-Wassia, A. and
4. Bevan, R. M.
(1988). Regional distribution of blood flow during swimming in the tufted duck (Aythya fuligula). J. Exp. Biol 135, 461–.
1. Cavagna, G. A.,
2. Heglund, N. C. and
3. Taylor, C. R.
(1977). Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditures. Am. J. Physiol 233, 243–.
1. Clark, B. D. and
2. Fish, F. E.
(1994). Scaling of the locomotory apparatus and paddling rhythm in swimming mallard ducklings (Anas platyrhynchos): test of a resonance model. J. Exp. Zool 270, 245–.
1. Dial, K. P. and
2. Biewener, A. A.
(1993). Pectoralis muscle force and power output during different modes of flight in pigeons (Columba livia). J. Exp. Biol 176, 31–.
1. Fedak, M. A. and
2. Seeherman, H. J.
(1979). Reappraisal of energetics of locomotion shows identical cost in bipeds and quadrupeds including ostrich and horse. Nature 282, 713–.
1. Fish, F. E.
(1984). Mechanics, power output and efficiency of the swimming muskrat (Ondatra zibethicus). J. Exp. Biol 110, 183–.
1. Gans, C. and
2. Gaunt, A. S.
(1992). Muscle architecture and control demands. Brain Behav. Evol 40, 70–.
1. Gillis, G. B. and
2. Biewener, A. A.
(2000). Musculoskeletal mechanisms for accommodating locomotion in different environments: hindlimb extensor muscle function during hopping and swimming in the toad (Bufo marinus). J. Exp. Biol 203, 3547–.
1. Goldman, D. E. and
2. Richards, J.
(1954). Measurements of high-frequency sound velocity in mammalian soft tissue. J. Acoust. Soc. Am 26, 981–.
1. Grubb, B. R.
(1982). Cardiac output and stroke volume in exercising ducks and pigeons. J. Appl. Physiol 53, 207–.
1. Harry, J. D.,
2. Ward, A.,
3. Hegland, N. C.,
4. Morgan, D. L. and
5. McMahon, T. A.
(1990). Cross-bridge cycling theories cannot explain high-speed lengthening behavior in muscle. Biophys. J 57, 201–.
1. Heglund, N. C.,
2. Cavagna, G. A. and
3. Taylor, C. R.
(1982). Energetics and mechanics of terrestrial locomotion. III. Energy changes of the centre of mass as a function of speed and body size in birds and mammals. J. Exp. Biol 79, 41–.
1. Heglund, N. C.,
2. Fedak, M. A.,
3. Taylor, C. R. and
4. Cavagna, G. A.
(1982). Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. J. Exp. Biol 97, 57–.
1. Herzog, W. and
2. Leonard, T. R.
(1991). Validation of optimization models that estimate the forces exerted by synergistic muscles. J. Biomech 24, 31–.
1. Herzog, W.,
2. Leonard, T. R. and
3. Guimaraes, A. C. S.
(1993). Forces in gastrocnemius, soleus and plantaris muscles for the freely moving cat. J. Biomech 26, 945–.
1. Hill, A. V.
(1938). The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126, 136–.
1. Josephson, R. K. and
2. Stokes, D. R.
(1999). Work-dependent deactivation of crustacean muscle. J. Exp. Biol 202, 2551–.
1. Ker, R. F.
(1981). Dynamic tensile properties of the plantaris tendon of sheep (Ovis aries). J. Exp. Biol 93, 283–.
1. Kram, R. and
2. Taylor, C. R.
(1990). Energetics of running: a new perspective. Nature 346, 265–.
1. Lutz, G. J. and
2. Rome, L. C.
(1994). Built for jumping: the design of the frog muscular system. Science 263, 370–.
1. Morgan, D. L.
(1990). New insights into the behavior of muscle during active lengthening. Biophys. J 57, 209–.
1. Olson, J. M. and
2. Marsh, R. L.
(1998). Activation patterns and length changes in hindlimb muscles of the bullfrog Rana catesbeiana during jumping. J. Exp. Biol 201, 2763–.
1. Prange, H. D. and
2. Schmidt-Nielsen, K.
(1970). The metabolic cost of swimming in ducks. J. Exp. Biol 53, 763–.
1. Prilutsky, B. I.,
2. Herzon, W.,
3. Leonard, T. R. and
4. Allinger, T. L.
(1996). The role of the muscle belly and tendon of soleus, gastrocnemius, and plantaris in mechanical energy absorption and generation during cat locomotion. J. Biomech 29, 417–.
1. Purslow, P. P. N.
(1989). Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J. Biomech 22, 21–.
1. Roberts, T. J.,
2. Marsh, R. L.,
3. Weyand, P. G. and
4. Taylor, C. R.
(1997). Muscular force in running turkeys: the economy of minimizing work. Science 275, 1113–.
1. Shadwick, R. E.
(1990). Elastic energy storage in tendons: mechanical differences related to function and age. J. Appl. Physiol 68, 1033–.
1. Taylor, C. R.
(1994). Relating mechanics and energetics during exercise. Adv. Vet. Sci. Comp. Med 38, 181–.
1. Tobalske, B. W. and
2. Dial, K. P.
(2000). Effects of body size on takeoff flight performance in the Phasianidae (Aves). J. Exp. Biol 203, 3319–.
1. Trotter, J. A. and
2. Purslow, P. P.
(1992). Functional morphology of the endomysium in series fibered muscles. J. Morph 212, 109–.
1. Trotter, J. A.,
2. Salgado, J. D.,
3. Ozbaysal, R. and
4. Gaunt, A. S.
(1992). The composite structure of quail pectoralis muscle. J. Morph 212, 27–.
1. Walmsley, B.,
2. Hodgson, J. A. and
3. Burke, R. E.
(1978). Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J. Neurophysiol 41, 1203–.
1. Williams, T. M.
(1983). Locomotion in the North American mink, a semi-aquatic mammal. I. Swimming energetics and body drag. J. Exp. Biol 103, 155–.
1. Williamson, M. R.,
2. Dial, K. P. and
3. Biewener, A. A.
(2001). Pectoralis muscle performance during ascending and slow level flight in mallards (Anas platyrhynchos). J. Exp. Biol 204, 495–.

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[1] Aigledinger, T. L. and
Fish, F. E.
(1995). Hydroplaning by ducklings: overcoming limitations to swimming at the water surface. J. Exp. Biol 198, 1567–.

[2] Aigledinger, T. L. and

[3] Fish, F. E.

[4] Bech, C. and
Nomoto, S.
(1982). Cardiovascular changes associated with treadmill running in the Pekin duck. J. Exp. Biol 97, 345–.

[5] Bech, C. and

[6] Nomoto, S.

[7] Biewener, A. A.
(1983). Locomotory stresses in the limb bones of two small mammals: the ground squirrel and chipmunk. J. Exp. Biol 103, 135–.

[8] Biewener, A. A.

[9] Biewener, A. A.
(1998). Muscle function in vivo: the design of muscles used as springs versus muscles used to generate mechanical power. Am. Zool 38, 703–.

[10] Biewener, A. A.

[11] Biewener, A. A. and
Baudinette, R. V.
(1995). In vivo muscle force and elastic energy storage during steady-speed hopping of tammar wallabies (Macropus eugenii). J. Exp. Biol 198, 1829–.

[12] Biewener, A. A. and

[13] Baudinette, R. V.

[14] Biewener, A. A. and
Blickhan, R.
(1988). Kangaroo rat locomotion: design for elastic energy storage or acceleration?. J. Exp. Biol 140, 243–.

[15] Biewener, A. A. and

[16] Blickhan, R.

[17] Biewener, A. A.,
Corning, W. R. and
Tobalske, B. T.
(1998). In vivo pectoralis muscle force—length behavior during level flight in pigeons (Columba livia). J. Exp. Biol 201, 3293–.

[18] Biewener, A. A.,

[19] Corning, W. R. and

[20] Tobalske, B. T.

[21] Biewener, A. A. and
Gillis, G. B.
(1999). Dynamics of muscle function during locomotion: accommodating variable conditions. J. Exp. Biol 202, 3387–.

[22] Biewener, A. A. and

[23] Gillis, G. B.

[24] Biewener, A. A.,
Konieczynski, D. D. and
Baudinette, R. V.
(1998). In vivo muscle force—length behavior during steady-speed hopping in tammar wallabies. J. Exp. Biol 201, 1681–.

[25] Biewener, A. A.,

[26] Konieczynski, D. D. and

[27] Baudinette, R. V.

[28] Biewener, A. A. and
Roberts, T. J.
(2000). Muscle and tendon contributions to force, work and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev 28, 99–.

[29] Biewener, A. A. and

[30] Roberts, T. J.

[31] Butler, P. J.,
Turner, D. L.,
Al-Wassia, A. and
Bevan, R. M.
(1988). Regional distribution of blood flow during swimming in the tufted duck (Aythya fuligula). J. Exp. Biol 135, 461–.

[32] Butler, P. J.,

[33] Turner, D. L.,

[34] Al-Wassia, A. and

[35] Bevan, R. M.

[36] Cavagna, G. A.,
Heglund, N. C. and
Taylor, C. R.
(1977). Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditures. Am. J. Physiol 233, 243–.

[37] Cavagna, G. A.,

[38] Heglund, N. C. and

[39] Taylor, C. R.

[40] Clark, B. D. and
Fish, F. E.
(1994). Scaling of the locomotory apparatus and paddling rhythm in swimming mallard ducklings (Anas platyrhynchos): test of a resonance model. J. Exp. Zool 270, 245–.

[41] Clark, B. D. and

[42] Fish, F. E.

[43] Dial, K. P. and
Biewener, A. A.
(1993). Pectoralis muscle force and power output during different modes of flight in pigeons (Columba livia). J. Exp. Biol 176, 31–.

[44] Dial, K. P. and

[45] Biewener, A. A.

[46] Fedak, M. A. and
Seeherman, H. J.
(1979). Reappraisal of energetics of locomotion shows identical cost in bipeds and quadrupeds including ostrich and horse. Nature 282, 713–.

[47] Fedak, M. A. and

[48] Seeherman, H. J.

[49] Fish, F. E.
(1984). Mechanics, power output and efficiency of the swimming muskrat (Ondatra zibethicus). J. Exp. Biol 110, 183–.

[50] Fish, F. E.

[51] Gans, C. and
Gaunt, A. S.
(1992). Muscle architecture and control demands. Brain Behav. Evol 40, 70–.

[52] Gans, C. and

[53] Gaunt, A. S.

[54] Gillis, G. B. and
Biewener, A. A.
(2000). Musculoskeletal mechanisms for accommodating locomotion in different environments: hindlimb extensor muscle function during hopping and swimming in the toad (Bufo marinus). J. Exp. Biol 203, 3547–.

[55] Gillis, G. B. and

[56] Biewener, A. A.

[57] Goldman, D. E. and
Richards, J.
(1954). Measurements of high-frequency sound velocity in mammalian soft tissue. J. Acoust. Soc. Am 26, 981–.

[58] Goldman, D. E. and

[59] Richards, J.

[60] Grubb, B. R.
(1982). Cardiac output and stroke volume in exercising ducks and pigeons. J. Appl. Physiol 53, 207–.

[61] Grubb, B. R.

[62] Harry, J. D.,
Ward, A.,
Hegland, N. C.,
Morgan, D. L. and
McMahon, T. A.
(1990). Cross-bridge cycling theories cannot explain high-speed lengthening behavior in muscle. Biophys. J 57, 201–.

[63] Harry, J. D.,

[64] Ward, A.,

[65] Hegland, N. C.,

[66] Morgan, D. L. and

[67] McMahon, T. A.

[68] Heglund, N. C.,
Cavagna, G. A. and
Taylor, C. R.
(1982). Energetics and mechanics of terrestrial locomotion. III. Energy changes of the centre of mass as a function of speed and body size in birds and mammals. J. Exp. Biol 79, 41–.

[69] Heglund, N. C.,

[70] Cavagna, G. A. and

[71] Taylor, C. R.

[72] Heglund, N. C.,
Fedak, M. A.,
Taylor, C. R. and
Cavagna, G. A.
(1982). Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. J. Exp. Biol 97, 57–.

[73] Heglund, N. C.,

[74] Fedak, M. A.,

[75] Taylor, C. R. and

[76] Cavagna, G. A.

[77] Herzog, W. and
Leonard, T. R.
(1991). Validation of optimization models that estimate the forces exerted by synergistic muscles. J. Biomech 24, 31–.

[78] Herzog, W. and

[79] Leonard, T. R.

[80] Herzog, W.,
Leonard, T. R. and
Guimaraes, A. C. S.
(1993). Forces in gastrocnemius, soleus and plantaris muscles for the freely moving cat. J. Biomech 26, 945–.

[81] Herzog, W.,

[82] Leonard, T. R. and

[83] Guimaraes, A. C. S.

[84] Hill, A. V.
(1938). The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126, 136–.

[85] Hill, A. V.

[86] Josephson, R. K. and
Stokes, D. R.
(1999). Work-dependent deactivation of crustacean muscle. J. Exp. Biol 202, 2551–.

[87] Josephson, R. K. and

[88] Stokes, D. R.

[89] Ker, R. F.
(1981). Dynamic tensile properties of the plantaris tendon of sheep (Ovis aries). J. Exp. Biol 93, 283–.

[90] Ker, R. F.

[91] Kram, R. and
Taylor, C. R.
(1990). Energetics of running: a new perspective. Nature 346, 265–.

[92] Kram, R. and

[93] Taylor, C. R.

[94] Lutz, G. J. and
Rome, L. C.
(1994). Built for jumping: the design of the frog muscular system. Science 263, 370–.

[95] Lutz, G. J. and

[96] Rome, L. C.

[97] Morgan, D. L.
(1990). New insights into the behavior of muscle during active lengthening. Biophys. J 57, 209–.

[98] Morgan, D. L.

[99] Olson, J. M. and
Marsh, R. L.
(1998). Activation patterns and length changes in hindlimb muscles of the bullfrog Rana catesbeiana during jumping. J. Exp. Biol 201, 2763–.

[100] Olson, J. M. and

[101] Marsh, R. L.

[102] Prange, H. D. and
Schmidt-Nielsen, K.
(1970). The metabolic cost of swimming in ducks. J. Exp. Biol 53, 763–.

[103] Prange, H. D. and

[104] Schmidt-Nielsen, K.

[105] Prilutsky, B. I.,
Herzon, W.,
Leonard, T. R. and
Allinger, T. L.
(1996). The role of the muscle belly and tendon of soleus, gastrocnemius, and plantaris in mechanical energy absorption and generation during cat locomotion. J. Biomech 29, 417–.

[106] Prilutsky, B. I.,

[107] Herzon, W.,

[108] Leonard, T. R. and

[109] Allinger, T. L.

[110] Purslow, P. P. N.
(1989). Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J. Biomech 22, 21–.

[111] Purslow, P. P. N.

[112] Roberts, T. J.,
Marsh, R. L.,
Weyand, P. G. and
Taylor, C. R.
(1997). Muscular force in running turkeys: the economy of minimizing work. Science 275, 1113–.

[113] Roberts, T. J.,

[114] Marsh, R. L.,

[115] Weyand, P. G. and

[116] Taylor, C. R.

[117] Shadwick, R. E.
(1990). Elastic energy storage in tendons: mechanical differences related to function and age. J. Appl. Physiol 68, 1033–.

[118] Shadwick, R. E.

[119] Taylor, C. R.
(1994). Relating mechanics and energetics during exercise. Adv. Vet. Sci. Comp. Med 38, 181–.

[120] Taylor, C. R.

[121] Tobalske, B. W. and
Dial, K. P.
(2000). Effects of body size on takeoff flight performance in the Phasianidae (Aves). J. Exp. Biol 203, 3319–.

[122] Tobalske, B. W. and

[123] Dial, K. P.

[124] Trotter, J. A. and
Purslow, P. P.
(1992). Functional morphology of the endomysium in series fibered muscles. J. Morph 212, 109–.

[125] Trotter, J. A. and

[126] Purslow, P. P.

[127] Trotter, J. A.,
Salgado, J. D.,
Ozbaysal, R. and
Gaunt, A. S.
(1992). The composite structure of quail pectoralis muscle. J. Morph 212, 27–.

[128] Trotter, J. A.,

[129] Salgado, J. D.,

[130] Ozbaysal, R. and

[131] Gaunt, A. S.

[132] Walmsley, B.,
Hodgson, J. A. and
Burke, R. E.
(1978). Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J. Neurophysiol 41, 1203–.

[133] Walmsley, B.,

[134] Hodgson, J. A. and

[135] Burke, R. E.

[136] Williams, T. M.
(1983). Locomotion in the North American mink, a semi-aquatic mammal. I. Swimming energetics and body drag. J. Exp. Biol 103, 155–.

[137] Williams, T. M.

[138] Williamson, M. R.,
Dial, K. P. and
Biewener, A. A.
(2001). Pectoralis muscle performance during ascending and slow level flight in mallards (Anas platyrhynchos). J. Exp. Biol 204, 495–.

[139] Williamson, M. R.,

[140] Dial, K. P. and

[141] Biewener, A. A.

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Developmental and reproductive physiology of small mammals at high altitude

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Summary

REFERENCES

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Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Meet the Editors at SICB Virtual 2021

2020 at The Company of Biologists

The Big Biology podcast

Developmental and reproductive physiology of small mammals at high altitude

Read & Publish participation extends worldwide