6 - Fiber architecture, muscle function, and behavior: gluteal and hamstring muscles of semiterrestrial and arboreal guenons  pp. 99-133

Fiber architecture, muscle function, and behavior: gluteal and hamstring muscles of semiterrestrial and arboreal guenons

By Fred Anapol, Nazima Shahnoor and J. Patrick Gray

Image View Previous Chapter Next Chapter


Charles Oxnard championed the use of statistical techniques to reduce a multitude of variables into a comprehendible pattern in order to demonstrate some aspect of primate behavior or evolution. In reality, Professor Oxnard's interests and writings have spanned an enormity and diversity of topics. By analogy, one might conclude that the “first principal component” of his work is reflected by the succinct statement on page 6 of his 1975 book, Uniqueness and Diversity in Human Evolution: “There is no doubt that the locomotor behavior of an animal is, on a gross level, controlled by the anatomy of the animal.” This point of departure for the research of many contributors to this volume, has influenced our own endeavor to understand how the internal morphology of a muscle itself, i.e., fiber architecture and histochemical fiber type composition, is associated with organ function and animal behavior. In this chapter, we consider the relationship of locomotor behavior, muscle function, and the fiber architecture of the gluteal and hamstring muscle groups.

Many classes of polymorphic variables determine the internal morphology of whole skeletal muscles. These include the relative composition of histo/immunocytochemical fiber types (see Chapter 7), neurological compartmentalization related to fascial partitioning (English, 1984) by the branching pattern of motoneurons (e.g., Herring et al., 1989, 1991), and the spatial arrangement of muscle fibers and tendons, otherwise known as fiber architecture (Gans and Bock, 1965; Gans, 1982; Richmond, 1998).

Alexander, R. McN. (1974). The mechanics of jumping by a dog (Canis familiaris). J. Zool. Lond., 173, 549–573
Alexander, R. McN. and Bennet-Clark, H. C. (1977). Storage of elastic strain energy in muscle and other tissue. Nature, 265, 114–117
Anapol F. (1987). Telemetered electromyography of the fast and slow extensors of the leg of the brown lemur (Lemur fulvus). J. Exp. Biol., 130, 341–358
Anapol, F. (1984). Morphological and functional diversity within the quadriceps femoris in Lemur fulvus: architectural, histochemical, and electromyographic considerations.Ph. D. thesis, State University of New York at Stony Brook
Anapol, F. (1988). Morphological and videofluorographic study of the hyoid apparatus and its function in the rabbit (Oryctolagus cuniculus). J. Morphol., 195, 141–157
Anapol, F. (2003). Fiber architecture in primate limb muscles with new data for triceps surae in Eulemur fulvus. Amer. J. Phys. Anthropol. (Suppl. 36), 59
Anapol, F. and Barry, K. (1996). Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. Amer. J. Phys. Anthropol., 99, 429–447
Anapol, F. and Bischoff, L. K. (1992). Comparative skeletal adaptations of Cercopithecus ascanius and C. aethiops to locomotor behavior. Amer. J. Phys. Anthropol. (Suppl. 14), 43
Anapol, F. and Gray, J. P. (2003). Fiber architecture of the intrinsic muscles of the shoulder and arm in semiterrestrial and arboreal guenons. Amer. J. Phys. Anthropol., 122, 51–65
Anapol, F. and Herring, S. W. (1989). Length–tension relationships of masseter and digastric muscles of miniature swine during ontogeny. J. Exp. Biol., 143, 1–16
Anapol, F. and Jungers, W. L. (1986). Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus). Amer. J. Phys. Anthropol., 69, 355–375
Anapol, F., Muhl, Z. F., and Fuller, J. H. (1987). The force–velocity relation of the rabbit digastric muscle. Arch. Oral Biol., 32, 93–99
Appleton, A. B. (1921). The gluteal region of Tarsius spectrum. Proc. Camb. Philos. Soc., 20, 466–474
Armstrong, R. B. (1980). Properties and distributions of the fiber types in the locomotory muscles of mammals. In: Comparative Physiology: Primitive Mammals, ed. K. Schmidt-Nielsen, L. Bolis, and C. R. Taylor. Cambridge: Cambridge University Press. pp. 243–254
Armstrong, R. B. and Phelps, R. O. (1984). Muscle fiber type composition of the rat hindlimb. Amer. J. Anat., 171, 259–272
Armstrong, R. B., Sauber, C. W., Seeherman, H. J., and Taylor, C. R. (1982). Distribution of fiber types in locomotory muscles of dogs. Amer. J. Anat., 163, 87–98
Ashton, E. H. and Oxnard, C. E. (1963). The musculature of the primate shoulder. Trans. Zool. Soc. Lond., 29, 553–650
Benninghoff, A. and Rollhäuser, H. (1952). Zur inneren Mechanik des gefiederten Muskels. Pflugers Arch. Ges. Physiol., 254, 527–548
Biewener, A. (1998). Muscle function in vivo: a comparison of muscles used for elastic energy savings versus muscles used to generate mechanical power. Amer. Zool., 38, 703–717
Biewener, A. and Baudinette, R. V. (1998). In vivo muscle force-length behavior during steady-speed hopping of tammar wallabies. J. Exp. Biol., 201, 1681–1694
Biewener, A., Alexander, R. McN., and Heglund, N. C. (1981). Elastic energy storage in the hopping of kangaroo rats (Dipodomys spectabilis). J. Zool. Lond., 195, 369–383
Buchner, H. (1877). Kritische und experimentelle Studien über den Zusammenhalt des Hüftgelenks während des Lebens in allen normalen Fallen. Arch. Anat. Physiol., 1877, 22–45
Burke, R. E. and Edgerton, V. R. (1975). Motor unit properties and selective involvement in movement. Exerc. Spt. Sci. Rev., 3, 31–81
Cavagna, G. A. (1969). Travail mécanique dans la marche et la course. J. Physiol., Paris, 61, 3–42
Cavagna, G. A. and Kaneko, M. (1977). Mechanical work and efficiency in level walking and running. J. Physiol., 268, 467–481
Cavagna, G. A., Citterio, G., and Jacini P. (1980). Elastic storage: role of tendons and muscles. In: Comparative Physiology: Primitive Mammals, ed. K. Schmidt-Nielsen, L. Bolis, and C. R. Taylor. Cambridge: Cambridge University Press. pp. 231–242
Disotell, T. R. (2000). Molecular systematics of the Cercopithecidae In: Old World Monkeys, ed. P. F. Whitehead and C. J. Jolly. Cambridge: Cambridge University Press. pp. 29–56
Edgington, E. (1995). Randomization Tests. 3rd edn. New York, NY: Marcel Dekker
English, A. W. (1984). An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion. Exp. Neurol., 87, 96–108
Fawcett, D. W. (1986). Bloom and Fawcett, a Textbook of Histology. 11th edn. Philadelphia, PA: Saunders
Fick, A. (1860). Über die Längenverhältnisse der Skelettmuskelfasern. Aus der Inaug.-Diss. des Herrn Dr. GUBLER, mitgeteilt von A. FICK. Moleschtt Us, 8, 253–263 (1860) und GS, 1, 445–455 (1903)
Fick, R. (1910). Anatomie und Mechanik der Gelenke unter Berücksichtigung der bewegenden Muskeln. In: Handbuch der Anatomie des Menschen, ed. K. V. Bardeleben. Jena: Gustav Fischer. Vol. 2, sect. 1, part 2, pp. 1–363
Fleagle J. G. (1999). Primate Adaptation and Evolution. 2nd edn. San Diego, CA: Academic Press
Fleagle, J. G. (1977). Locomotor behavior and muscular anatomy of sympatric Malaysian leaf monkeys (Presbytis obscura and Presbytis melalophos). Amer. J. Phys. Anthropol., 46, 297–308
Fleagle, J. G. and Anapol, F. (1992). The indriid ischium and the hominid hip. J. Hum. Evol., 22, 285–305
Fleagle, J. G., Stern, J. T., Jr., Jungers, W. L., and Susman, R. L. (1981). Climbing: a biomechanical link with brachiation and with bipedalism. In: Vertebrate Locomotion, ed. M. Day. Symp. Zool. Soc. Lond. 48. London: Academic Press. pp. 359–375
Gans, C. (1982). Fiber architecture and muscle function. Exerc. Spt. Sci. Rev., 10, 160–207
Gans, C. and Bock, W. F. (1965). The functional significance of muscle architecture – a theoretical analysis. Ergeb. Anat. Entwicklungsgesch., 38, 115–142
Gans, C. and de Vree, F. (1989). Functional bases of fiber length and angulation in muscle. J. Morphol., 192, 63–85
Gaunt, A. S. and Gans, C. (1992). Serially arranged myofibers: an unappreciated variant in muscle architecture. Experientia, 48, 864–868
Gebo, D. L. and Chapman, C. A. (1995). Positional behavior in five sympatric Old World monkeys. Amer. J. Phys. Anthropol., 97, 49–76
Gillespie, C. A., Simpson, D. R., and Edgerton, V. R. (1974). Motor unit recruitment as reflected by muscle fiber glycogen loss in a prosimian (bushbaby) after running and jumping. J. Neurol. Neurosurg. Psych., 37, 817–824
Gonyea, W. J. and Ericson, G. C. (1977). Morphological and histochemical organization of the flexor carpi radialis muscle in the cat. Amer. J. Anat., 148, 329–344
Good, P. I. (1999). Resampling Methods: a Practical Guide to Data Analysis. Boston, MA: Birkhäuser
Gordon, A. M., Huxley, A. F., and Julian, F. J. (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol., 184, 170–192
Goslow, G. E., Jr., Cameron, W. E., and Stuart, D. G. (1977). Ankle flexor muscles in the cat: length-active tension and muscle unit properties as related to locomotion. J. Morphol., 15, 23–38
Grand T. I. (1968a). The functional anatomy of the lower limb of the Howler monkey (Alouatta caraya). Amer. J. Phys. Anthropol., 28, 163–183
Grand T. I. (1968b). Functional anatomy of the upper limb. In: Biology of the Howler Monkey (Alouatta caraya), ed. M. R. Malinow. Bibl. Primatol., 7. Basel: Karger. pp. 104–125
Grand T. I. (1977). Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecific comparisons. Amer. J. Phys. Anthropol., 47, 211–239
Grand, T. I. (1967). The functional anatomy of the ankle and foot of the slow loris (Nycticebus coucang). Amer. J. Phys. Anthropol., 26, 207–218
Grand, T. I. and Lorenz, R. (1968). Functional analysis of the hip joint in Tarsius bancanus (Horsfield, 1821) and Tarsius syrichta (Linnaeus, 1758). Folia Primatol., 9, 161–181
Gray, J. E. (1870). Catalogue of Monkeys, Lemurs and Fruit-eating Bats in the Collection of the British Museum. London: Trustees of the British Museum
Gregory, W. K. (1912). Notes on the principles of quadrupedal locomotion and on the mechanism of the limbs in hoofed animals. Ann. N. Y. Acad. Sci., 22, 267–294
Groves, C. P. (1989). A Theory of Human and Primate Evolution. Oxford: Oxford University Press
Groves, C. P. (2000). The phylogeny of the Cercopithecoidea. In: Old World Monkeys, ed. P. F. Whitehead and C. J. Jolly. Cambridge: Cambridge University Press. pp. 77–98
Haines, R. W. (1932). The laws of muscle and tendon growth. J. Anat., 66, 578–585
Haxton, H. A. (1944). Absolute muscle force in the ankle flexors of man. J. Physiol. Lond., 103, 267–273
Herring, S. W., Anapol, F. C., and Wineski, L. E. (1991). Motor unit territories in the masseter muscle of infant pigs. Archiv. Oral Biol., 36, 867–873
Herring, S. W., Wineski, L. E., and Anapol, F. C. (1989). Neural organization of the masseter muscle in the pig. J. Comp. Neurol., 280, 563–576
Hildebrand, M. (1959). Motions of the running cheetah and horse. J. Mammal., 40, 481–495
Hildebrand, M. (1974). Analysis of Vertebrate Structure. New York, NY: Wiley
Hill, A. V. (1938). The heat of shortening and the dynamic constants of muscle. Proc. Roy. Soc. B, 126, 136–194
Howell, A. B. and Straus, W. L., Jr. (1933). The muscular system. In: The Anatomy of the Rhesus Monkey, ed. C. G. Hartman and W. L. Straus. New York, NY: Hafner. pp. 89–175
Hoyle, G. and Smyth, T., Jr. (1963). Giant muscle fibers in a barnacle, Balanus nubilus (Darwin). Sci., 139, 49–50
Huxley, A. F. (1957). Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem., 7, 255–318
Jenkins, F. A. and Weijs, W. A. (1979). The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J. Zool. Lond., 188, 379–410
Jungers, W. L., Jouffroy, F. K., and Stern, J. T., Jr. (1980). Gross structure and function of the quadriceps femoris in Lemur fulvus: an analysis based on telemetered electromyography. J. Morphol., 164, 287–299
Jungers, W. L., Stern, J. T., Jr., and Jouffroy, F. K. (1983). Functional morphology of the quadriceps femoris in primates: a comparative anatomical and experimental analysis. Ann. Sci. Nat., Zool., Paris, 13 Serie, 5, 101–116
Kimura, K., Takahashi, Y., Konishi, M., and Iwamoto, S. (1983). Extensor muscles of the thigh of crab-eating monkeys (Macaca fascicularis). Primates, 24, 86–93
Larson S. G. (1987). EMG of chimpanzee shoulder muscles during knuckle-walking: problems of terrestrial locomotion in a suspensory adapted primate. J. Zool. Lond., 212, 629–655
Larson, S. G. and Stern, J. T., Jr. (1986). EMG of scapulohumeral muscles in the chimpanzee during reaching and “arboreal” locomotion. Amer. J. Anat., 176, 171–190
Lewontin, R. C. (1966). On the measurement of relative variability. Syst. Zool., 15, 141–142
Lieber, R. L. and Blevins, F. T. (1989). Skeletal muscle architecture of the rabbit hindlimb: functional implications of muscle design. J. Morphol., 199, 93–101
Manly, B. F. J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology. 2nd edn. New York, NY: Chapman Hall
McClearn, D. (1985). Anatomy of racoon (Procyon lotor) and coati (Nasua narica and N. nasua) forearm and leg muscles: relations between fiber length, moment-arm length, and joint-angle excursion. J. Morphol., 183, 87–115
Muhl, Z. F. (1982). Active length–tension relation and the effect of muscle pinnation on fiber lengthening. J. Morphol. 173, 285–292
Murphy, R. A. and Beardsley, A. C. (1974). Mechanical properties of the cat soleus muscle in situ. Amer. J. Physiol., 227, 1008–1013
Oxnard, C. E. (1975). Uniqueness and Diversity in Human Evolution: Morphometric studies of Australopithecines. Chicago, IL: University of Chicago Press
Paul, R. J. (1983). Physical and biochemical energy balance during an isometric tetanus and steady state recovery in frog sartorius at 0 °C. J. Gen. Physiol., 81, 337–354
Peters, S. E. and Rick, C. (1977). The actions of three hamstring muscles of the cat: a mechanical analysis. J. Morphol., 152, 315–328
Pfuhl, W. (1937). Die gefiederten Muskeln, ihre Form und ihre Wirkungsewise. Z. Anat. Enwickl.-Gesch., 196, 749–769
Prophet, E. B., Mills, B., Arrington, J. B., and Sobin, L. H. (1992). Laboratory Methods in Histotechnology. Washington, DC: Armed Forces Institute of Pathology
Quest, W. J. (1987). Estimation of Intrinsic Strength of Rabbit Digastric Muscles from Physiological Cross-Sectional Area. M.S. thesis, University of Illinois at Chicago
Ramsey, R. W. and Street, S. F. (1940). The isometric length tension diagram of isolated skeletal muscle fibers of the frog. J. Cell. Comp. Physiol., 15, 11–34
Rasmussen, S., Chan, A. K., and Goslow, G. E., Jr. (1978). The cat step cycle: electromyographic patterns for hind limb muscles during posture and unrestrained locomotion. J. Morphol., 155, 253–270
Reiser, P. J., Moss, R. L., Giulian, G. G., and Greaser, M. L. (1985). Shortening velocity in single fibers from adult rabbit soleus muscle is correlated with myosin heavy chain composition. J. Biol. Chem., 260, 9077–9080
Richmond, F. J. R. (1998). Elements of style in neuromuscular architecture. Amer. Zool., 38, 729–742
Sacks, R. D. and Roy, R. R. (1982). Architecture of the hind limb muscles of cats: Functional significance. J. Morphol., 173, 185–195
Scapino, R. P. (1968). Biomechanics of Feeding in Carnivora. Ph. D. thesis, University of Illinois at Chicago
Schmitt, D. (1998). Forelimb mechanics during arboreal and terrestrial quadrupedalism in Old World monkeys. In: Primate Locomotion: Recent Advances, ed. E. Strasser, J. G. Fleagle, H. McHenry, and A. Rosenberger. New York, NY: Plenum Press. pp. 175–200
Schmitt, D. (2003). Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates. J. Hum. Evol., 44, 47–58
Schumacher, G. H. (1961). Funktionelle Morphologie der Kaumuskulatur. Jena: Gustav Fischer. (Trans. by Z. Muhl)
Shapiro, S. S. and Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52, 591–611
Smith, J. L., Betts, B., Edgerton, V. R., and Zernicke R. F. (1980). Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J. Neurophysiol., 43, 612–620
Smith, J. L., Edgerton, V. R., Betts, B., and Collatos, T. C. (1977). EMG of slow and fast ankle extensors of cat during posture, locomotion, and jumping. J. Neurophysiol., 40, 503–513
Smith, J. M. and Savage, R. J. G. (1955). Some locomotory adaptations in mammals. J. Linn. Soc. Lond. Zool., 42, 603–622
Sokal, R. R. and Rohlf, F. J. (1981). Biometry. 2nd edn. San Francisco, CA: W. H. Freeman
Spector, S. A., Gardiner, P. F., Zernicke, R. F., Roy, R. R., and Edgerton, V. R. (1980). Muscle architecture and force–velocity characteristics of cat soleus and medial gastrocnemius: implications for motor control. J. Neurophysiol., 44, 951–960
Stern, J. T. Jr., Wells, J. P., Vangor, A. K., and Fleagle, J. G. (1977). Electromyography of some muscles of the upper limb in Ateles and Lagothrix. Yrbk. Phys. Anthropol., 20, 98–507
Stern, J. T., Jr. (1971). Functional Myology of the Hip and Thigh of Cebid Monkeys and its Implications for the Evolution of Erect Posture. Bibl. Primatol, 14. Basel: Karger
Stern, J. T., Jr. (1974). Computer modeling of gross muscle dynamics. J. Biomech., 7, 4111–28
Swartz, S. M. and Tuttle, R. H. (1990). Allometric patterns in the limb musculature of catarrhine primates. Amer. J. Phys. Anthropol., 81, 304
Tappen, N. C. (1991). Present and future status of the Tappen collection of primate specimens at the University of Wisconsin–Milwaukee. In: Primatology Today, ed. A. Ehara and T. Kimura. Amsterdam: Elsevier. pp. 555–558
Tokuriki, M. (1973). Electromyographic and joint-mechanical studies in quadrupedal locomotion. I. Walking. Jpn. J. Vet. Sci., 35, 433–446
Tuttle R. H. (1978b). Electromyography of pongid shoulder muscles. III. Quadrupedal positional behavior. Amer. J. Phys. Anthropol., 49, 57–70
Tuttle, R. H. and Basmajian, J. V. (1978a). Electromyography of pongid shoulder muscles. II. Deltoid, rhomboid and “rotator cuff.” Amer. J. Phys. Anthropol., 49, 47–56
Vangor, A. K. (1979). Electromyography of Gait in Non-Human Primates and its Significance for the Evolution of Bipedality. Ph. D. thesis, State University of New York at Stony Brook
Walmsley, B. and Proske, U. (1981). Comparison of stiffness of soleus and medial gastrocnemius muscles in cats. J. Neurophysiol., 46, 250–259
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, 1203–1216
Weber, E. F. (1851). Uber die Langenverhaltnisse der Fleischfasern der Muskeln im allgemeinen. Ber. K. sachs. Ges. Wiss. nat. phys., K1, 64–86
Wilkie, D. R. (1968). Heat work and phosphoryl creatine breakdown in muscle. J. Physiol., 195, 157–183
Willemse J. J. (1977). Morphological and functional aspects of the arrangement of connective tissue and muscle fibres in the tail of the Mexican axolotl, Siredon mexicanum (Shaw) (Amphibia, Urodela). Acta Anat., 97, 266–285
Willemse, J. J. (1963). Some characteristics of muscle fibers in a pinnate muscle. Proc. Kon. Ned. Akad. Wet. Ser. C, 66, 162–171
Wineski, L. and Gans, C. (1984). Morphological basis of the feeding mechanics in the shingleback lizard Trachydosaurus rugosus (Scincidae: Reptilia). J. Morphol., 181, 271–295
Woods, C. A. and Hermanson, J. W. (1985). Myology of hystricognath rodents: an analysis of form, function and phylogeny. In: Evolutionary Relationships Among Rodents: a Multidisciplinary Analysis, ed. W. P. Luckett and J. L. Hartenberger. New York, NY: Plenum Press. pp. 515–548
Zar, J. H. (1984). Biostatistical Analysis. 2nd edn. Englewood Cliffs, NJ: Prentice-Hall