The musculotendinous system of an anguilliform swimmer: Muscles, myosepta, dermis, and their interconnections in Anguilla rostrata

Journal of Morphology

Volumn 269, Issue 1, 2008, Pages 29-44

  Danos, Nicole ^a   Fisch, Nina ^b   Gemballa, Sven ^b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Anguilla rostrata; Connective tissue; Myoseptal tendons; Red muscle; Skin

Indexed keywords

ANIMAL; ARTICLE; AUDIOVISUAL EQUIPMENT; BIOMECHANICS; CONNECTIVE TISSUE; DERMIS; EEL; HISTOLOGY; MUSCLE CELL; MUSCLE CONTRACTION; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; SKELETAL MUSCLE; SWIMMING; TENDON; ULTRASTRUCTURE;

ANGUILLA; ANIMALS; BIOMECHANICS; CONNECTIVE TISSUE; DERMIS; MICROSCOPY, ELECTRON, SCANNING; MODELS, ANATOMIC; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE, SKELETAL; SWIMMING; TENDONS;

ANGUILLA ROSTRATA; ANGUILLIFORMES; PISCES; SALMONIDAE;

EID: 37649002341     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10570     Document Type: Article

References (75)

1. Alexander RMcN. 1969. The orientation of muscle fibers in the myomeres of fishes. J Mar Biol Assoc UK 49:263-290.
2. Alexander RM. 1987. Bending of cylindrical animals with helical fibres in their skin or cuticle. J Theor Biol 124:97-110.
3. Brainerd EL, Patek SN. 1998. Vertebral column morphology. C-start curvature, and the evolution of mechanical defenses in tetraodontiform fishes. Copeia 1998:971-984.
4. Chapman GB, Dawson AB. 1961. Fine structure of larval anuran epidermis, with special reference to figures of Eberth. J Biophys Biochem Cytol 10:425-436.
5. Coughlin DJ, Valdes L, Rome LC. 1996. Muscle length changes during swimming in scup: Sonomicrometry verifies the anatomical high-speed cine technique. J Exp Biol 199:459-463.
6. Danos N. 2005. Biomechanics of the skin during swimming in the American Eel, Anguilla rostrata. Masters Thesis. Amherst: University of Massachusetts, 47 p.
7. D'Aout K, Curtin NA, Williams TL, Aerts P. 2001. Mechanical properties of red and white swimming muscles as a function of the position along the body of the eel Anguilla anguilla. J Exp Biol 204:2221-2230.
8. Dingerkus G, Uhler DL. 1977. Enzyme clearing of Alcian blue-stained whole small vertebrates for demonstration of cartilage. Stain Technol 32:229-231.
9. Donley JM, Dickson KA. 2000. Swimming kinematics of juvenile Kawakawa Tuna (Euthynnus affinis) and Chub Mackerel (Scomber japonicus). J Exp Biol 203:3103-3116.
10. Donley JM, Shadwick RE. 2003. Steady swimming muscle dynamics in the leopard shark Triakis semifasciata. J Exp Biol 206:1117-1126.
11. Donley JM, Sepulveda CA, Konstantinidis P, Gemballa S, Shadwick RE. 2004. Convergent evolution in mechanical design of lamnid sharks and tunas. Nature 429:61-65.
12. Donley JM, Shadwick RE, Sepulveda CA, Konstantinidis P, Gemballa S. 2005. Longitudinal patterns of red muscle strain and activation and body kinematics during steady swimming in a lamnid shark, the shortfin mako (Isurus oxyrinchus). J Exp Biol 208:2377-2387.
13. Dowis JD, Sepulveda CA, Graham JB, Dickson KA. 2003. Swimming peformance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae). II. Kinematics. J Exp Biol 206:2749-2758.
14. Fishelson L. 1972. Histology and ultrastructure of the skin of Lepadichthys lineatus (Gobiesocidae: Teleostei). Mar Biol 17:357-364.
15. Fishelson L. 1996. Skin morphology and cytology in marine eels adapted to different lifestyles. Anat Rec 246:15-29.
16. Fujii R. 1968. Fine structure of the collagenous lamella underlying the epidermis of the goby, Chasmichthys gulosus. Annot Zool Jpn 41:95-106.
17. Gemballa S. 2005. Locomotory specializations in aquatic environments: Morphological differences in the axial musculotendinous system of cruising specialists and accelerators. Comp Biochem Physiol A 141:S163.
18. Gemballa S, Bartsch P. 2002. Architecture of the integument in lower teleostomes: Functional morphology and evolutionary implications. J Morphol 253:290-309.
19. Gemballa S, Hagen K. 2004. The myoseptal system in Chimaera monstrosa and its evolution in the gnathostome stem lineage. Zoology 107:13-27.
20. Gemballa S, Röder K. 2004. From head to tail: The myoseptal system in basal actinopterygians. J Morphol 259:155-171.
21. Gemballa S, Treiber K. 2003. Cruising specialists and accelerators - Are different types of fish locomotion driven by differently structured myosepta? Zoology 106:203-222.
22. Gemballa S, Vogel F. 2002. Spatial arrangement of white muscle fibers and myoseptal tendons in fishes. Comp Biochem Physiol A 133:1013-1037.
23. Gemballa S, Ebmeyer L, Hagen K, Hoja K, Treiber K, Vogel F, Weitbrecht GW. 2003a. Evolutionary transformations of myoseptal tendons in gnathostomes. Proc R Soc Lond B 270:1229-1235.
24. Gemballa S, Hagen K, Röder K, Rolf M, Treiber K. 2003b. The horizontal septum: Structure and evolutionary transformations in vertebrates. J Evol Biol 16:966-975.
25. Gemballa S, Konstantinidis P, Donley JM, Sepulveda C, Shadwick RE. 2006. Evolution of high-performance swimming in sharks: transformation of the musculotendinous system from subcarangidorm to thunniform swimmers. J Morphol 267:477-493.
26. Gemballa S, Kistner N, Sepulveda C, Bernal D. 2007. The musculotendinous system of pelagic fishes: How does swordfish (Xiphias gladius) compare to thunniform and carangifom swimmers? ICVM-8 abstract. J Morphol 268:1077.
27. Gillis GB. 1996. Undulatory locomotion in elongate aquatic vertebrates: Anguilliform swimming since Sir James Gray. Am Zool 36:656-665.
28. Gillis GB. 1997. Anguilliform locomotion in an elongate salamander (Siren intermedia): Effects of speed on axial undulatory movements. J Exp Biol 200:767-784.
29. Gillis GB. 1998a. Neuromuscular control of anguilliform locomotion: Patterns of red and white muscle activity during swimming in the American Eel Anguilla rostrata. J Exp Biol 201:3245-3256.
30. Gillis GB. 1998b. Environmental effects on undulatory locomotion in the American Eel Anguilla rostrata: Kinematics on water and land. J Exp Biol 201:949-961.
31. Gray J. 1933a. Studies in animal locomotion. I. The movement of fish with special reference to the eel. J Exp Biol 10:88-104.
32. Gray J. 1933b. Studies in animal locomotion. II. The relationship between waves of muscular contraction and the propulsive mechanism of the eel. J Exp Biol 10:386-390.
33. Gray J. 1933c. Studies in animal locomotion. III. The propulsive mechanism of the whiting (Gadus merlangus). J Exp Biol 10:391-400.
34. Gray J. 1968. Animal Locomotion. New York: WW Norton & Co.
35. Harris JE, Crofton HD. 1957. Structure and function in the nematodes - Internal pressure and cuticular structure in Ascaris. J Exp Biol 34:116-130.
36. Hawkes JW. 1974. Structure of fish skin. I. General organization. Cell Tissue Res 149:147-158.
37. Hebrank MR. 1980. Mechanical properties and locomotor functions of eel skin. Biol Bull 158:58-68.
38. Hebrank MR. 1982. Functional morphology of fishes: Roles of the backbone and skin in locomotion. Doctoral Dissertation, Duke University. 142 p.
39. Hebrank MR, Hebrank JH. 1986. The mechanics of fish skin - Lack of an external tendon role in 2 teleosts. Biol Bull 171:236-247.
40. Jayne BC. 1988. Mechanical-behavior of snake skin. J Zool 214:125-140.
41. Katz SL, Shadwick RE, Rapoport HS. 1999. Muscle strain histories in swimming milkfish in steady as well as sprinting gaits. J Exp Biol 2002:529-541.
42. Katz SL, Syme DA, Shadwick RE. 2001. High speed swimming: Enhanced power in yellowfin tuna. Nature 410:770-771.
43. Kern S, Koumoutsakos P. 2006. Simulations of optimized anguilliform swimming. J Exp Biol 209:4841-4857.
44. Lauder GV. 2006. Locomotion. In: Evans DH, Claiborne JB, editors. The Physiology of Fishes, 3rd ed. Boca Raton: CRC Press. pp 3-46.
45. Lauder GV, Tytell ED. 2006. Hydrodynamics of undulatory propulsion. In: Shadwick RE, Lauder GV, editors. Fish Biomechanics. Fish Physiology, Vol. 23. San Diego: Academic Press. pp 425-468.
46. Le Guellec D, Morvan-Dubois G, Sire JY. 2004. Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). Int J Dev Biol 48:217-231.
47. Leonard JB, Summers RG. 1976. Ultrastructure of integument of American eel. Anguilla rostrata. Cell Tissue Res 171:1-30.
48. Liem KF. 1967. Functional morphology of integumentary respiratory and digestive systems of synbranchoid fish Monopterus albus. Copeia 1967:375-388.
49. Lindsey CC. 1978. Form, function, and locomotory habits in fish. In: Hoar WS, Randall DJ, editors. Locomotion. Fish Physiology, Vol. 7. New York: Academic Press. pp 1-100.
50. Logan VH, Odense PH. 1974. Integument of ocean sunfish (Mola-Mola L) (Plectognathi) with observations on lesions from two ectoparasites. Capsala-Martinierei (Trematoda) and Philorthagoriscus-Serratus (Copepoda). Can J Zool 52:1039-1045.
51. Long JH Jr. 1998. Muscles, elastic energy, and the dynamics of body stiffness in swimming eels. Am Zool 38:771-792.
52. Long JH Jr, Hale ME, McHenry MJ, Westneat MWW. 1996. Functions of fish skin: Flexural stiffness and steady swimming of longnose gar Lepisosteus osseus. J Exp Biol 199:2139-2151.
53. Long JH Jr, Adcock B, Root RG. 2002. Force transmission via axial tendons in undulating fish: A dynamic analysis. Comp Biochem Physiol A 133:911-929.
54. Mittal AK, Banerjee TK. 1974. Structure and keratinization of the fresh water teleost Notopterus notopterus (Notopteridae, Pisces). J Zool (Lond) 174:341-355.
55. Mittal AK, Banerjee TK. 1975a. Histochemistry and structure of skin of a Murrel, Channa striata (Bloch, 1797) (Channiformes, Channidae). I. Epidermis. Can J Zool 53:833-843.
56. Mittal AK, Banerjee TK. 1975b. Histochemistry and structure of skin of a Murrel, Channa striata (Bloch, 1797) (Channiformes, Channidae). II. Dermis and subcutis. Can J Zool 53:844-852.
57. Motta PJ. 1977. Anatomy and functional-morphology of dermal collagen-fibers in sharks. Copeia 1977:454-464.
58. Müller UK, Smit J, Stamhuis EJ, Videler JJ. 2001. How the body contributes to the wake in undulatory swimming fish: Flow fields of a swimming eel (Anguilla anguilla). J Exp Biol 204:2751-2762.
59. Olsson R. 1961. The skin of Amphioxus. Z Zellforsch 54:90-104.
60. Patterson C, Johnson GD. 1995. The intermuscular bones and ligaments of teleostean bones. Smithsonian Contrib Zool 559:1-83.
61. Romeis B. 1986. Mikroskopische Technik. München: Urban and Schwarzenberg. 697 p.
62. Shadwick RE, Gemballa S. 2006. Kinematics and muscle dynamics in undulatory swimming. In: Shadwick RE, Lauder GV, editors. Fish Biomechanics. Fish Physiology, Vol. 23. San Diego: Academic Press. pp 241-280.
63. Shadwick RE, Steffensen JF, Katz SL, Knower T. 1998. Muscle dynamics in fish during steady swimming. Am Zool 38:755-770.
64. Shadwick RE, Katz SL, Korsmeyer K, Knower T, Covell JW. 1999. Muscle dynamics in skipjack tuna Katsuwonus pelamus: Timing of red muscle shortening and body curvature during steady swimming. J Exp Biol 202:2139-2150.
65. Tytell ED. 2004a. The hydrodynamics of eel swimming. II. Effect of swimming speed. J Exp Biol 207:3265-3279.
66. Tytell ED. 2004b. Kinematics and hydrodynamics of linear acceleration in eels, Anguilla rostrata. Proc R Soc Lond B 271:2535-2540.
67. Tytell ED, Lauder GV. 2004. The hydrodynamics of eel swimming. I. Wake structure. J Exp Biol 207:1825-1841.
68. Videler JJ. 1993. Fish Swimming. Fish and Fisheries Series 10. London: Chapman & Hall. 260 p.
69. Vogel S. 2004. Comparative Biomechanics. Princeton and Oxford: Princeton University Press.
70. Wardle CS, Videler JJ, Altringham JD. 1995. Tuning in to fish swimming waves: Body form, swimming mode and muscle function. J Exp Biol 198:1629-1636.
71. Westneat MW, Wainwright SA. 2001. Mechanical design for swimming: Muscle, tendon, and bone. In: Block BA, Stevens ED, editors. Tuna: Physiology, Ecology, and Evolution. Fish Physiology, Vol. 19. San Diego: Academic Press. pp 271-311.
72. Westneat MW, Hale ME, McHenry MJ, Long JH Jr. 1998. Mechanics of the fast-start: Muscle function and the role of intramuscular pressure in the escape behavior of Amia calva and Polypterus palmas. J Exp Biol 201:3041-3055.
73. Wainwright SA. 1983. To bend a fish. In: Webb PW, Weihs D, editors. Fish Biomechanics. New York: Praeger Publishers. pp 68-91.
74. Wainwright SA, Vosburgh F, Hebrank JH. 1978. Shark skin - Function in locomotion. Science 202:747-749.
75. Wainwright SA, Biggs WD, Currey JD, Gosline JM. 1982. Mechanical Design in Organisms. Princeton, New Jersey: Princeton University Press.