Skin and Bones, Sinew and Gristle: the Mechanical Behavior of Fish Skeletal Tissues

Fish Physiology

Volumn 23, Issue C, 2005, Pages 141-177

  Summers, Adam P ^a   Long Jr , John H ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77956733763     PISSN: 15465098     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1546-5098(05)23005-4     Document Type: Review

References (127)

1. Aleev Y.G. "Function and Gross Morphology in Fish." (1969), Keter Press, Jerusalem
2. Alexander R.M. Orientation of muscle fibres in myomeres of fishes. J. Mar. Biol. Assoc. UK 49 (1969) 263-290
3. Alexander R.M. "Elastic Mechanisms in Animal Movement." (1984), Cambridge University Press, Cambridge, UK
4. Alfaro M.E., Bolnick D.I., and Wainwright P.C. Evolutionary dynamics of complex biomechanical systems: An example using the four-bar mechanism. Evolution 58 (2004) 495-503
5. Azizi E., Gillis G.B., and Brainerd E.L. Morphology and mechanics of myosepta in a swimming salamander (Siren lacertina). Comp. Biochem. Physiol. 133 (2002) 967-978
6. Bemis W.E. Paedomorphosis and the evolution of the Dipnoi. Paleobiology 10 (1984) 293-307
7. Benjamin M. Hyaline-cell cartilage (chondroid) in the heads of teleosts. Anat. Embryol. 179 (1989) 285-303
8. Benjamin M. The cranial cartilages of teleosts and their classification. J. Anat. 169 (1990) 153-172
9. Benjamin M., Ralphs J.R., and Eberewariye O.S. Cartilage and related tissues in the trunk and fins of teleosts. J. Anat. 181 (1992) 113-118
10. Bernal D., Dickson K.A., Shadwick R.E., and Graham J.B. Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comp. Biochem. Physiol. 129 (2001) 695-726
11. Biewener A.A., Blickhan R., Perry A.K., Heglund N.C., and Taylor C.R. Muscle forces during locomotion in kangaroo rats: Force platform and tendon buckle measurements compared. J. Exp. Biol. 137 (1988) 191-205
12. Biewener A.A., Konieczynski D.D., and Baudinette R.V. In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. J. Exp. Biol. V201 (1998) 1681-1694
13. Blake R.W. The mechanics of labriform locomotion in the angelfish (Pterphyllum eimekei): an analysis of the power stroke. J. Exp. Biol. 82 (1979) 255-271
14. Blake R.W. "Fish Locomotion." (1983), Cambridge University Press, London
15. Blight A.R. The muscular control of vertebrate swimming movements. Biol. Rev. 52 (1977) 181-218
16. Brainerd E.L. Mechanical design of polypterid fish integument for energy storage during recoil aspiration. J. Zool. (Lond.) 232 (1994) 7-19
17. Brainerd E.L. Pufferfish inflation: functional morphology of postcranial structures in Diodon holocanthus (Tetraodontiformes). J. Morphol. 220 (1994) 243-261
18. Brainerd E.L., Liem K.F., and Samper C.T. Air ventilation by recoil aspiration in polypterid fishes. Science 246 (1989) 1593-1595
19. Breder C.M.J. The locomotion of fishes. Zoologica 4 (1926) 159-297
20. Carling J.C., Williams T.L., and Bowtell G. Self-propelled anguilliform swimming: simultaneous solution of the two-dimensional Navier-Stokes equations and Newton's laws of motion. J. Exp. Biol. 201 (1998) 3143-3166
21. Cheng J.-Y., and Blickhan R. Bending moment distribution along swimming fish. J. Theor. Biol. 168 (1994) 337-348
22. Coates M.I., Sequeira S.E.K., Sansom I.J., and Smith M.M. Spines and tissues of ancient sharks. Nature 396 (1998) 729-730
23. Cole A.G., and Hall B.K. The nature and significance of invertebrate cartilages revisited: Distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107 4 (2004) 261-274
24. Courtland H.W., Wright G.M., Root R.G., and DeMont M.E. Comparative equilibrium mechanical properties of bovine and lamprey cartilaginous tissues. J. Exp. Biol. 206 (2003) 1397-1408
25. Currey J.D. Mechanical properties of vertebrate hard tissues. Proc. Inst. Mech. Eng. 212 (1998) 399-411
26. Currey J.D. The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202 (1999) 3285-3294
27. Currey J.D. "Bones: Structure and Mechanics." (2002), Princeton University Press, Princeton, NJ
28. Czuwala P.J., Blanchette C., Varga S., Root R.G., and Long Jr. J.H. A mechanical model for the rapid body flexures of fast-starting fish. "Proceedings of the 11th International Symposium on Unmanned Untethered Submersible Technology," (1999) 415-426
29. Daniel T.L. Forward flapping flight from flexible fins. Can. J. Zool. 66 (1988) 630-638
30. Donely J.M., Sepulveda C.A., Konstantinidis P., Gemballa S., and Shadwick R.E. Convergent evolution in mechanical design of lamnid sharks and tunas. Nature 429 (2004) 61-65
31. Downing S.W., Salo W.L., Spitzer R.H., and Koch E.A. The hagfish slime gland: A model system for studying the biology of mucus. Science 214 (1981) 1143-1145
32. Erickson G.M., Catanese J., and Keaveny T.M. Evolution of the biomechanical material properties of the femur. Anat. Rec. 268 (2002) 115-124
33. Fudge D.S., and Gosline J.M. Molecular design of the alpha-keratin composite: Insights from a matrix-free model, hagfish slime threads. Proc. Roy. Soc. Lond. B Biol. Sci. 271 (2004) 291-299
34. Fudge D.S., Gardner K., Forsyth V.T., Riekel C., and Gosline J.M. The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads. Biophys. J. 85 (2003) 2015-2027
35. Geerlink P.J. Pectoral fin kinematics of Coris formosa (Teleostei, Labridae). Neth. J. Zool. 33 (1983) 515-531
36. Geerlink P.J., and Videler J.J. The relation between structure and bending properties of teleost fin rays. Neth. J. Zool. 37 1 (1987) 59-80
37. Gemballa S., and Bartsch P. Architecture of the integument in lower teleostomes: Functional morphology and evolutionary implications. J. Morphol. 253 (2002) 290-309
38. Gemballa S., and Britz R. The homology of the intermuscular bones in acanthomorph fishes. Am. Mus. Novitates 3241 (1998) 1-25
39. Gemballa S., and Roder K. From head to tail: The myoseptal system in basal actinopterygians. J. Morphol. 259 (2004) 155-171
40. Gemballa S., and Treiber K. Cruising specialists and accelerators-Are different types of fish locomotion driven by differently structured myosepta?. Zoology 106 (2003) 203-222
41. Gemballa S., and Vogel F. Spatial arrangement of white muscle fibers and myoseptal tendons in fishes. Comp. Biochem. Physiol. Mol. Integ. Physiol. 133 (2002) 1013-1037
42. Gemballa S., and Vogel F. The spatial arrangement of white muscle fibers and myoseptal tendons in fishes: How may muscle fibers and myoseptal tendons work together to induce bending?. Comp. Biochem. Physiol. 133 (2002) 1013-1037
43. Gemballa S., Hagen K., Roder K., Rolf M., and Treiber K. Structure and evolution of the horizontal septum in vertebrates. J. Evol. Biol. 16 (2003) 966-975
44. Gibb A.C., Jayne B.C., and Lauder G.V. Kinematics of pectoral fin locomotion in the bluegill sunfish Lepomis macrochirus. J. Exp. Biol. 189 (1994) 133-161
45. Gordon J.E. "The New Science of Strong Materials, or, Why You Don't Fall through the Floor." (1984), Princeton University Press, Princeton, NJ
46. Grande L., and Bemis W.E. A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. J. Vert. Paleontol. Sp. Mem. 44 (1984) 1-690 (suppl. to Vol. 18).
47. Hagen K., Gemballa S., and Freiwald A. Locomotory design and locomotory habits of Chimaera monstrosa. J. Morphol. 248 (2001) 237
48. Halstead L.B. "Vertebrate Hard Tissues." (1974), Wykeham Publications distributed by Chapman & Hall, London
49. Hebrank J.H., Hebrank M.R., Long J.H., Block B.A., and Wainwright S.A. Backbone mechanics of the blue marlin Makaira nigricans (Pisces: Istiophoridae). J. Exp. Biol. 148 (1990) 449-459
50. Hebrank M.R. Mechanical properties and locomotor functions of eel skin. Biolog. Bull. 158 (1980) 58-68
51. Hebrank M.R. Mechanical properties of fish backbones in lateral bending and tension. J. Biomech. 15 (1982) 85-89
52. Hebrank M.R., and Hebrank J.H. The mechanics of fish skin: The lack of an external tendon in two teleosts. Biolog. Bull. 171 (1986) 236-247
53. Helfman G.S., Collette B.B., and Facey D.E. "The Diversity of Fishes." (1997), Blackwell Science Malden, MA
54. Hernandez L.P. Intraspecific scaling of feeding mechanics in an ontogenetic series of zebrafish, Danio rerio. J. Exp. Biol. 203 (2000) 3033-3043
55. Hernandez L.P., and Motta P.J. Trophic consequences of differential performance: Ontogeny of oral jaw-crushing performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae). J. Zool. 243 (1997) 737-756
56. Hess F., and Videler J.J. Fast continuous swimming of Saithe (Pollachius virens): A dynamic analysis of bending moments and muscle power. J. Exp. Biol. 109 (1984) 229-251
57. Home E. On the nature of the intervetebral substance in fish and quadrupeds. Phil. Trans. Roy. Soc. 99 (1809) 177-187
58. Horton J.M., Drucker E.G., and Summers A.P. Swiftly swimming fish show evidence of stiff spines. Integ. Comp. Zool. 43 (2004) 905
59. Junquiera L.C.U., Toledo O.M.S., and Montes G.S. Histochemical and morphological studies of a new type of acellular cartilage. Basic Appl. Histochem. 27 (1983) 1-8
60. Koob T.J., and Long Jr. J.H. The vertebrate body axis: Evolution and mechanical function. Am. Zool. 40 1 (2000) 1-18
61. Lakes R.S. "Viscoelastic Solids." (1999), CRC Press, Boca Raton, FL
62. Lanyon L.E., and Baggott D.G. Mechanical function as an influence on the structure and form of bone. J. Bone Joint Surg. 58 (1976) 436-443
63. Lauder G.V., and Lanyon L.E. Functional anatomy of feeding in the bluegill, Lepomis macrochirus: In vivo measurement of bone strain. J. Exp. Biol. 84 (1980) 33-55
64. Lee D.D., and Glimcher M.J. Three dimensional spacial relationship between collagen fibrils and the inorganic calcium phosphate crystals of pickeral and herring bone. J. Mol. Biol. 217 (1991) 487-501
65. Librizzi N.N., Long Jr. J.H., and Root R.G. Modeling a swimming fish with an initial-boundary value problem: Unsteady maneuvers of an elastic plate with internal force generation. Comp. Math. Model. 30 11/12 (1999) 77-93
66. Liem K.F., Bemis W.E., Walker Jr. W.F., and Grande L. "Functional Anatomy of the Vertebrates: An Evolutionary Perspective, Third Ed." (2001), Harcourt, New York
67. Long J.H. Stiffness and damping forces in the intervertebral joints of blue marlin (Makaira nigricans). J. Exp. Biol. 162 (1992) 131-155
68. Long Jr. J.H., McHenry M.J., and Boetticher N.C. Undulatory swimming: How traveling waves are produced and modulated in sunfish (Lepomis gibbosus). J. Exp. Biol. 192 (1994) 129-145
69. Long J.H. Morphology, mechanics, and locomotion-The relation between the notochord and swimming motions in sturgeon. Environ. Biol. Fishes 44 (1995) 199-211
70. Long J.H. Muscle, elastic energy, and dynamics of body stiffness in swimming eels. Am. Zool. 38 4 (1998) 181-202
71. Long J.H., and Nipper K.S. The importance of body stiffness in undulatory propulsion. Am. Zool. 36 (1996) 678-694
72. Long J.H., Hale M.E., McHenry M.J., and Westneat M.W. Functions of fish skin: Flexural stiffness and steady swimming of longnose gar Lepisosteus osseus. J. Exp. Biol. 199 (1996) 2139-2151
73. Long J.H., Koob-Emunds M., Sinwell B., and Koob T.J. The notochord of hagfish Myxine glutinosa: Visco-elastic properties and mechanical functions during steady swimming. J. Exp. Biol. 205 (2002) 3819-3831
74. Long Jr. J.H., Adcock B., and Root R.G. Force transmission via axial tendons in undulating fish: A dynamic analysis. Comp. Biochem. Physiol. A 133 (2002) 911-929
75. Lund R., and Grogan E.D. Relationships of the chimaeriformes and the basal radiation of the Chondrichthyes. Rev. Fish Biol. Fisheries 7 (1997) 65-123
76. Lundberg J.G., and Baskin J.N. The caudal skeleton of the catfishes, order Siluriformes. Am. Mus. Novitates 2398 (1969) 1-49
77. Lundberg J.G., and Marsh E. The evolution and functional anatomy of the pectoral fin rays in cyprinoid fishes, with emphasis on the suckers (family Catostomidae). Am. Midland Natur. 96 2 (1976) 332-349
78. Madden P.G., and Lauder G.V. Pectoral fin locomotion in fishes: Fin ray deformation and material properties. Integ. Comp. Biol. 43 (2003) 903
79. Martin R.B., Burr D.B., and Sharkey N.A. "Skeletal Tissue Mechanics." (1998), Springer, New York
80. Martinez G., Drucker E.G., and Summers A.P. Under pressure to swim fast. Integ. Comp. Biol. 42 (2003) 1273-1274
81. Moss M.L. Studies of the acellular bone of teleost fish. I. Morphological and systematic variation. Acta Anatom. 46 (1961) 343-362
82. Moss M.L. Studies of the acellular bone of teleost fish. II. Response to fracture under normal and acalcemic conditions. Acta Anatom. 48 (1961) 46-60
83. Moss M.L. Skeletal tissue in sharks. Am. Zool. 17 (1977) 335-342
84. Motta P.J. Anatomy and functional morphology of dermal collagen fibers in sharks. Copeia 1977 (1977) 454-464
85. Mueller U.K., and van Leeuwen J.L. Swimming of larval zebrafish: Ontogeny of body waves and implications for locomotory development. J. Exp. Biol. 207 (2004) 853-868
86. Ørvig T. Histologic studies of Placoderm and fossil elasmobranchs. I. The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Arkiv. Zoolog. 2 (1951) 321-454
87. Pawlicki J.M., Pease L.B., Pierce C.M., Startz T.P., Zhang Y., and Smith A.M. The effect of molluscan glue proteins on gel mechanics. J. Exp. Biol. 207 (2004) 1127-1135
88. Porter M., and Summers A.P. Biochemical and structural properties of the cartilaginous vertebral column of sharks. Integ. Comp. Biol. 43 (2004) 828
89. Raven H.C. On the anatomy and evolution of the locomotor apparatus of the nipple-tailed ocean sunfish (Masturus lanceolatus). Bull. Am. Mus. Nat. His. 76 (1939) 143-150
90. Rho J.Y., Mishra S.R., Chung K., Bai J., and Pharr G.M. Relationship between ultrastructure and the nanoindentation properties of intramuscular herring bones. Ann. Biomed. Eng. 29 (2001) 1082-1088
91. Ridewood W.G. On the calcification of the vertebral centra in sharks and rays. Phil. Trans. Roy. Soc. Lond. 210 (1921) 311-407
92. Robson P., Wright G.M., Youson J.H., and Keeley F.W. A family of non-collagen-based cartilages in the skeleton of the sea lamprey, Petromyzon marinus. Comp. Biochem. Physiol. B 118 (1997) 71-78
93. Robson P., Wright G.M., and Keeley F.W. Distinct non-collagen based cartilages comprising the endoskeleton of the Atlantic hagfish, Myxine glutinosa. Anat. Embryol. 202 (2000) 281-290
94. Rockwell H., Evans F.G., and Pheasant H.C. The comparative morphology of the vertebrate spinal column: its form as related to function. J. Morphol. 63 (1938) 87-117
95. Root R.G., Courtland H.-W., Pell C.A., Hobson B., Twohig E.J., Suter R.J., Shepherd III W.R., Boetticher N., and Long Jr. J.H. Swimming fish and fish-like models: The harmonic structure of undulatory waves suggests that fish actively tune their bodies. "Proceedings of the 11th International Symposium on Unmanned Untethered Submersible Technology," (1999) 378-388
96. Roy M.E., Nishimoto S.K., Rho J.Y., Bhattacharya S.K.A., Lin J.S., and Pharr G.M. Correlations between osteocalcin content, degree of mineralization, and mechanical properties of C. carpio rib bone. J. Biomed. Mat. Res. 54 (2001) 547-553
97. Schaefer J.T., and Summers A.P. Batoid wing skeletal structure: Novel morphologies, mechanical implications, and phylogenetic patterns. J. Morphol. 264 (2005) 1-16
98. Schmitz R.J. Ultrastructure and function of cellular components of the intercentral joint in the percoid vertebral column. J. Morphol. 226 (1995) 1-24
99. Shadwick R.E., Rapoport H.S., and Fenger J.M. Structure and function of the tuna tail tendons. Comp. Biochem. Physiol. 133A (2002) 1109-1126
100. Shephard K.L. Functions for fish mucus. Rev. Fish Biol. Fisheries 4 (1994) 401-429
101. Smith B.G. The heterodontid sharks: their natural history, and the external development of Heterodontus japonicus based on notes and drawings by Bashford Dean. In: Gudger E.W. (Ed). "The Bashford Dean Memorial Volume-Archaic Fishes," Vol. VIII (1942), American Museum of Natural History, New York 651-769
102. Smith M.M., and Hall B.K. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65 (1990) 277-373
103. Summers A.P. Stiffening the stingray skeleton-An investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatoidea). J. Morphol. 243 (2000) 113-126
104. Summers A.P., and Koob T.J. The evolution of tendon. Comp. Biochem. Physiol. 133 (2002) 1159-1170
105. Summers A.P., Ketcham R., and Rowe T. Structure and function of the horn shark (Heterodontus francsisi) cranium through ontogeny-The development of a hard prey crusher. J. Morphol. 260 (2004) 1-12
106. Symmons S. Notochordal and elastic components of the axial skeleton of fishes and their functions in locomotion. J. Zool. (Lond.) 189 (1979) 157-206
107. Thompson D.A.W. "On Growth and Form." (1917), Cambridge University Press, London
108. Thorsen D.H., and Westneat M.W. Diversity of pectoral fin structure and function in fishes with labriform propulsion. J. Morphol. 263 (2005) 133-150
109. Videler J.J. On the interrelationships between morphology and movement in the tail of the cichlid fish Tilapia nilotica (L). Neth. J. Zool. 25 (1974) 143-194
110. Videler J.J. "Fish Swimming." (1993), Chapman and Hall, London
111. Vincent J.F.V. "Biomechanics-Materials: A Practical Approach." (1992), IRL Press at Oxford University Press, Oxford, UK
112. Vincent J. "Structural Biomaterials, Revised Ed." (1990), Princeton University Press, Princeton, NJ
113. Vogel F., and Gemballa S. Locomotory design of 'cyclostome' fishes: Spatial arrangement and architecture of myosepta and lamellae. Acta Zoolog. (Stockholm) 81 (2000) 267-283
114. Vogel S. "Comparative Biomechanics: Life's Physical World." (2003), Princeton University Press, Princeton, NJ
115. Wainwright S.A., Biggs W.D., Currey J.D., and Gosline J.M. "Mechanical Design in Organisms." (1976), Princeton University Press, Princeton, NJ
116. Wainwright S.A., Vosburgh F., and Hebrank J.H. Shark skin: Function in locomotion. Science 202 (1978) 747-749
117. Webb J.E. The role of the notochord in forward and reverse swimming and burrowing in the amphioxus Branchiostoma lanceolatum. J. Zool. (Lond.) 170 (1973) 325-338
118. Webb P.W. Kinematics of pectoral fin propulsion in Cymatogaster aggregata. J. Exp. Biol. 59 (1973) 697-710
119. Webb P.W., Hardy D.H., and Mehl V.L. The effect of armored skin on the swimming of longnose gar, Lepisosseus osseus. Can. J. Zool. 70 (1992) 1173-1179
120. Weitbrecht G.W., and Gemballa S. Arrangement and architecture of myosepta in the lancelet Branchiostoma lanceolatum. J. Morphol. 248 (2001) 299
121. Westneat M.W. Evolution of levers and linkages in the feeding mechanisms of fishes. Integ. Comp. Biol. 44 (2004) 378-389
122. Westneat M.W., Hoese W., Pell C.A., and Wainwright S.A. The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes (Scombridae, Perciformes). J. Morphol. 217 (1993) 183-204
123. Wilga C.D., and Lauder G.V. Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in leopard sharks Triakis semifasciata. J. Exp. Biol. 203 (2000) 2261-2278
124. Wright G.M., Keeley F.W., and Youson J.H. Lamprin: A new vertebrate protein comprising the major structural protein of adult lamprey cartilage. Experientia 39 (1983) 495-497
125. Wright G.M., Youson J.H., and Keeley F.W. Lamprey cartilage: A new type of vertebrate cartilage. Anat. Rec. 205 (1983) 221A
126. Wright G.M., Keeley F.W., Youson J.H., and Babineau D.L. Cartilage in the Atlantic hagfish, Myxinus glutinosa. Am. J. Anat. 169 (1984) 407-424
127. Yanega G., and Rubega M. Placing intramandibular kinesis in hummingbirds in the context of tetrapod feeding evolution. Integ. Comp. Biol. 43 (2003) 983 -983.