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

Publisher Summary This chapter reviews the functional capacities of fish skeletal structures and tissues, as those capacities have been determined by the measurement of mechanical properties under life‐like loading conditions. The mechanical workings of fishes have been approached in a two-pronged framework, with (1) muscle as the engine of motion and force and (2) water as the external source of resistance and purchase. The interaction of muscle and water certainly lays the foundation for behaviors as diverse as swimming, breathing, and feeding, but the interaction between them is only part of the picture. Understanding fishes as mechanical actors requires study of a third factor: the skeleton. This chapter defines skeleton broadly to include connective tissues such as tendon, ligament, cartilage, and bone that have a large component of extracellular collagen fibers. By measuring the mechanical properties of skeletal tissue and structures, one can begin modeling a few mechanical behaviors of a few species and understanding the integrated function of muscle, water, and skeleton. Even though the skeletal systems of fishes are complicated, analysis is helped by the often clear connection between skeletal structure and mechanical function, particularly when that correlation has convergently evolved. A clear causal connection is easily seen between the teeth and prey processing in heterodontid sharks and in sparid fish: their robust molariform teeth permit the crushing of hard prey such as mollusks and echinoderms.

[1]  M. Moss STUDIES OF THE ACELLULAR BONE OF TELEOST FISH. V. HISTOLOGY AND MINERAL HOMEOSTASIS OF FRESH-WATER SPECIES. , 1965, Acta anatomica.

[2]  S. Gemballa,et al.  Cruising specialists and accelerators--are different types of fish locomotion driven by differently structured myosepta? , 2003, Zoology.

[3]  M. E. Demont,et al.  Comparative equilibrium mechanical properties of bovine and lamprey cartilaginous tissues , 2003, Journal of Experimental Biology.

[4]  G. Lauder,et al.  Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in leopard sharks Triakis semifasciata. , 2000, The Journal of experimental biology.

[5]  Sven Gemballa,et al.  Architecture of the integument in lower teleostomes: Functional morphology and evolutionary implications , 2002, Journal of morphology.

[6]  A. Summers,et al.  Stiffening the stingray skeleton — an investigation of durophagy in Myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae) , 2000, Journal of morphology.

[7]  P. W. Webb,et al.  Kinematics of Pectoral Fin Propulsion in Cymatogaster Aggregata , 1973 .

[8]  M. Coates,et al.  Spines and tissues of ancient sharks , 1998, Nature.

[9]  Sven Gemballa,et al.  Convergent evolution in mechanical design of lamnid sharks and tunas , 2004, Nature.

[10]  M. Moss Skeletal Tissues in Sharks , 1977 .

[11]  Peter Geerlink,et al.  Pectoral Fin Kinematics of Coris Formosa (Teleostei, Labridae) , 1982 .

[12]  Adam P. Summers,et al.  Batoid wing skeletal structure: Novel morphologies, mechanical implications, and phylogenetic patterns , 2005, Journal of morphology.

[13]  Karel F. Liem,et al.  Functional Anatomy of the Vertebrates: An Evolutionary Perspective , 1994 .

[14]  C. Breder The locomotion of fishes , 1926 .

[15]  J. H. Long,et al.  Backbone Mechanics of the Blue Marlin Makaira Nigricans (Pisces, Istiophoridae) , 1990 .

[16]  Mary Reidy Hebrank,et al.  MECHANICAL PROPERTIES AND LOCOMOTOR FUNCTIONS OF EEL SKIN , 1980 .

[17]  Elizabeth L. Brainerd,et al.  Mechanical design of polypterid fish integument for energy storage during recoil aspiration , 1994 .

[18]  P. Motta,et al.  Trophic consequences of differential performance: ontogeny of oral jaw‐crushing performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae) , 1997 .

[19]  W. Salo,et al.  The hagfish slime gland: a model system for studying the biology of mucus. , 1981, Science.

[20]  J. H. Long Muscles, Elastic Energy, and the Dynamics of Body Stiffness in Swimming Eels' , 1998 .

[21]  K. Liem,et al.  Air Ventilation by Recoil Aspiration in Polypterid Fishes , 1989, Science.

[22]  L. B. Halstead Vertebrate hard tissues , 1974 .

[23]  J. Lundberg,et al.  Evolution and Functional Anatomy of the Pectoral Fin Rays in Cyprinoid Fishes, with Emphasis on the Suckers (Family Catostomidae) , 1976 .

[24]  T. Keaveny,et al.  Evolution of the biomechanical material properties of the femur , 2002, The Anatomical record.

[25]  Sven Gemballa,et al.  Spatial arrangement of white muscle fibers and myoseptal tendons in fishes. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[26]  Y. Zhang,et al.  The effect of molluscan glue proteins on gel mechanics , 2004, Journal of Experimental Biology.

[27]  B. Hall,et al.  DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES , 1990, Biological reviews of the Cambridge Philosophical Society.

[28]  C. A. Pell,et al.  The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes (Scombridae, Perciformes) , 1993, Journal of morphology.

[29]  Adam P. Summers,et al.  Structure and function of the horn shark (Heterodontus francisci) cranium through ontogeny: Development of a hard prey specialist , 2004, Journal of morphology.

[30]  Melina E. Hale,et al.  Functions of fish skin: flexural stiffness and steady swimming of longnose gar, Lepisosteus osseus , 1996, The Journal of experimental biology.

[31]  J. Hebrank,et al.  THE MECHANICS OF FISH SKIN: LACK OF AN "EXTERNAL TENDON" ROLE IN TWO TELEOSTS , 1986 .

[32]  Maureen Kearney,et al.  Cranial anatomy of the extinct amphisbaenian Rhineura hatcherii (Squamata, Amphisbaenia) based on high‐resolution X‐ray computed tomography , 2005, Journal of morphology.

[33]  S. Wainwright,et al.  Shark Skin: Function in Locomotion , 1978, Science.

[34]  John H. Long,et al.  The Importance of Body Stiffness in Undulatory Propulsion , 1996 .

[35]  L. Hernandez,et al.  Intraspecific scaling of feeding mechanics in an ontogenetic series of zebrafish, Danio rerio. , 2000, The Journal of experimental biology.

[36]  Thomas L. Daniel,et al.  Forward flapping flight from flexible fins , 1988 .

[37]  L. Grande,et al.  A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy : an empirical search for interconnected patterns of natural history , 1998 .

[38]  G. Pharr,et al.  Correlations between osteocalcin content, degree of mineralization, and mechanical properties of C. carpio rib bone. , 2001, Journal of biomedical materials research.

[39]  Robert J. Schmitz Ultrastructure and function of cellular components of the intercentral joint in the percoid vertebral column , 1995, Journal of morphology.

[40]  J. V. van Leeuwen,et al.  Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development , 2004, Journal of Experimental Biology.

[41]  F. G. Evans,et al.  The comparative morphology of the vertebrate spinal column. Its form as related to function , 1938 .

[42]  Christian Riekel,et al.  The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. , 2003, Biophysical journal.

[43]  Iu G Aleev,et al.  Function and gross morphology in fish , 1969 .

[44]  M. Glimcher,et al.  Three-dimensional spatial relationship between the collagen fibrils and the inorganic calcium phosphate crystals of pickerel (Americanus americanus) and herring (Clupea harengus) bone. , 1991, Journal of molecular biology.

[45]  E. Brainerd Pufferfish inflation: Functional morphology of postcranial structures in Diodon holocanthus (Tetraodontiformes) , 1994, Journal of morphology.

[46]  J. Videler,et al.  On the interrelationships between morphology and movement in the tail of cichlid fish Tilapia nilotica (L.). , 1974 .

[47]  R. Shadwick,et al.  Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[48]  M. Benjamin Hyaline-cell cartilage (chondroid) in the heads of teleosts , 2004, Anatomy and Embryology.

[49]  P. Robson,et al.  A Family of Non–Collagen-Based Cartilages in the Skeleton of the Sea Lamprey, Petromyzon marinus , 1997 .

[50]  E. Azizi,et al.  Morphology and mechanics of myosepta in a swimming salamander (Siren lacertina). , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[51]  S. Gemballa,et al.  From head to tail: The myoseptal system in basal actinopterygians , 2004, Journal of morphology.

[52]  B. Hall,et al.  The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa. , 2004, Zoology.

[53]  John H Long,et al.  The notochord of hagfish Myxine glutinosa: visco-elastic properties and mechanical functions during steady swimming. , 2002, The Journal of experimental biology.

[54]  W. Bemis Paedomorphosis and the evolution of the Dipnoi , 1984, Paleobiology.

[55]  Bruce M. Adcock,et al.  Force transmission via axial tendons in undulating fish: a dynamic analysis. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[56]  R. McN. Alexander,et al.  The orientation of muscle fibres in the myomeres of fishes , 1969, Journal of the Marine Biological Association of the United Kingdom.

[57]  J. Ralphs,et al.  Cartilage and related tissues in the trunk and fins of teleosts. , 1992, Journal of anatomy.

[58]  A. Blight THE MUSCULAR CONTROL OF VERTEBRATE SWIMMING MOVEMENTS , 1977 .

[59]  S. Gemballa,et al.  Locomotory design of ‘cyclostome’ fishes: Spatial arrangement and architecture of myosepta and lamellae , 2001 .

[60]  K. Shephard Functions for fish mucus , 1994, Reviews in Fish Biology and Fisheries.

[61]  J. Currey The design of mineralised hard tissues for their mechanical functions. , 1999, The Journal of experimental biology.

[62]  M. Westneat,et al.  Diversity of pectoral fin structure and function in fishes with labriform propulsion , 2005, Journal of morphology.

[63]  F. Keeley,et al.  Cartilage in the Atlantic hagfish, Myxine glutinosa. , 1984, The American journal of anatomy.

[64]  J. Videler,et al.  FAST CONTINUOUS SWIMMING OF SAITHE (POLLACHIUS VIRENS): A DYNAMIC ANALYSIS OF BENDING MOMENTS AND MUSCLE POWER , 1984 .

[65]  R. Blickhan,et al.  Muscle forces during locomotion in kangaroo rats: force platform and tendon buckle measurements compared. , 1988, The Journal of experimental biology.

[66]  J. Gosline,et al.  Molecular design of the α–keratin composite: insights from a matrix–free model, hagfish slime threads , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  E. Grogan,et al.  Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes , 1997, Reviews in Fish Biology and Fisheries.

[68]  Lauder,et al.  KINEMATICS OF PECTORAL FIN LOCOMOTION IN THE BLUEGILL SUNFISH LEPOMIS MACROCHIRUS , 1994, The Journal of experimental biology.

[69]  M R Hebrank,et al.  Mechanical properties of fish backbones in lateral bending and in tension. , 1982, Journal of biomechanics.

[70]  J. Videler,et al.  The Relation Between Structure and Bending Properties of Teleost Fin Rays , 1986 .

[71]  Morphology, mechanics, and locomotion: the relation between the notochord and swimming motions in sturgeon , 1995 .

[72]  SWIMMING FISH AND FISH-LIKE MODELS: THE HARMONIC STRUCTURE OF UNDULATORY WAVES SUGGESTS THAT FISH ACTIVELY TUNE THEIR BODIES , 1999 .

[73]  M. Benjamin The cranial cartilages of teleosts and their classification. , 1990, Journal of anatomy.

[74]  L. Lanyon,et al.  Mechanical function as an influence on the structure and form of bone. , 1976, The Journal of bone and joint surgery. British volume.

[75]  Bruce B. Collette,et al.  The Diversity of Fishes , 1997 .

[76]  Mchenry,et al.  UNDULATORY SWIMMING: HOW TRAVELING WAVES ARE PRODUCED AND MODULATED IN SUNFISH (LEPOMIS GIBBOSUS) , 1994, The Journal of experimental biology.

[77]  Adam P. Summers,et al.  The evolution of tendon--morphology and material properties. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[78]  Steven Vogel,et al.  Comparative Biomechanics: Life's Physical World , 2003 .

[79]  Williams,et al.  Self-propelled anguilliform swimming: simultaneous solution of the two-dimensional navier-stokes equations and Newton's laws of motion , 1998, The Journal of experimental biology.

[80]  Reinhard Blickhan,et al.  Bending Moment Distribution along Swimming Fish , 1994 .

[81]  Robert E Shadwick,et al.  Structure and function of tuna tail tendons. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[82]  D'arcy W. Thompson On growth and form i , 1943 .

[83]  John H. Long,et al.  Stiffness and Damping Forces in the Intervertebral Joints of Blue Marlin (Makaira Nigricans) , 1992 .

[84]  G. M. Pharr,et al.  Relationship Between Ultrastructure and the Nanoindentation Properties of Intramuscular Herring Bones , 2004, Annals of Biomedical Engineering.

[85]  W. G. Ridewood On the Calcification of the Vertebral Centra in Sharks and Rays , 1921 .

[86]  F. Keeley,et al.  Lamprin: A new vertebrate protein comprising the major structural protein of adult lamprey cartilage , 1983, Experientia.

[87]  Michael E Alfaro,et al.  EVOLUTIONARY DYNAMICS OF COMPLEX BIOMECHANICAL SYSTEMS: AN EXAMPLE USING THE FOUR‐BAR MECHANISM , 2004, Evolution; international journal of organic evolution.

[88]  J. Currey,et al.  Mechanical properties of vertebrate hard tissues , 1998, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[89]  S. Gemballa,et al.  Structure and evolution of the horizontal septum in vertebrates , 2003, Journal of evolutionary biology.

[90]  Julian F. V. Vincent,et al.  Biomechanics--materials : a practical approach , 1992 .

[91]  David L. Butler,et al.  Mechanical design in organisms , 1986 .

[92]  R. M. Alexander,et al.  Elastic mechanisms in animal movement , 1988 .

[93]  R. W. Blake,et al.  The Mechanics of Labriform Locomotion I. Labriform Locomotion in the Angelfish (Pterophyllum Eimekei): An Analysis of the Power Stroke , 1979 .

[94]  L. Lanyon,et al.  FUNCTIONAL ANATOMY OF FEEDING IN THE BLUEGILL SUNFISH, LEPOMIS MACROCHIRUS: IN VIVO MEASUREMENT OF BONE STRAIN , 1980 .

[95]  J. H. Long,et al.  Modeling a swimming fish with an initial boundary value problem: Unsteady maneuvers of an elastic plate with internal force generation , 1999 .

[96]  Everard Home,et al.  IX. On the nature of the intervertebral substance in fish and quadrupeds , 1809, Philosophical Transactions of the Royal Society of London.

[97]  P. Webb,et al.  The effect of armored skin on the swimming of longnose gar, Lepisosteus osseus , 1992 .

[98]  John D. Currey,et al.  Bones: Structure and Mechanics , 2002 .

[99]  A. Biewener,et al.  In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. , 1998, The Journal of experimental biology.

[100]  M. Moss Studies of the acellular bone of teleost fish. II. Response to fracture under normal and acalcemic conditions. , 1962, Acta anatomica.

[101]  P. Motta Anatomy and Functional Morphology of Dermal Collagen Fibers in Sharks , 1977 .

[102]  M. Westneat,et al.  Evolution of Levers and Linkages in the Feeding Mechanisms of Fishes1 , 2004, Integrative and comparative biology.