© 2000 by The Society for Integrative and Comparative Biology
The Animal Axis1
1 Zoology Department, Duke University, Durham, North Carolina 27708, USA
2 E-mail: sawanryt{at}duke.edu
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Soft-bodied animals are an answer to the problem, solved for each species over evolutionary time, to design a cylindrical, motile machine composed of pliant polymeric materials (collagen and glycoproteins) and actuated by a contractile polymer (actomyosin).
The vertebrate body is a cylindrical set of pliant collagenous membranes. Axial notochords and backbones occur where membranes intersect. The basis for all vertebrate architecture is the collagen fiber that best functions to resist tension. Axial compressive forces in notochords and backbones occur as tensile stresses in collagen fibers in intervertebral discs and zygapohyseal ligaments. Bone provides local stiffening where muscles pull. Large muscle masses apply large forces via tendons thus allowing for leverage in the function of axes of bodies and appendages. Although isolated species in invertebrate phyla have notochord- or backbone-like structures, only echinoderms and vertebrates have a central axis to resist axial compression. Design is a useful tool in forming scientific hypotheses.
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INTRODUCTION |
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The vertebrate axis we celebrate in this symposium is a mechanical supportive structure, either a notochord or a backbone (vertebral column).
A notochord consists of a fibrous collagenous sheath filled with large, vacuolated cells and some intercellular polymeric material. A backbone is composed of a series of cartilaginous or bony vertebrae connected by collagenous intervertebral joints (IVJ). The generic backbone is thought to be derived evolutionarily and in some species developmentally from a notochord by the constriction of the notochordal cavity and the segmental addition of cartilage and, ultimately, extracellular submicroscopic crystals of hydroxyapatite in calcified cartilage or bone. In every vertebrate the notochord or backbone lies between the gut and the dorsal hollow nerve chord. In embryos of amphioxus, fishes, amphibians, and reptiles the notochord develops as a longitudinal outpocketing of the dorsal wall of the gut in response to induction by the overlying nerve chord. In young and adult vertebrates the function of the axial structure is mechanical support. This axial support structure is the subject of the present account that takes a mechanical, historical, and designing approach to the vertebrate axis.
Let us review the fundamental features of the vertebrate body as context for notochords and backbones. As we go, let us remember that the vertebrate body is a subset of a larger category, the animal body: invertebrate bodies and axes will be treated below after the discussion of backbones.
The model vertebrate body here is a cylindrical form whose length is several times its diameter. It was nicely described by Goodrich (1930)
in his textbook of comparative vertebrate anatomy. Goodrich's diagram is reproduced here once again (Fig. 1). The first words in his text are still germane:
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"The entire body of a vertebrate is supported by a framework of connective tissue which packs and binds the various parts together, delimits spaces,and serves for the attachment of muscles. Doubtless primitively the vertebrates had an elongated body stiffened by the notochordal rod, and moved by a side-to-side bending more especially of the caudal region. Correlated with this mode of progression is the segmentation of the somatic or body-wall muscles, entailing the corresponding segmentation of the peripheral nervous system and the skeleton." And on page 2, "...endoskeletal cartilage and bone may be looked upon as local specializations of the general connective tissue system developed in those regions where the stresses are most pronounced and where muscle attachment needs most support."
Notice that there is no muscle, gut, excretory,reproductive or endocrine tissue represented in the figure. What is shown is the basic architectural layout in which all the juicy "interesting" tissues and organs are "packed and bound." This is the architecture that supports and is supported by the vertebrate axis, namely the notochord or vertebral column. The framework is basically a hollow cylinder of collagenous connective tissue, the skin.
The membrane-bound cavity is divided into left and right halves by a collagenous membrane, the vertical septum, that attaches to the skin or body wall along mid-dorsal and mid-ventral lines. There is also a horizontal collagenous membrane, the horizontal septum, that divides the dorsal and ventral halves, and attaches to skin or body wall along midlateral lines from head to tail. Where these two great septa meet in the midline is where the notochord or backbone lies. The central nervous system lies in the vertical septum above the notochord or backbone while the gut lies within the ventral part of the vertical septum, suspended in the body cavity. Seen in transverse section, the body cavity is thus divided into quarters that are filled in the first approximation with muscle. In amphioxus and vertebrates these long tenderloins of muscle are each divided into a series of segments, the myotomes, along the body that are separated and connected by collagenous membranes, the myosepta. The basic features of this blueprint are found in all classes of vertebrates.
Let's take an architectural and engineering approach to how one might arrive at this blueprint. First we will state the design problem—in hindsight, to be sure. Then we will consider the role of the axial structure with respect to the whole body. Then we will observe that the mechanism of compression resistance is in fact tension resistance in various fibrous, collagenous elements. And finally, we will take a sideways look at non-vertebrate axial supports as convergent systems.
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The design problem
In designing a motile machine such as a bicycle, a submarine or an automobile, you start with the load to be carried and the engine. Then you design a framework that supports the load in comfort and safety and the engine in such a fashion that its forceful motion is transferred to appendages and wheels to make frictional contact with the environment.
Animal design
Think about designing a motile machine using only hydrated, saturated, pliant polymeric materials—no metals or minerals—whose engine is a contractile polymer. This is a bizarre design assignment for most engineers, but it describes the first and all subsequent soft-bodied polyps and worms on Earth before they evolved calcareous and bony skeletal support materials. And, as Goodrich indicated, bone is a regional stiffening of the body's membranes associated with muscle attachment.
The contractile polymer actomyosin pulls on its ends when it contracts, so a pulling, tensile force must be housed in a pliant polymeric framework so that the machine can locomote by pushing against the ambient fluid or ground. The actomysion cannot re-extend itself and must be re-extended by being pulled out.
One solution to the problem of designing a force-reactive pliant chassis is to use straight-chain polymers as fibers and to make a two-dimensional array of them, a membrane, that is then formed into a cylinder. The cylinder can be filled with ambient water through a closable intake or it can be a permanently closed volume of liquid secreted by the machine. Thus we design a stiff or stiffenable body to support the tensile engine. We have a worm whose body wall is a collagenous membrane and whose engine is the muscle protein actomyosin.
If our designed worm's body is to move, the muscle must have an effective array in the body, and it requires fuel and a control system. Small, simple bodies have a gut for fuel intake and larger ones actually distribute food energy to muscle and all other tissues by a hydraulic circulatory system of cylindrical pipes and spaces. Control of muscle is effected by an electrically conductive nervous system and a chemical endocrine system whose elements are distributed by the circulatory system. The pipes, spaces and electrical systems must be appropriately supported in the space or in or on the polymeric wall. It becomes possible to design spaces within the basic cylinder in such a way that all functional units are served by one general design whose evolutionary modifications can support a gratifying diversity of machine types in different phyla that will be tested by natural selection.
To allow locomotor muscle to pull one way and then back again, it makes sense to put half on one side and half on the other, like a fish—or to put the halves on top and underneath, like a whale. Maximum bending moment is achieved for the body if the longitudinal muscle is attached as far as it can get from the body axis—to the body wall.
The structural feature that gave permission for the evolution of an axial support and that is the basic structural feature of all multicellular plants and animals on Earth is the cylindrical body form (Wainwright 1988). Here are useful functional aspects of cylindrical form:
- For organisms attached to the Earth such as cnidarian, ectoproct and endoproct polyps and colonies, and virtually all plants, cylindrical form allows them to outreach neighbors for food, sunlight, or air or water-borne gametes and pheromones.
- For soft-bodied, wormlike creatures, being long and thin and bi-tapered facilitates burrowing headfirst in sediments, algal turf, and leaf litter as well as through the tissues of any parasite's host.
- For animals that swim or fly, the cylindrical body is pre-adapted for moving head-first in fluids when they are small and, when they are big or fast enough, to take advantage of being streamlined.
- Cylindrical bodies and appendages can be stiffened by placing stiff materials peripherally, and flexibility can be permitted, localized, and oriented by a local directional decrease in radius.
Tapering the posterior end (streamlining), localizing rigid materials, and locally decreasing radius are indeed simple changes to be wrought through evolution, and they are at the basis of the distinguishing characteristics by which we classify animals and plants.
Bodies are not the only cylindrical elements to consider. As animals evolved appendages such as proboscides, antennae, horns, fins, podia, penes, legs, gills, and wings, these structures were fit to be used as levers from the start. Any leverlike function had to be supported by a compression-accommodating axis, and so it is with appendages throughout the Kingdom. So,
- Cylindrical elements are well suited to be levers that can confer mechanical advantage (force advantage or speed and displacement advantage) to motions. This can happen through leverage by rigid levers, or it can occur in pliant hydrostatic cylinders of constant volume (Kier and Smith, 1985).
Short, thick cylindrical parts, like vertebrae evolved before long, thin legs and perhaps before paired fins. Notochords are surrounded by longitudinal body musculature that originates and mostly inserts elsewhere, sometimes on skin and myosepta. The placement of even small rigid structures such as precursors of vertebral centra into the notochordal wall allows the origin or insertion of a tendon that can focus the force of a large muscle mass onto a point. This feature in turn permits the efficient powering of levers by large muscle masses.
It is interesting to note that the cylindrical form is rare in nonbiotic nature. Icicles, stalactites, stalagmites, lava tubes, and some crystals may be considered cylindrical, but the rest of the nonbiotic Universe has other shapes. Thus, cylindrical body form is a distinguishing characteristic of multicellular life on Earth. Perhaps we should consider this as we think about how any class of animals has come to support this shape by an internal axial structure.
The notochord is a hydrostatic support whose presence releases the body cavity and wall from the chore of resisting length changes. Mineralized tissues in the backbone can accept larger forces than the membranous notochordal sheath and can serve as sites of muscle attachment.
Our designed motile machine can now contract muscles behind the head on the right side from a signal from the CNS. The muscle pulls on tracts of collagen fibers in myosepta that in turn pull on skin. The skin's collagenous crossed-helical fiber array allows it to be stretched over the radially expanding, longitudinally contracting muscle, thus storing elastic energy to aid the return. The body bends and pushes against the water or sediment outside: locomotion happens. The system is designed by central nervous control and by the flexural stiffness of the body to propagate the bend backward along the body.
Role of the vertebrate axis
Both notochords and backbones resist longitudinal compressional change in length that would otherwise result from contraction of longitudinal locomotor muscle (Young, 1950). The accumulation of solid material in a thick notochordal sheath or a cartilaginous or bony vertebra provides an attachment site allowing a tendon to apply a point load from a large mass of muscle. In polyps, medusae, and worms, all longitudinal and circumferential muscles attach to the thin body wall over a wide area. This distributes their applied force and avoids the formation of kinks that would spoil locomotor shapes for swimming and burrowing.
The basic vertebrate body described above is a wormlike set of collagenous membranes whose massive axial muscles are contained in segmental membranous compartments. There is a continuum of myoseptal shapes from nearly transverse slabs to strongly folded cone-shaped structures in higher fishes. The membranous myosepta of these fishes have evolved regions of highly oriented collagen fibers that originate from wide distribution over the attached muscle and then converge to insert on rigid vertebrae (Westneat et al., 1993). In fishes there are tendons focusing enormous masses of longitudinal locomotor muscle on caudal and precaudal vertebrae.
Longitudinal axial musculature remains segmental in fishes, amphibia, and reptiles and then loses its myotomal nature in adult birds and mammals where it originates and inserts on segmental vertebrae but spans many IVJs. It seems like good design to have long muscles that span many segments: fewer parts to produce and to innervate and coordinate. When ancestors of the Cetacea returned to the water, they did not revert to fishlike myotomal muscle architecture. Yet they have an elastic subdermal sheath of collagen fibers in crossed helical array around the body that is strongly reminiscent of body walls of worms and the skin of fishes. Cetacean axial musculature is attached to this sheath, and it is constrained by the sheath to a range of diameters that allow it to use the forceful expansion of a contracting muscle to help drive longitudinal re-extension of the contralateral muscle.
In the evolution of vertebrates, long bodies with continuously flexible notochords and segmental muscles existed before the appearance of segmental vertebrae. With muscle already segmented, the appearance of vertebrae as solid blocks of relatively rigid material allows for the possibility, often realized, that all muscle of a segment might pull on a single tendon to a single, more posterior vertebra. One wonders what segmental muscles provide that continuous muscles cannot. Theoretical accounts assert that segmentation of muscles allows different parts of the body to do different things at the same time and that the propagation of waves of contraction can happen. However, locomotion of synaptid holothurians (Heffernan and Wainwright, 1974), tiny meiofaunal nematodes, and large burrowing nemerteans is also characterized by propagation of waves of muscle activity along the body. The segmental design in backbones provides for an efficient and timely transmission of muscle force of a myotome to bend one or more IVJs. It is interesting to note that in the tunas, highly specialized for fast continuous swimming, myoseptal extensions have evolved that transmit force from many myotomes through robust tendinous extensions to the caudle fin. Cetacean axial muscles originate segmentally on vertebrae but fuse to form long continuous muscles with long tendons that attach to a few posterior vertebrae (Pabst, 1990). Perhaps the advantage here lies in the long tendons of insertion of these long muscles: elastic energy storage in a tensile element is proportional to its length.
Design for tension
Buckminster Fuller (Marks, 1960) told us that tension is the associative force. This means that molecules and organisms are held together by the tensile nature of interatomic bonds. He also pointed out that in any complex structure at rest, tensile stresses must be balanced by compressive ones. He noted that carrying compressive loads over large distances demands more material, often denser materials, than to carry loads of the same magnitude in tension. He designed structures that maximized the use of tensile cables and reduced compressive elements to isolated rigid elements. He and Kenneth Snelson (Fox, 1981) gave the name ‘tensegrity’ to a support system of struts and ties wherein tension exists throughout the system and the compressive elements are minimal and do not touch one another—they are suspended in a web of tensile fibers.
Applying these ideas to the design of organismic bodies, we note that the supportive materials of plants and animals are based on fibrous macromolecules—cellulose in plants and collagen and chitin in animals. Joseph Needham (1936) observed that "Biology is largely the study of fibers." Arthropod exoskeleton is chitinous and the rest of us animals have collagen-based connective tissues, cartilage, and bone. From a lifetime spent with polarized light, I assert that wherever you find linear macromolecules in highly preferred or parallel orientation, you can rest assured that the structure functions in tension.
So, the basic biological structural element is the fiber. It is the least-materials way to transmit a force and it resists tension according to its diversity and structural array of atomic bonds and associated glycoproteins. Because of its high length to diameter ratio it has virtually no ability to resist compressive forces along its axis. However, if you weave many fibers into a membrane, it will resist compressive forces from one side by putting fibers into tension. Further, a fibrous membrane wrapped around a pressurized container can oppose compressive forces caused by the enclosed fluid. And the disparity between circumferential and longitudinal forces in the wall of a cylinder can be relieved by reinforcing the cylinder with helically wound tensile fibers (Wainwright et al., 1976).
Notochords are good examples of helically wound, pressurized cylinders. In general they are so long and thin that they are not very stiff in bending, but their axial compressive stiffness is adequate to keep them at constant length during locomotion.
What about backbones? They have rigid vertebrae alternating with less rigid but moderately deformable cartilage. In spite of their high length to diameter ratio, vertebral rigidity allows them to act as levers in body bending. Bony structure of vertebrae has been shown by Laerm (1976) and others to be designed to resist the forces caused by muscles. But the interesting thing is that axial compressive forces are accommodated in tension by collagen fibers in the fibrous layer of the intervertebral mechanism. The IVJ is essentially a thick membrane surrounding a central liquid-filled cavity pressurized by the action of longitudinal axial musculature and reinforced by highly oriented collagen fibers.
In some mammals that are good leapers such as cats and rabbits, vertebral extensions, the transverse processes, extend forward and overlap the IVJ. They are connected to the posterior end of the next anterior vertebral centrum by a substantial collagenous ligament. When the animal pushes off forcefully with its hind legs, the anterior body mass applies a large compressive force to the backbone. This compressive force is taken as tension in the collagenous wall of the IVJ and by the collagenous ligaments twixt transverse processes and centra.
Where zygapophyses overlap each other, they are connected by collagen fibers that contribute to the flexural stiffness of the backbone. In marlin and sailfish, anterior zygapopohyses overlap expanded neural and hemal spines of the next anterior vertebra. This overlap is tightly connected by collagen fibers that will be put into tension by axial compression of the backbone. The taking of compressive forces as tensile stresses by fields of tensile collagen is not a rare phenomenon in vertebrates. When you bite down and compress your molars, you do indeed compress the tooth, but where the tooth meets the jaw, dentin (bone) does not contact the jaw bone but is suspended from the jaw bone in a hammock of collagen fibers in tension.
Collagen also is a dominant component of cartilage. Mow and co-workers (1992) have analysed the accommodation to compressive forces of articular cartilage lining the acetabulum of the pelvis and covering the head of the femur in Homo sapiens. This multifaceted study concludes that even here the stresses in the cartilage are distributed such that the arched collagen fibers carry the compressive load in tension.
So the axial compressive function of notochords and backbones is really a story about tension in collagen fibers. Notochordal material was initially, and remains, tensile collagenous material. This design occurs in backbones in the IVJ and in other intervertebral ligaments.
Leverage
Backbones are long and thin at the scale of the organism just as vertebral processes such as neural and hemal spines, lateral processes and zygapohyses can also be relatively long and thin. Long and thin rigid elements make good levers that have high speed and displacement advantage. The tail sweep of a tuna, a newt, a crocodile, or a whale is the leverage act of the backbone pushing water with the expanded tail.
Along the backbone, muscles attach to the ends of vertebral processes and thus gain a larger input length and input moment on the vertebra than they would if they attached to the centra. Neural and hemal spines are short or absent in chondrichthians and can be quite long in actinopterygians. Lateral processes are short in fishes and are relatively longer in anurans, plesiosaurs, and jumping and swimming mammals. Vertebral processes are most fun in cetaceans and extinct swimming reptiles. In dolphins, neural and hemal spines and transverse processes are almost gracefully long and thin and greatly add to the bending moments created by axial musculature (Pabst, 1990).
Some vertebrates have greatly expanded surfaces on neural and hemal spines. Marlin, sailfish, beaked whales and large artiodactyls and the recently discovered bipedal predatory dinosaur Suchomimus tenenerensis have neural spines that have broad anterior-to-posterior surfaces (Sereno et al., 1998). Broad surfaces are a design feature associated with the attachment of muscle. Consider the scapula of all quadrupedal mammals: the head, neck, and thorax of these mammals is supported between the scapulas in a tensile sling of muscle and tendon. The mystery here is why backbones of so few species have such expanded surfaces for attachment of axial muscles.
Appendages
Our symposium specifies axes, implying body axes. It is important to realize that appendages also have longitudinal axes and that these axial supports follow the same mechanical permissions and limitations that body axes do. Everything from cuticular spines in worms of many phyla to antennae, maxillipeds, mandibles, penes, legs, podia, tentacles, trunks, wings, horns, and tails acts as some kind of lever and the principles alluded to above apply to their mechanical support. While these support systems also have nerve cords and circulatory vessels associated with them along their length, they are independent of the gut. Another symposium will surely be offered to treat this subject.
Invertebrate axial support
The first animal with an axial supportive structure situated between the gut and a dorsal hollow nerve chord arose, developed, and evolved from one without such a structure. Thus, the early vertebrates were worms with some axial support. Worm shape is such a good solution to many of life's problems in the physics of earth's surface—gravity and the viscous reaction to motion in air, water, and sediment—that it occurs in every phylum of animals, even the single-celled Protista. There are worm-shaped species in all invertebrate phyla and vertebrate classes except the Mammalia and I am prepared to imagine that cetaceans are still headed in that direction. Prediction: 60 million years from now there will be wormlike burrowing dolphins.
What about polyps and worms and molluscs and arthropods and echinoderms? They also have axially supported wormlike bodies. What is it like? And does it give us insight into the vertebrate axis?
At one extreme of near-vertebrateness, we are familiar with amphioxus, whose actual notochord, situated between the gut and the nerve chord, is a long, thin stack of vacuolated cells, like a stack of coins, wrapped in a fibrous collagenous sheath. In addition, each cell contains a swatch of paramyosin muscle filaments oriented from right to left side whose contraction causes the notochordal cross sectional shape to change from round to elliptical, the long axis of the ellipse being dorsoventral. This change in shape reduces the flexural stiffness of the notochord (Flood, 1969) as it varies during locomotion.
Urochordates abound in notochordal structures, all of which are cellular, hydrostatic structures.
Notochordal structures are found in isolated cases among invertebrate phyla. Consider Chordodasys (phylum Gastrotricha), a tiny worm, a tenth of a millimeter long, that lives among sand grains in the beach. It has a post-anal tail about a quarter the length of its body that ends in two stiff appendages with sticky ends. The sticky organs allow the animal to attach to a sand grain when the wave-driven water flow is tending to wash it downstream. The tail has a notochord whose anterior end lies just dorsal to the gut. The notochord is a stack of cells containing paramyosin muscle reminiscent of the situation in amphioxus.
The turbellarian Nematoplana (phylum Platyhelminthes) is also tiny and lives in the beach. A cord of cells runs the length of the body from head to tail in the dorsal side of the gut. The cells are large and highly vacuolated. I am unaware of any information about how the animal moves and behaves, but I wonder if this column of cells is not also functionally a notochord.
Perhaps it is pushing the limits of even my roving eye, but the cirrus of a barnacle strikes me as a segmented cylindrical support structure designed for bending in the oral direction, much like my own backbone. The cirrus is a series of 20 to 30 stiff segments continuous with flexible arthrodial membranes. True, all this structure is exoskeletal, produced by epidermis and does not originate in conjunction with either gut or central nervous system, but it is certainly convergent structurally and functionally with backbones.
The arms of ophiuroids and crinoids (phylum Echinodermata) are supported by calcitic ossicles reminiscent of vertebral centra. They are connected in series by muscle and by ligaments made of a unique collagenous connective tissue characteristic of echinoderms. These supportive systems are endoskeletal but do not develop in conjunction with guts or nerve cords. They converge functionally and structurally at a superficial level with backbones.
The Cnidaria exhibit the greatest diversity of fundamentally different axial support systems of all the phyla. Among them is an interesting convergence with backbones. This is the sea fan Melithaea ochracea whose axis is made up of rigid, polycrystalline calcitic sclerites organized into bulging flexible "knees" alternating in series with slender, rigid "shins." Sclerites in the rigid parts are 10 µm long and about 1 µm diameter. They are tightly packed and oriented parallel to each other and they show a preferred orientation parallel to the axis of the colony or its branch. They are cemented together with more, rigid CaC03. If I were designing a rigid cylindrical structure and I had bricks that were ten times longer than wide and a brick-like glue, I would arrange them overlapping and parallel and apply the rigid glue just as Melithaea does. In the flexible parts of the axis, the sclerites are 5 µm long and 1 µm diameter. They are set in an open, apparently random 3-dimensional, array and stuck together with a pliant polymeric material. Triangular and tetrahedronal arrays are exceedingly rare: we infer this structure to be designed to be flexible (Muzik and Wainwright, 1977).
The solid collagenous axial skeletons of alcyonarian corals are striking, often very long, thin supports representing a wide array of designs including the specialized distribution of polycrystalline calcified material. By having multiple axes in a single colony they are pre-adapted to form a series of long thin stems (Ellisella), or bushy clusters of feathery stems (Pseudopterogorgia), or stems anastamosed into planar fans (Gorgonia). The Alcyonaria could be the basis of study of the widest variety of axial support materials and systems of any plant or animal group. They make the structural diversity of vertebrate axial systems seem very narrowly focused indeed.
So backbones as segmented cylindrical structures with alternating stiff and pliant segments are not unique to the vertebrates. The design has been used in other phyla and in some plants (e.g., the calcareous marine Green alga Halimeda and the prickly pear cactus Opuntia). What vertebrates have invented is making such an axial supportive structure between the gut and the dorsal nerve cord. One can't help but wonder whether there is any continuity in genetic instructions to make the notochords of Chordodasys, Nematoplana, amphioxus, lampreys, hagfish, and the plants. Are convergent structures genetically related? I imagine that they might be but that there need not be any genetic connection twixt convergent organizations.
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What is offered here is an acknowledgment of the vision of E. S. Goodrich, a lifetime ago, on the importance of connective tissue in the structure and function of the vertebrate axis and its surrounding body. Thinking in terms of mechanical design leads us to appreciate the compression-resisting structures that tensile collagen fibers get themselves into in animal bodies. The design process, that is much used in art, architecture, and engineering, can generate hypotheses and promote understanding when used in scientific analysis and synthesis.
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FOOTNOTES |
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1 From the Symposium on The Function and Evolution of the Vertebrate Axis presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 6–10 January 1999, at Denver, Colorado.
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References |
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Wainwright, S.A. 1988. Axis and circumference.. Harvard University Press, Cambridge, Massachusetts.
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Westneat, M.W., Wm Hoese, C.A. Pell, and S.A. Wainwright. 1993. The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes. J. Morph., 217:183-204.[CrossRef]
Young, J.Z. 1950. The life of vertebrates.. Oxford University Press, London.
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