© 2000 by The Society for Integrative and Comparative Biology
To Bend a Dolphin: Convergence of Force Transmission Designs in Cetaceans and Scombrid Fishes1
1 Biological Sciences and Center for Marine Science Research, University of North Carolina at Wilmington, Wilmington, North Carolina 28403
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SYNOPSIS |
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 SYNOPSIS INTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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The similarity in swimming style and external body shape between dolphins and scombrid fishes, especially tunas, is a textbook example of evolutionary convergence. I identify additional morphological features of the musculoskeletal system shared by dolphins and tunas. Specifically, these swimmers share a pattern of force transmission through a complex, three-dimensional system of collagenous fabrics, which are stiffened by muscular hydrostatic pressure. This force transmission system increases both the displacement advantage and moment arm of contracting axial muscle. These features represent a functionally significant design for steady swimming vertebrates.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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Most fish swim by laterally undulating or oscillating their body and propulsive caudal fin. Axial muscles, arranged in complexly folded myomeres, transmit contractile forces via the connective tissue "fabrics" of myosepta, horizontal and vertical septa, and skin (e.g., Kishinouye, 1923
; Kafuku, 1950; Fierstine and Walters, 1968; Wainwright et al., 1978; Wainwright, 1983; Westneat et al., 1993; Long et al., 1996). These forces do work against a variably flexible beam, the vertebral column, to affect swimming movements (e.g., Hebrank, 1982; Hebrank et al., 1990; Long, 1992).
Cetaceans (whales, dolphins and porpoises) are derived aquatic mammals that locomote by dorsoventral oscillation of their caudal tailstock and propulsive caudal flukes (e.g., Slijper, 1936, Parry 1949; Fish and Hui, 1991). Axial muscles, arranged in longitudinal tracts (Slijper, 1936; Smith, et al., 1976; Strickler, 1980), transmit forces via connective tissue "fabrics" of aponeurotic tendon sheets, subdermal connective tissue sheath (SDS), horizontal septa, and skin (Pabst, 1990, 1993, 1996a). Transmitted muscular forces do work against the variably flexible vertebral column to affect swimming movements (Long et al., 1997).
The striking similarities of body shape and swimming behavior observed in cetaceans and one group of teleost fishes, the tunas, is a textbook example of convergent evolution (i.e., the independent evolution of homoplastic characters) (e.g., Howell, 1930; Hildebrand, 1974, Walker and Liem, 1994; Fish, 1996). These similarities include a highly streamlined shape with a relatively deep mid-body and narrow necking of the caudal tailstock or peduncle; a high aspect ratio, lunate caudal fin that provides lift-based thrust; and an oscillatory "thunniform" swimming style (Lighthill, 1969; Webb, 1982, 1984; Fish, 1993a; Vogel, 1994; Pabst, 1996a). Each feature increases propulsive efficiency in these steady-swimming vertebrates by increasing either swimming speed or thrust efficiency, and by decreasing body drag (reviewed in Webb, 1982).
Convergence provides a way to identify characters that have "important functional significance" from those that do not (Vogel, 1998). That is, convergence is a powerful tool for identifying morphological designs (sensu Lauder, 1982), and for identifying potential causal reasons for evolutionary change (Lauder, 1990). Thus, the similarities in external body shape of cetaceans and tunas can be interpreted as functionally significant designs that decrease the energetic costs of locomotion.
To date, those characters identified as convergent between cetaceans and tunas have predominantly been external features. In this paper, I compare the pattern of force transmission through the bodies of cetaceans and tunas, and identify the following convergent features of the musculoskeletal system.
- Connections between axial muscles and peripheral, helically wound, connective tissue membranes that function to increase locomotor muscle performance.
- A pattern of caudal intervertebral joint flexibility that controls caudal tailstock/peduncle movement.
- Long, terminal tendons that function to control the angle of attack of the propulsive caudal fin/flukes.
- A peripheral connective tissue membrane in the region of the caudal tailstock/peduncle, which is thickened and reinforced with steeply angled connective tissue fibers, that functions as a retinaculum.
I propose that these convergent features are "functionally significant design features" (Lauder, 1982; Vogel, 1998) of steady swimming vertebrates. I begin by briefly reviewing the evolution of vertebrate axial muscles to establish the differences in their organization in actinopterygian fishes and tetrapod mammals. I will then discuss each of the convergent characters listed above.
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EVOLUTION OF VERTEBRATE AXIAL MUSCLES: FROM MYOMERES TO LONGITUDINAL TRACTS OF MUSCLE |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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The evolution of axial muscles involved changes in morphology, activation pattern, and function as vertebrates made the transition from axially-powered swimming to appendicularly-powered, terrestrial locomotion.
Most fish swim using myomeric axial muscles that are organized into a series of discrete, complexly folded units, separated by connective tissue membranes called myosepta (Fig. 1a). Myomeres and myosepta are connected directly to the dermis of the skin, as well as to the vertebral column (reviewed in Wainwright, 1983; Westneat et al., 1993). The function of the myomeres is to produce lateral bending of the axial skeleton. During steady swimming, the pattern of muscle activity is both unilateral and uniphasic—at any point along the body, muscles on only one side of the animal are active at a time, and there is only one bout of muscle activity per side, per locomotor cycle (definitions from Ritter, 1995).
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Most amphibians (anamniotic tetrapods) hatch as aquatic, swimming larvae, then metamorphose into terrestrial forms (e.g., Walker and Liem, 1994
). In salamanders, both swimming and ambulatory locomotion involves lateral body bending (e.g., Carrier, 1993, Frolich and Biewener, 1992). In neotenic and metamorphosed adult salamanders, swimming is powered by unilateral and uniphasic contractions of both the myomeric epaxial, and predominantly myomeric hypaxial muscles (Fig. 1b) (Carrier, 1993, Frolich and Biewener, 1992). During walking, the epaxial muscles function to produce lateral bending (Frolich and Biewener, 1992), but there is a new pattern of firing and a new function attributed to the hypaxial muscles. Some hypaxial muscles fire bilaterally and uniphasically, suggesting that they function to stabilize the trunk against ground reaction forces experienced during appendicular locomotion (Carrier, 1993), although the hypaxials probably also contribute to lateral body bending (as suggested by Ritter, 1995). As in fishes, the epaxial muscles are connected to the dermis (Frolich and Schmid, 1991; Frolich and Biewener, 1992).
In amniotes, both the morphology and the function of the epaxial muscles have changed relative to anamniotes. The hypothesized basal condition for amniotes, as represented by lizards, is to have epaxial muscles organized into three longitudinal tracts, the transversospinalis, longissimus and iliocostalis (Fig. 1c) (Walker and Liem, 1994). Within each of these three tracts, muscle fascicles retain a serial arrangement, reminiscent of the myomeric pattern of fishes and lower tetrapods. The new function of the epaxials is not to produce lateral undulations of the axis, but rather to stabilize the longitudinal axis against ground reaction forces experienced during appendicular locomotion (Ritter, 1995). Although the epaxials take on a new postural function, their firing pattern remains unilateral and uniphasic. Concomitant with this change in function, most epaxial muscles also lose their connection to the skin. The hypaxial muscles appear to function both to produce lateral undulations (Ritter, 1996) and to stabilize the trunk (Carrier, 1990).
In most mammals, the appendages are aligned vertically beneath the body, and the trunk undergoes little or no lateral bending during locomotion (Hildebrand, 1974). During walking, the epaxial muscles, organized into longitudinal tracts, function to stabilize the vertebral column. This postural function relies upon bilateral and biphasic muscle activity (English, 1980), a derived character state for vertebrates (Ritter, 1995). In galloping, the epaxial and hypaxial muscles function to produce dorsoventral bending of the vertebral column, and muscles fire bilaterally and uniphasically (English, 1980).
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AXIAL LOCOMOTOR MUSCLES WRAPPED BY A HELICALLY-REINFORCED, CONNECTIVE TISSUE MEMBRANE |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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Almost all fish possess a dermis that is reinforced by multiple layers of helically wound collagen fibers (e.g., Motta, 1977
; Wainwright et al., 1978; Hebrank, 1980; Hebrank and Hebrank, 1986; Long et al., 1996). The helical reinforcement permits the skin to bend smoothly without wrinkling, and offers resistance to both torsional and internal pressure loads (Wainwright et al., 1978). The skin also controls passive body stiffness, and, thus, whole body undulatory mechanics (e.g., Long et al., 1994; Long et al., 1996), and may function as a spring in parallel with the swimming muscles in some species (e.g., sharks, Wainwright et al., 1978). Because the skin is attached to the underlying myomeric axial musculature and to the axial skeleton, it can function to transmit locomotor forces along the fish body (Wainwright, 1983), as has been demonstrated in sharks (Wainwright et al., 1978), eels (Hebrank, 1980), and gars (Long et al., 1996).
The skin of scombrid fishes, including tunas, is reinforced with helically wound collagen fibers (Hebrank and Hebrank, 1986) connected to both myomeres and axial skeleton, and involved with transmitting locomotor forces along the body (Westneat et al., 1993).
The axial muscles of cetaceans are also wrapped by a helically wound connective tissue membrane, the subdermal connective tissue sheath (SDS) (Pabst, 1990). The multiple, interwoven layers of obliquely oriented collagen fibers that form the SDS come from many sources, including axial and abdominal muscles, and blubber, their specialized hypodermis (Pabst, 1990). The SDS is piece-wise homologous to the mammalian thoraco-lumbar fascia—that is, some of the connective tissues fibers that form these membranes are from homologous sources, such as abdominal muscles. The SDS, though, also has unique contributions, such as from the blubber (reviewed in Pabst, 1996a). The SDS is connected to axial muscles, tendons and the vertebral column, and transmits locomotor forces, as described below (Pabst, 1990, 1996a).
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MORPHOLOGY OF AXIAL MUSCLES AND PATTERN OF FORCE TRANSMISSION THROUGH PERIPHERAL CONNECTIVE TISSUE MEMBRANES |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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Westneat et al. (1993)
have hypothesized a functional model for the transmission of locomotor forces in scombrid fishes. They suggest that collagen fibers within myosepta, horizontal septa, and skin transmit muscle forces to the axial skeleton and caudal fin, and that this three dimensional system of tensile elements is stiffened by hydrostatic pressure produced by radially bulging, contracting myomeres.
The myoseptum of each complexly folded myomere is reinforced by two populations of collagen fibers—one wrapped circumferentially, the other longitudinally (Fig. 2). Both populations of fibers coalesce in the main horizontal septum (the connective tissue structure that lies along the lateral mid-line and that connects the skin to the vertebral centra) to form obliquely oriented tendons. The circumferential fibers form anterior oblique tendons (AOTs), the longitudinal fibers form posteriorly oblique tendons (POTs). Thus, the main horizontal septum is reinforced with a crossed fiber array of AOTs and POTs (Westneat et al., 1993).
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The contractile force of each myomere is transmitted caudally by its POT. Each POT, at the lateral margin of the main horizontal septum, becomes woven with fibers of an AOT, forming a pulley, or sling apparatus (schematically illustrated in Fig. 3a; see Figs. 5–7 in Westneat et al., 1993
, for photographs of these tendons). This sling apparatus functions to keep the turning fibers of the POT far lateral to the neutral axis of bending. The POT then continues caudally and inserts on "downstream" vertebral centra. In tunas (represented by the little tunny, Euthynnus alletteratus, and big-eye, Thunnus obesus), the POTs travel at a lower angle, and traverse a greater number of vertebrae, than in other scombrid fishes. The sling apparatus, which can be modeled as a lever system, confers two mechanical attributes to the pattern of muscular force transmission. (1) The velocity ratio (output motion/input motion) of a myomere, and, thus, the lateral displacement of its insertional tendon, is increased. Tunas have a larger displacement advantage than do other scombrids. (2) The mechanical advantage of a myomere's lateral pulling force is increased because the sling apparatus acts as a "jib" that increases the force's moment arm. That is, it increases the perpendicular distance from the application of force to the neutral axis. This jib function requires that the AOT, and other collagenous septa, are under tension. Westneat et al. (1993) geometrically model myomeres as constant volume cones and demonstrate that physiologically realistic muscle shortening will create radial bulging (based upon muscular hydrostatic models of Kier and Smith, 1985; Smith and Kier, 1989). Thus, hydrostatic pressure, provided by contracting myomeres, puts the entire force transmission system under tension. In tunas, there is also extensive branching of the POTs at their insertions, which Westneat et al. (1993) suggest may "diffuse muscular forces" over many intervertebral joints.
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In contrast to fish myomeres, the axial locomotor muscles of dolphins are organized into longitudinal tracts as is typical of mammals (reviewed in Pabst, 1990
). The intramuscular morphology and tendon geometry of the epaxial (upstroke) muscles have been investigated in common (Delphinus delphis) and bottlenose (Tursiops truncatus) dolphins (Pabst, 1993). I will focus this description on the longissimus, the largest epaxial muscle, and the one that does most mechanical work on the vertebral column during swimming.
The longissimus muscle, and its caudal extension, the extensor caudae lateralis, run virtually the entire length of the dolphin (Pabst, 1990) (Fig. 4a). Muscle fascicles originate off the skull, the transverse processes and neural arches of vertebrae, and off two connective tissues—the deep surface of the SDS, and the ventral surface of the deep tendon. Muscle fibers insert primarily via the superficial tendon, an aponeurotic sheet composed of many long, flat tendons (Fig. 4b). Each tendon fiber runs caudally from the body of the longissimus towards the dorsal midline. Just lateral to the midline, the tendon fibers split into smaller fibers, and the paths of these fibers diverge.
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A small number of these tendons insert onto the neural spines of thoracic and lumbar vertebrae, an insertion pattern common to terrestrial mammals. The vast majority of these tendons, though, do not share this pattern of insertion, but instead become woven into, and form part of, the helically wound SDS. These tendon fibers either cross the dorsal midline and run at approximately 45° through the SDS towards the vertebral transverse processes on the contralateral side of the dolphin, or turn laterally away from the dorsal midline as they enter the SDS and run at approximately 45° through the SDS towards the ipsilateral vertebral transverse processes (Fig. 4b). Thus, the large forces developed by the longissimus in the thoracic and cranial lumbar spine are transmitted to the vertebrae in the caudal tailstock. To the best of my knowledge, this tendon insertional pattern represents a unique morphological construct for cetaceans, mammals that lack connections between epaxial muscles and pelves. It is also functionally analogous to the sling mechanism of scombrid fishes (see Fig. 3b).
Pabst (1993) identified three mechanical consequences of the interactions between the superficial tendon and the SDS. (1) The displacement advantage, or tendon excursion, of the longissimus is increased. The mechanical work potential of the muscle is 30–60% larger than if the tendons inserted on the neural spines. (2) The mechanical advantage of the longissimus's dorsal pulling force is increased because the superficial tendon-SDS complex acts as a jib that increases the force's moment arm. Pabst (1996a) hypothesized that the SDS is tensed when it experiences hydrostatic pressure loading by the action of contracting, radially bulging axial muscles (Kier and Smith, 1985; Smith and Kier, 1989). (3) The longissimus distributes its force evenly along the vertebral column, and because the tendon fibers run on both sides of the vertebral column at angles close to 45°, they confer torsional stability to the caudal tailstock.
The insertional pattern of the dolphin longissimus, and hence, the path of force transmission through the dolphin, is convergent upon that of scombrid fishes. In both clades, interactions between locomotor tendon fibers and a peripheral, hydrostatically supported connective tissue membrane increases the displacement advantage and moment arm of contracting muscle. Because this pattern of force transmission increases the performance of locomotor muscle, I hypothesize that it is a functionally significant design (sensu Lauder, 1982 and Vogel, 1998) of steady swimming vertebrates.
Interestingly, dolphins and scombrid fishes do not share similar axial muscle morphologies. Although the design of the collagenous force transmitting structures are convergent, the morphology of the force generating axial muscle (i.e., metameric vs. longitudinal tracts) does not appear to be a functionally significant design.
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CAUDAL VERTEBRAL MECHANICS |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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During swimming, both tunas and dolphins restrict bending to the caudal one third to one quarter of the body (e.g., Fierstine and Walters, 1968
; Fish, 1993b; Pabst, 1993). The mechanical properties of the vertebral column, in part, will control the range and pattern of body bending permitted in these swimmers (reviewed in Long et al., 1997).
Although Hebrank (1982) demonstrated that the vertebral column of skipjack tuna was stiffer than that of spot (Leiostomus xanthurus), there exist no comparable quantitative data on regional variation in vertebral mechanics in tunas. Fierstine and Walters (1968) qualitatively observed that the stiffest regions of the axial skeleton are the (1) caudal peduncle (just cranial to the caudal fin), and (2) the caudal abdominal through the cranial-most caudal vertebrae. The regions of greatest flexibility are just cranial to the peduncle, and at the insertion of the caudal fin (e.g., the joint at the caudal fin is a highly mobile synovial joint, rather than a typical intervertebral joint). Thus, the peduncular vertebrae form a rigid bar, interposed between two relatively flexible joints. The caudal abdominals and cranial most caudals form a rigid base upon which the peduncle is anchored. The stiff peduncle, in turn, functions as a rigid base for the flexible insertion of the caudal fin.
Regional patterns of vertebral flexibility in common dolphin (Long et al., 1997) are similar to those described for tunas. Intervertebral joint stiffness is highest at the (1) lumbo-caudal joint, the base of the caudal tailstock and (2) the caudal 20/21 joint, just cranial to the insertion of the caudal flukes. The intervening caudal spine is more flexible, and the prefluke/fluke joint (caudal 21/22) has negligible stiffness. Thus, the lumbo-caudal region appears to function as a rigid base of support for the muscles that act on the caudal tailstock. Caudal vertebrae 20 and 21 appear to function as a base for the highly flexible insertion of the caudal flukes.
Thus, tunas and dolphins possess convergent patterns of caudal vertebral flexibility. The serial arrangement of a stiff tail base, intervening flexible spine, stiff caudal fin base, and compliant joint at the caudal fin insertion, appears to be a functionally significant design that controls the pattern of body bending in steady swimming vertebrates. Dynamic bending tests on tuna vertebral columns would be valuable to test this hypothesis.
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LONG TENDONS THAT CONTROL ANGLE OF ATTACK OF CAUDAL FIN |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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In scombrid fishes, the five to six caudal most myosepta form two sets of long, terminal tendons (Fierstine and Walters, 1968
; Westneat et al., 1993). The great lateral tendon (GLT), which inserts on the caudal fin, is formed by the longitudinally oriented collagen fibers of the myosepta of anterior pointing cones. The GLT is probably homologous to POTs (Westneat et al., 1993). Likewise, the medial caudal tendon (MCT), which also inserts on the caudal fin, is formed by the longitudinally oriented collagen fibers of the myosepta of posterior pointing cones. The tendons transmit muscular force across the compliant joint at the base of the caudal fin and aid in controlling its angle of attack. Long, terminal, myoseptal-tendons are an apparently derived character for scombrids (Katz and Jordon, 1997).
In dolphins, the caudal extension of the longissimus, the extensor caudae lateralis, inserts onto the dorsal surfaces of the caudal-most vertebrae in the flukes, by way of seven long, terminal tendons that are serially homologous to the superficial tendons (Pabst, 1990). The extensor caudal lateralis is the only epaxial muscle to insert on fluke vertebrae, and aids in controlling the flukes' angle of attack.
Thus, tunas and dolphins have converged upon a pattern of long terminal tendons that insert upon the propulsive caudal fin/flukes. This tendon morphology permits forces, which are generated by large cross-sectional areas of more cranially-placed muscle, to be transmitted and focussed through the narrow-necked caudal peduncle—a functionally significant design feature of steady swimming vertebrates recognized as an adaptation to reduce drag. I suggest that a force transmission system designed to traverse such a constraining body feature is an equally significant functional design. Long tendons may also provide both tunas and dolphins with a spring, in-series with their locomotor muscles, that may reduce the energetic costs of swimming (reviewed in Pabst, 1996b).
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REINFORCEMENT OF THE PERIPHERAL BODY AS A RETINACULUM |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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Long tendons have a tendency to "bowstring"—that is, to lift away from the joints when they are pulled on by their muscles and when joints bend. A retinaculum is a connective tissue band, reinforced with fibers at high angles (often perpendicular to) the direction of the tendon, that prevents tendon bowstringing. Pabst (1996a)
hypothesized that the body walls of vertebrate swimmers with narrow-necked caudal tailstocks would have to be reinforced against tendon bowstringing. That is, they would have to possess skins, or circumferentially placed connective tissue structures reinforced with fibers at steep angles. Fierstine and Walters (1968) also hypothesized that the skin of scombrids functioned as a "flexor retinaculum."
Tunas possess two systems of fiber reinforcement that appear to function as retinacula. The skin of the caudal peduncle is wrapped by dermal fibers at very steep fiber angles (Hebrank and Hebrank, 1986). (Interestingly, this pattern of caudal dermal fiber reinforcement is not seen in fishes that lack terminal tendons, such as spot [Hebrank and Hebrank 1986] and eel [Hebrank 1980]). Deep to the dermis, the tuna peduncle is also reinforced with a thick subdermal sheath, formed by myoseptal collagen fibers of caudal posterior pointing arms (Westneat et al., 1993). In dolphins, the SDS surrounding the caudal tailstock is also reinforced with connective tissue fibers at steep angles (Pabst, 1996a). Thus, fiber reinforcement of the peripheral body as a retinaculum, shared by both tunas and dolphins, appears to be a functionally significant design feature of steady swimming vertebrates.
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ACKNOWLEDGMENTS |
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Thanks to Steve Wainwright, Bill McLellan, John Long, John Gosline, Sharon Babcock, Steve Katz, Margo Lillie, Mark Westneat, Chuck Pell and Butch Rommel for their time and thoughts on force transmission. This work was supported by the Office of Naval Research. CMSR Contribution Number 232.
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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.
2 E-mail: pabsta{at}uncwil.edu
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References |
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SYNOPSISINTRODUCTIONEVOLUTION OF VERTEBRATE AXIAL...AXIAL LOCOMOTOR MUSCLES WRAPPED...MORPHOLOGY OF AXIAL MUSCLES...CAUDAL VERTEBRAL MECHANICSLONG TENDONS THAT CONTROL...REINFORCEMENT OF THE PERIPHERAL...References |
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