High-speed swimming. Enhanced power in yellowfin tuna.
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Animals↗
Biomedical subjects
R E Shadwick
Publications and source records attributed to R E Shadwick.
Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas.
Elasmobranchs and bony fishes have evolved independently for more than 400 million years. However, two Recent groups, the lamnid sharks (Family Lamnidae) and tunas (Family Scombridae), display remarkable similarities in features related to swimming performance. Traits separating these two groups from other fishes include a higher degree of body streamlining, a shift in the position of the aerobic, red, locomotor muscle that powers sustained swimming to a more anterior location in the body and nearer to the vertebral column, the capacity to conserve metabolic heat (i.e. regional endothermy), an increased gill surface area with a decreased blood-water barrier thickness, a higher maximum blood oxygen carrying capacity, and greater muscle aerobic and anaerobic enzyme activities at in vivo temperatures. The suite of morphological, physiological, and biochemical specializations that define "high-performance fishes" have been extensively characterized in the tunas. This review examines the convergent features of lamnid sharks and tunas in order to gain insight into the extent that comparable environmental selection pressures have led to the independent origin of similar suites of functional characteristics in these two distinctly different taxa. We propose that, despite differences between teleost and elasmobranch fishes, lamnid sharks and tunas have evolved morphological and physiological specializations that enhance their swimming performance relative to other sharks and most other high performance pelagic fishes.
Adaptation, Biological↗
The dynamics and scaling of force production during the tail-flip escape response of the California spiny lobster Panulirus interruptus.
The tail-flip escape behavior is a stereotypical motor pattern of decapod crustaceans in which swift adduction of the tail to the thorax causes the animal to rotate, move vertically into the water column and accelerate rapidly backwards. Previous predictions that a strong jet force is produced during the flip as the tail adducts to the body are not supported by our simultaneous measurements of force production (using a transducer) and the kinematics (using high-speed video) of tail-flipping by the California spiny lobster Panulirus interruptus. Maximum force production occurred when the tail was positioned approximately normal to the body. Resultant force values dropped to approximately 15% of maximum during the last third of the flip and continued to decline as the tail closed against the body. In addition, maximum acceleration of the body of free-swimming animals occurs when the tail is positioned approximately normal to the body, and acceleration declines steadily to negative values as the tail continues to close. Thus, the tail appears to act largely as a paddle. Full flexion of the tail to the body probably increases the gliding distance by reducing drag and possibly by enhancing fluid circulation around the body. Morphological measurements indicate that Panulirus interruptus grows isometrically. However, measurements of tail-flip force production for individuals with a body mass (Mb) ranging from 69 to 412 g indicate that translational force scales as Mb0.83. This result suggests that force production scales at a rate greater than that predicted by the isometric scaling of muscle cross-sectional area (Mb2/3), which supports previously published data showing that the maximum accelerations of the tail and body of free-swimming animals are size-independent. Torque (tau) scaled as Mb1.29, which is similar to the hypothesized scaling relationship of Mb4/3. Given that tau is proportional to Mb1.29, one would predict rotational acceleration of the body (alpha) to decrease with increasing size as Mb(-0.37), which agrees with previously published kinematic data showing a decrease in alpha with increased Mb.
Analysis of Variance↗
Dynamic mechanical characterization of a mutable collagenous tissue: response of sea cucumber dermis to cell lysis and dermal extracts.
The dermis of the holothurian Cucumaria frondosa is a mutable collagenous tissue (MCT). In this study, the inner and outer regions of the dermis were separated and used to make two different tissue extracts. These extracts were applied to intact pieces of dermis, one invoking a stiff mechanical state and the other invoking a compliant state. The extracts were effective on tissues incubated in artificial sea water (ASW) and in those incubated in Ca(2+)-chelated ASW. Furthermore, the extracts were effective on both fresh tissues and tissues in which the cells had been lysed by freeze-thawing, indicating that the sites of action are in the extracellular matrix. Dynamic oscillatory shear tests and analyses were used to measure both the dynamic shear stiffness (G*) and the relative damping (tan delta ) of the tissue. These two parameters proved to be inversely related to each other (i.e. when G* increased, tan delta decreased). A theoretical viscoelastic model is constructed to interpret the results of these tests. It is concluded that changes in the mechanical state of the tissue involve interactions between elastic elements within the tissue rather than an alteration of its viscous components.
Animals↗
Mechanical design in arteries.
The most important mechanical property of the artery wall is its non-linear elasticity. Over the last century, this has been well-documented in vessels in many animals, from humans to lobsters. Arteries must be distensible to provide capacitance and pulse-smoothing in the circulation, but they must also be stable to inflation over a range of pressure. These mechanical requirements are met by strain-dependent increases in the elastic modulus of the vascular wall, manifest by a J-shaped stress-strain curve, as typically exhibited by other soft biological tissues. All vertebrates and invertebrates with closed circulatory systems have arteries with this non-linear behaviour, but specific tissue properties vary to give correct function for the physiological pressure range of each species. In all cases, the non-linear elasticity is a product of the parallel arrangement of rubbery and stiff connective tissue elements in the artery wall, and differences in composition and tissue architecture can account for the observed variations in mechanical properties. This phenomenon is most pronounced in large whales, in which very high compliance in the aortic arch and exceptionally low compliance in the descending aorta occur, and is correlated with specific modifications in the arterial structure.
Animals↗
Heart rate and stroke volume contribution to cardiac output in swimming yellowfin tuna: response to exercise and temperature.
Cardiac performance in the yellowfin tuna (Thunnus albacares, 673-2470 g, 33-53 cm fork length, FL) was examined in unanesthetized fish swimming in a large water tunnel. Yellowfin tuna were fitted with either electrocardiogram electrodes or a transcutaneous Doppler blood-flow probe over the ventral aorta and exposed to changes in swimming velocity (range 0.8-2.9 FLs-1) or to an acute change in temperature (18-28 degrees C). Heart rates (fH) at +/-1 degree C (30-130 beats min-1) were lower on average than previous measurements with non-swimming (restrained) tunas and comparable with those for other active teleosts at similar relative swimming velocities. Although highly variable among individuals, fH increased with velocity (U, in FLs-1) in all fish (fH = 17.93U + 49.93, r2 = 0.14, P < 0.0001). Heart rate was rapidly and strongly affected by temperature (Q10 = 2.37). Blood flow measurements revealed a mean increase in relative cardiac output of 13.6 +/- 3.0% with exercise (mean velocities 1.23-2.10 FLs-1) caused by an 18.8 +/- 5.4% increase in fH and a 3.9 +/- 2.3% decrease in stroke volume. These results indicate that, unlike most other fishes, cardiac output in yellowfin tuna is regulated primarily through increases in fH. Acute reductions in ambient temperature at slow swimming velocities resulted in decreases in cardiac output (Q10 = 1.52) and fH (Q10 = 2.16), but increases in stroke volume (Q10 = 0.78). This observation suggests that the lack of an increase in stroke volume during exercise is not due to the tuna heart operating at maximal anatomical limits.
Animals↗
Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna Thunnus albacares.
Yellowfin tuna Thunnus albacares (1400-2175 g) instrumented with electrocardiogram electrodes and pre- and post-branchial catheters were subjected to incremental swimming velocity tests. Increasing velocity, from a minimal speed of 1.0 FLs-1, where FL is fork length, resulted in a 1.4-fold increase in heart rate (from 61.4 to 84.6 beats min-1), an elevated ventral-aortic blood pressure (from 10.8 to 12.2 kPa) and a decreased systemic vascular resistance. Relative branchial vascular resistance at minimal speed ranged from 24.4 to 40.0% of total vascular resistance and tended to increase with velocity. Yellowfin blood has a high oxygen-carrying capacity (16-18 ml O2 dl-1), and a low in vivo oxygen affinity (P50 = 5.3 kPa). Exercise caused a rise in arterial saturation (from 74 to 88%) and a decline in venous saturation (from 48 to 44%), resulting in a 1.3-fold increase in tissue oxygen extraction from the blood (arterial-venous oxygen content difference). Whereas arterial oxygen partial pressure (PO2) tended to increase with exercise, venous PO2 remained unchanged (approximately 5.3 kPa). The observed decrease in venous oxygen content was brought about by a lowered blood pH (from 7.80 to 7.76) and a large Bohr shift. Cardiac output and the increased blood oxygen extraction are estimated to have contributed nearly equally to the increased oxygen consumption during exercise. The large venous oxygen reserve still available to yellowfin tuna at maximal prolonged velocities suggests that the maximal oxygen delivery potential of the cardiovascular system in this species is not fully utilized during aerobic swimming. This reserve may serve other aerobic metabolic processes in addition to continuous swimming.
Animals↗
The mechanical properties of fin whale arteries are explained by novel connective tissue designs.
The aortic arch and the descending aorta in the fin whale (Balaenoptera physalus) are structurally and mechanically very different from comparable vessels in other mammals. Although the external diameter of the whale's descending thoracic aorta (approximately 12 cm) is similar to that predicted by scaling relationships for terrestrial mammals, the wall thickness:diameter ratio in the whale (0.015) is much smaller than the characteristic value for other mammals (0.05). In addition, the elastic modulus of the thoracic aorta (12 MPa at 13 kPa blood pressure) is about 30 times higher than in other mammals. In contrast, the whale's aortic arch has a wall thickness/diameter ratio (0.055) and an elastic modulus (0.4 MPa) that are essentially identical to those for other mammals. However, the aortic arch is unusual in that it can be deformed biaxially to very large strains without entering a region of high stiffness caused by the recruitment of fully extended collagen fibres. Chemical composition studies indicate that the elastin:collagen ratio is high in the aortic arch (approximately 2:1) and that this ratio falls in the thoracic (approximately 1:2) and abdominal (approximately 1:3) aortas, but the magnitude of the change in composition does not account for the dramatic difference in mechanical properties. This suggests that there are differences in the elastin and collagen fibre architecture of these vessels. The descending aorta contains dense bands of tendon-like, wavy collagen fibres that run in the plane of the arterial wall, forming a fibre-lattice that runs in parallel to the elastin lamellae and reinforces the wall, making it very stiff. The aortic arch contains a very different collagen fibre-lattice in which fibres appear to have a component of orientation that runs through the thickness of the artery wall. This suggests that the collagen fibres may be arranged in series with elastin-containing elements, a difference in tissue architecture that could account for both the lower stiffness and the extreme extensibility of the whale's aortic arch. Thus, both the structure and the mechanical behaviour of the lamellar units in the aortic arch and aorta of the whale have presumably been modified to produce the unusual mechanical and haemodynamic properties of the whale circulation.
Animals↗
Arterial Windkessels in marine mammals.
In marine mammals, the aortic arch is enlarged relative to the descending aorta to varying degrees in different species. The ratio of maximal diameter of the arch to that of the thoracic aorta is about 2.3 in the harbour seal (Phoca vitulina), 3.6 in the Weddell seal (Leptonychotes weddelli) and 3.2 in the fin whale (Balaenoptera physalus), compared with only 1.4 in the dog. This anatomical specialisation probably provides increased volume capacitance in the arterial circulation as an adaptation to diving bradycardia. Data on the morphometric and mechanical properties of aortic tissues from seals and fin whale are compared. In the harbour seal, more than 80% of the volume change in the entire thoracic aorta that results from a pressure pulse occurs in the bulbous arch, and this is more than 90% in the Weddell seal and fin whale. The enhanced capacitance of the arch in the harbour seal is primarily due to its larger diameter, as the relative wall thickness and elasticity of the arch and thoracic aorta are the same. A similar situation appears to exist in the larger Weddell seal, although extrapolation of the pressure-volume curves suggests that the arch might be somewhat less stiff than the thoracic aorta. In addition to being greatly expanded, the aortic arch of the fin whale is also much more distensible than the relatively thin-walled and much stiffer descending aorta. At the estimated mean blood pressure, the elastic modulus of this vessel is 12 MPa, or 30 times that of the aortic arch. The major haemodynamic consequence of this type of arterial modification is that the aortic arch acts as a Windkessel, i.e. the capacitance of the aorta is increased significantly close to the heart, leading to a reduced characteristic impedance and probably reduced pulsatility in the descending aorta. In the extreme case of the whale, the arterial capacitance is shifted entirely to the arch, and the impedance change at the entrance to the thoracic aorta is so high that this probably represents the major reflection site in the arterial tree.
Adaptation, Physiological↗
Relationship between body mass and biomechanical properties of limb tendons in adult mammals.
We investigated the allometric relationship between the mechanical properties of various limb tendons and body mass. The elastic modulus (i.e., stiffness) and hysteresis (i.e., energy dissipation) of digital flexor, ankle extensor, and digital extensor tendons from 18 species of adult quadrupedal mammals ranging in body mass from 0.5 to 545 kg were determined by cyclic tensile testing in vitro. The results show that these elastic properties do not vary significantly among tendons from animals of different body mass, nor do they differ between the digital flexor and ankle extensor tendons (those situated to act as springs during locomotion) and the digital extensor tendons (those not likely to function as springs during locomotion). Consequently, the inherent capability of different limb tendons to store elastic energy, based on their material properties, is the same for large and small animals. The relationship between tendon elastic modulus (E; in GPa) and body mass (Mb; in kg) is described by the allometric equation E = 1.22Mb0.00. The hysteresis (H), as a percentage of total strain energy, is related to body mass as H = 8.89Mb-0.03.
Animals↗
Allometry of muscle, tendon, and elastic energy storage capacity in mammals.
This paper considers the structural properties of muscle-tendon units in the hindlimbs of mammals as a function of body mass. Morphometric analysis of the ankle extensors, digital flexors, and digital extensors from 35 quadrupedal species, ranging in body mass from 0.04 to 545 kg, was carried out. Tendon dimensions scale nearly isometrically, as does muscle mass. The negative allometry of muscle fiber length results in positive allometric scaling of muscle cross-sectional areas in all but digital extensors. Maximum muscle forces are predicted to increase allometrically, with mass exponents as high as 0.91 in the plantaris, but nearly isometrically (0.69) in the digital extensors. Thus the maximum amount of stress a tendon may experience in vivo, as indicated by the ratio of muscle and tendon cross-sectional areas, increases with body mass in digital flexors and ankle extensors. Consequently, the capacity for elastic energy storage scales with positive allometry in these tendons but is isometric in the digital extensors, which probably do not function as springs in normal locomotion. These results suggest that the springlike tendons of large mammals can potentially store more elastic strain energy than those of smaller mammals because their disproportionately stronger muscles can impose higher tendon stresses.
Animals↗
Arterial mechanics in the fin whale suggest a unique hemodynamic design.
An analysis of the dimensions of the aortic tree and the mechanical properties of arterial wall tissues in the fin whale (Balaenoptera physalus) is presented. The aortic arch is greatly expanded, having an internal radius at an estimated mean blood pressure (13 kPa) that is 2.5 times greater than that of the descending thoracic aorta. At this pressure, the elastic modulus of the arch wall (0.4 MPa) is 30 times less than that of the descending aorta (12 MPa). Consequently, even though some capacitance is provided anteriorly by the relatively compliant innominate and carotid arteries, > 90% of the arterial capacitance resides in the arch. The characteristic pressure wave velocity (C0) and impedance (Z0) were calculated from vessel dimensions and elasticity. A predicted 20-fold increase in Z0 between the arch and thoracic aorta should provide a major reflecting site, effectively uncoupling the arch from the remainder of the arterial tree. The dimensions of the arch relative to the likely pressure wavelengths within it suggest that it acts like a compliant windkessel that greatly reduces the pulsatility of the inflow to the descending aorta, which itself likely acts as a rigid, tapered manifold. It is suggested that the presence of both a highly compliant arch and a relatively rigid descending aorta is an adaptation for diving.
Animals↗
The structure and mechanical design of rhinoceros dermal armour.
The collagenous dermis of the white rhinoceros forms a thick, protective armour that is highly specialized in its structure and material properties compared with other mammalian skin. Rhinoceros skin is three times thicker than predicted allometrically, and it contains a dense and highly ordered three-dimensional array of relatively straight and highly crosslinked collagen fibres. The skin of the back and flanks exhibits a steep stress-strain curve with very little 'toe' region, a high elastic modulus (240 MPa), a high tensile strength (30 MPa), a low breaking strain (0.24) and high breaking energy (3 MJm-3) and work of fracture (78 kJm-2). By comparison, the belly skin is somewhat less stiff, weaker, and more extensible. In compression, rhinoceros skin withstands average stresses and strains of 170 MPa and 0.7, respectively, before yielding. As a biological material, rhinoceros dorsolateral skin has properties that are intermediate between those of 'normal' mammalian skin and tendons. This study shows that the dermal armour of the rhinoceros is very well adapted to resist blows from the horns of conspecifics, as might occur during aggressive behaviour, due to specialized material properties as well as its great thickness.
Aggression↗
Functional importance of a highly elastic ligament on the mammalian diaphragm.
The diaphragm of mammals is a musculotendinous dome separating the thoracic and abdominal cavities. With no skeletal elements to stretch it, the diaphragm has the problem of positioning its muscle fibres at a length appropriate for the onset of an inspiratory contraction. This is achieved through a negative intrapleural pressure, resulting from the opposing elastic recoil of the ribcage and lungs, which sucks the diaphragm into the thorax and extends the muscle fibres. A consequence of this negative pressure is that the diaphragm muscle is under tension when inactive during expiration. This is an unusual condition for skeletal muscles, which can suffer irreversible changes when stretched to long length, or they may respond by growing longer. We now describe a highly elastic and resilient diaphragmatic ligament which sets a sarcomere length enabling the muscle to use its full operating range, reduces stress on the diaphragm muscle fibres, and assists shortening of the diaphragm muscle at the onset of inspiration by means of elastic recoil.
Animals↗
Elastic energy storage in tendons: mechanical differences related to function and age.
We investigated the possibility that tendons that normally experience relatively high stresses and function as springs during locomotion, such as digital flexors, might develop different mechanical properties from those that experience only relatively low stresses, such as digital extensors. At birth the digital flexor and extensor tendons of pigs have identical mechanical properties, exhibiting higher extensibility and mechanical hysteresis and lower elastic modulus, tensile strength, and elastic energy storage capability than adult tendons. With growth and aging these tendons become much stronger, stiffer, less extensible, and more resilient than at birth. Furthermore, these alterations in elastic properties occur to a significantly greater degree in the high-load-bearing flexors than in the low-stress extensors. At maturity the pig digital flexor tendons have twice the tensile strength and elastic modulus but only half the strain energy dissipation of the corresponding extensor tendons. A morphometric analysis of the digital muscles provides an estimate of maximal in vivo tendon stresses and suggests that the muscle-tendon unit of the digital flexor is designed to function as an elastic energy storage element whereas that of the digital extensor is not. Thus the differences in material properties between mature flexor and extensor tendons are correlated with their physiological functions, i.e., the flexor is much better suited to act as an effective biological spring than is the extensor.
Age Factors↗
Functional similarities in the mechanical design of the aorta in lower vertebrates and mammals.
The mechanical properties of the aorta from the toad Bufo marinus, the lizard Gekko gecko and the garter snake Thamnophis radix were compared to those of the rat, by inflation of vessel segments in vitro. The arteries of the lower vertebrates, like those of mammals, were compliant, highly resilient, and non-linearly elastic. The elastic modulus of the artery wall was similar in the lower vertebrates and mammals, at their respective mean physiological pressures. We conclude that the aorta in each of these animals is suitably designed to function effectively as an elastic pulse smoothing component in the circulation; differences in the pressure wave transmission characteristics of lower vertebrates and mammals do not result from dissimilarities in arterial elastic properties, but from substantial differences in heart rate of these two groups.
Animals↗
Elastic arteries in invertebrates: mechanics of the octopus aorta.
The aorta of the octopus, Octopus dofleini, is a highly distensible, elastic tube. The circumferential elastic modulus increases with inflation in the physiological range from abut 10(4) to 10(5) newtons per square meter. Rubber-like fibers have been isolated, apparently for the first time, from the aorta of an invertebrate. These fibers have an elastic modulus, like elastin, of about 4 x 10(5) newtons per square meter and are present in sufficient quantity to account for the elastic properties of the intact vessel under physiological conditions. Thus the circulatory system of an invertebrate animal provides an "elastic reservoir" (much like that of the vertebrate system), which increases the efficiency of the circulation.
Animals↗