Locomotor Patterns in the Evolution of Actinopterygian Fishes'

Transcription

1 AMER. ZOOL., 22: (1982) Locomotor Patterns in the Evolution of Actinopterygian Fishes' PAUL W. WEBB The University of Michigan, School of Natural Resources, Ann Arbor, Michigan and National Marine Fisheries Service, Southwest Fisheries Center, Lajolla, California SYNOPSIS. Locomotor adaptations in actinopterygian fishes are described for (a) caudal propulsion, used in cruising and sprint swimming, acceleration, and fast turns and (b) median and paired fin propulsion used for slow swimming and in precise maneuver. Caudal swimming is subdivided into steady (time independent) and unsteady (time dependent acceleration and turning) locomotion. High power caudal propulsion is the major theme in actinopterygian swimming morphology because of its role in predator evasion and food capture. Non-caudal slow swimming appears to be secondary and is not exploited before the Acanthopterygii. Optimal morphological requirements for unsteady swimming are (a) large caudal fin and general body area, (b) deep caudal peduncle, often enhanced by posterior dorsal and anal fins, (c) an anterior stabilizing body mass and/or added mass, (d) flexible body and (e) large ratio of muscle mass to body mass. Optimal morphological requirements for steady swimming are (a) high aspect ratio caudalfin, (b) narrow caudal peduncle, (c) small total caudal area, (d) anterior stabilizing body mass and added mass, and (e) a stiff body. Small changes in morphology can have large effects on performance. Exclusive morphological requirements for steady versus unsteady swimming are partially overcome using collapsible fins, but compromises remain necessary. Morphologies favoring unsteady performance are a recurring theme in actinopterygian evolution. Successive radiations at chondrostean, halecostome and teleostean levels are associated with modifications in the axial and caudal skeleton. Strength of ossified structures probably limited maximum propulsion forces early in actinopterygian evolution, so that specializations for fast cruising (carangiform and thunmform modes) followed structural advances especially in the caudal skeleton. No such limits apply to eel-like forms which consequently recur in successive actinopterygian radiations. Slow swimming using mainly non-caudal propulsion probably first occurred among neopterygians in association with reduced and neutral buoyancy. Slow swimming adaptations can add to and extend the scope of caudal swimming, but specialization is associated with reduced caudal swimming performance. Marked exploitation of slow swimming opportunities does not occur prior to the anterodorsal location of pectoral and pelvic girdles and the vertical rotation of the base of the pectoral fin, as found in the Acanthopterygii. INTRODUCTION Changes in skeletal elements provide the At some stage in their lives, all fish swim, major basis for assessing phylogeny. The and water is a dense, viscous medium that major actinopterygian trends relevant to places a premium on effective propulsion locomotor mechanics and swimming permechanisms. Among fishes, the actinop- formance are as follows (Greenwood el ai, terygians show greatest diversity of pro- 1966; Patterson, 1968a, b; Gosline, 1980; pulsive mechanisms that involve the body Rosen, 1982). and caudal fin, dorsal and anal fins, and... c r u i. c /r> i inor-s n (a) progressive ossification ot the axial paired fins (Breder, 1926), as well as spe- K. i cializations for benthic life where swim-... S,? e n ' r,, i» -i.,,.,..., (b) abbreviation or the heterocercal tail to ming may be great y reduced (Marshall, ',,, -, attain an external homoceral tail. ' (c) emphasis of caudal ray support on a few hypural bones (modified hemal arches)...,. (d) reduction in the number of vertebrae 1 From the Symposium on Evolutionary Morphology,,, of the ActinopteigiL Fishes presented at the AnnJal Supporting the hypural bones. Meeung of the American Society of Zoologists, 27- (e) reduction in the number ot vertebrae. 30 December 1980, at Seattle, Washington. (f) reduction in scale mass and armor, ex- 329

2 330 PAUL W. WEBB cept for their secondary reappearance in some modern teleosts. (g) dorsal migration of the pectoral girdle and pectoral fin insertion, (h) forward migration of the pelvic girdle, anus and origin of the anal fin. The question to be addressed here is how these phylogenetic trends are related to the major trends in external body form that determining how water is moved in generating thrust, and how efficiently that thrust is generated. The major trends in body form pertinent to locomotor mechanics are: (a) a recurring fusiform carnivore-type with a large tail and caudal area. This generalized form is dominant in primitive groups. (b) recurring radiation from the generalized form towards elongate and benthic forms. (c) progressive specialization of forms with forked tails and a narrow caudal peduncle. (d) appearance of specialized deep-bodied forms with dominant non-caudal propulsors. Most of these interrelationships cannot be experimentally tested because they frequently involve extinct animals. Therefore, the usual methods of considering functional-morphology in an evolutionary context are employed. It is assumed that similar structures or suites of characters are functionally similar. These functions can be determined by experiment on living fish, fleshed out in most cases by the known laws of physics. Where a change in structure or suites of structures is observed through time, then functional hypotheses for the changes can be formulated. These functional hypotheses will evolve as data accumulate, and also as the phylogenetic reference framework evolves. This is because phylogenies are also hypotheses of relationship among animals (Atz et al., 1980) that not only cannot be experimentally verified or rejected, but which also evolve as data accrue and opinions change. Also, the limited meager knowledge on fish locomotion mechanisms must be recognized. To a large extent research has concentrated on body/caudal fin locomotion, particularly steady (constant speed) swimming. Many fish rarely swim. Fish rarely swim steadily (Nursall, 1958; Mc- Cutcheon, 1976). They frequently use non-caudal fins. Indeed, research may have concentrated on biologically and behaviorally less important swimming modes! In spite of the inevitable constraints, a general, and necessarily preliminary, analysis of locomotor patterns in actinopterygian phylogeny seems possible.. These patterns can be discussed under two categories; (a) caudal propulsion adaptations mainly involved in fast-swimming, high acceleration and fast turns and (b) non-caudal adaptations used mainly in slow swimming and precise maneuver. A major theme throughout actinopterygian evolution is a trend towards high power caudal swimming (Gosline, 1971); slow swimming is not exploited in any great degree prior to the percoid level of organization among the higher teleosts. The two patterns will be discussed separatedly in relation to phylogenic trends in actinopterygians. CAUDAL PROPULSION Occurrence Body and caudal fin propulsion appears to be a common denominator throughout the evolution of fish. This propulsion system has been retained in all groups, with the exception of some specialized benthic fish. The conservatism in caudal swimming probably occurs because it is mechanically most efficient (compare Wu, 1971; Wu and Newman, 1972; Webb, 1971, 1975a, c; Blake, 1980a, b, c) and it is the mechanism for achieving maximum acceleration rates, maximum turning couples and high sprint speeds. Most research has been performed in this area (see Lighthill, 1975; Wu et al., 1975; Pedley, 1977; Hoar and Randall, 1978; Sharp and Dizon, 1979). A recurring morphology in actinopterygian fishes is the fusiform, generalized carnivore, with a large caudal fin and caudal area and a deep caudal peduncle, e.g., the chondrostean Cheirolepis, early haleco-

3 ACTINOPTERYGIAN LOCOMOTION 331 PALEOZOIC ACTINOPTERYGIANS "LOWER" TELEOSTS (c) (D) "HIGHER TELEOSTS (E) (?) Gasteropetecus Pyntocepholus Xiphistor Conaroqadus Fic. 1. A diagrammatic representation of some of the typical body and fin forms seen at various times in selected radiations in actinopterygian fishes. Three general "grades" are illustrated. These show functional varieties about a recurring generalized carnivore form (Cheiroiepis, Salmo, Serranus) and are not intended to show phylogenetic lines. A, C, and E show variations among elongate and fusiform forms. Examples of body form along the anguilliform to thunniform continuum are illustrated; Anguilla is the type for the anguilliform mode and Thunnus for the thunniform mode. B, D and F show radiations towards deep-bodied non-caudal forms usually specializing in slow swimming. More specialized forms are shown above less specialized forms. stome Parasemionotus, halecomorph Lepidotus, lower teleosteans Hiodon, Engraulis, Salmo, etc. and higher teleosteans Mugil, Perca, Serranus, Micropterus, etc. Some examples are illustrated in Figure 1. Regular radiations have occurred towards more elongate forms at each level of actinopterygian organization. Radiation towards specialized short-bodied forms, with forked tails and a narrow caudal peduncle are relatively rare before the acanthopterygians, although there is a greater tendency in this direction in more recent groups. The recurrence of the generalized body forms raises several questions: What is its functional significance? What underlies replacement of similar forms in successive actinopterygian radiations? Why do elongate forms recur but not short streamlined forms? These questions can be approached using arguments based on recent studies on the locomotor mechanics of modern teleosts. A major emphasis of this research has been problems of thrust generation and resistance to motion (drag) that must equal that thrust. Theories concerning thrust have considered potential (inviscid) flow around a swimming fish, but outside the boundary which is a major source of drag. Because of this distinction, it is desirable to consider separately the mechanics of thrust and drag, and the functionalmorphological correlates for each. In addition, distinction must be made between steady swimming (time independent motion at cruising and sprint speeds) and unsteady swimming (time dependent motion involving linear and angular acceleration). This is because the theory treating thrust mechanics (see Weihs, 1972, 1973; Lighthill 1975, 1977; Wu, 1977; Wu and Yates, 1979) and experimental studies (Webb, 1977a, 1978; Webb and Smith, 1980) show that morphological requirements for maximum performance in steady and in unsteady swimming not only differ, but optimal designs are mutually exclusive. Therefore, the following discussion treats first thrust and then drag, and in each case, mechanics and functional-morphology related to steady and to unsteady swimming are considered.

4 332 PAUL W. WEBB X A (I) Steady Swimming (Lighthill 1971 ) -.--L...,. (2) Unsteady Swimming ( Weihs 1973) F--& mwnda-e L tangent at Q FIG. 2. Notation and summary of thrust forces acting on a fish during steady and unsteady swimming as predicted from hydromechanical theory. The figure shows the hypothetical outline of a swimming fish seen from above (dotted lines) with the body axis shown as a solid line. For analytical purposes, the body is divided into "propulsive segments" along the whole length, 1. One such segment is shown at a, following the usual convention of measurement from the trailing edge. This segment moves laterally and forward with resultant velocity V (a,t> resolved into a normal component, W (a, t) and tangential component, U (a. t). Each segment influences a mass of water in its vicinity, the added mass, m. In steady swimming (equation 1), the instantaneous force acting on the body depends on the sum of contributions from all propulsive segments both anterior to the trailing edge (the integral term) and at the trailing edge (terms in parentheses). In unsteady swimming (equation 2), the instantaneous force depends on the sum of contributions of propulsive segments anterior to the trailing edge (the integral term) plus a lift force, L), due to discrete fins i to k. Further discussion is given in the text. In both cases, n is the coordinate normal to the fish centerline, and s the tangential coordinate. The figure is based on equations 1 and 3 and figure 1 in Weihs (1973). Thrust. Hydromechanical theories concerning the generation of thrust by fish swimming motions have been widely discussed (see Weihs, 1973; Lighthill, 1975; Wu, 1977; Webb, 1978). Space does not permit a detailed development of these concepts. Instead, main principles are summarized, and to facilitate reading, formal mathematical descriptions are limited to key equations summarized in Figure 2. Steady swimming. During optimally efficient steady swimming, the body is bent into a propulsive wave which passes backwards over the body at a velocity near to, but of necessity greater than the swimming speed. Any point along the body (a propulsive "segment" sensu Gray, 1968) oscillates laterally relative to the head. The amplitude of these lateral oscillations increases along the body length to reach maximum values of approximately 0.2L (L = body length) at the tip of the caudal fin (the trailing edge). The depth of the caudal fin should be large to maximize the mass of water affected (the added mass) which is proportional to the square of the depth of the body and/or fins. The force acting on a steadily swimming fish at any instant due to the effect of these body movements on the water in the vicinity of the fish is formally described by equation 1 in Figure 2. The mechanism whereby thrust is generated can be visualized by considering that all the propulsive segments along the body interact in series to gradually accelerate water in the vicinity of the fish. The water reaches a maximum velocity just as it is discharged into the wake at the trailing edge. The total work done depends on the momentum gain of this water, but the thrust component is less than this because of the loss of energy involved in the acceleration of the water. Thus the instantaneous force acting on the body is the sum of the forces of the segments anterior to the trailing edge (the integral term in equation 1) plus that due to the momentum discharged across the trailing edge. However, because of interaction between segments, those anterior to the trailing edge have little effect on the

5 ACTINOPTERYGIAN LOCOMOTION 333 mean force (i.e., the integral term has a zero mean value). The mean force is given by the rate of change of water momentum discharged into the wake across a plane at the trailing edge (the terms in parentheses). Mean thrust is the difference between the total energy discharged to the wake and the kinetic energy associated with the increased water velocity (i.e., the difference between the two terms in parentheses in equation 1). There is a wide range of morphologies associated with steady swimming in bodycaudal fin modes, originally classified by Breder (1926). In mechanical terms (Lighthill, 1975), various locomotor types fall along a continuum ranging from eel-like fish to mackerel-like fish (anguilliform modes to carangiform modes of Breder). The range is associated with larger specific wavelength (propulsive wavelength/l), a more rapid rise in amplitude posteriorly, larger caudal fin depth but smaller tail area (high aspect ratio tail), reduced caudal peduncle depth (narrow necking) and more streamlined body (see Fig. IE). Larger specific wavelengths and caudal concentration of increases in amplitude both reduce the time available for secondary viscous-related growth in the added water mass which contributes to energy losses (Lighthill, 1975). The trends towards narrow necking of the caudal peduncle and a large body and fin depth over the center of mass reduce the magnitude of rapidly fluctuating side forces that can increase lateral recoil (the tail "wagging the head") which also increases energy loss (Lighthill, 1977). The increased depth of the trailing edge increases the added mass of water accelerated in each tail beat, increasing thrust (Lighthill, 1975) or efficiency (Alexander, 1968). These kinematic features presumably result in higher swimming speeds and/or higher efficiency at a given speed as the carangiform mode is approached. The anguilliform to carangiform continuum includes all non-lunate tail swimmers. A further mode is the mechanically distinct thunniform mode (Lindsey, 1978), represented by the tunas (family Thunnidae) among the actinopterygians. Thunniform swimmers have the most advanced adaptations for improved thrust and locomotor efficiency (see Lighthill, 1975, 1977; Hoar and Randall, 1978; Wu and Yates, 1979) such that the slender body theory applied along the anguilliform to carangiform continuum is no longer applicable. Instead, separate hydromechanical theories are being developed that take into account the unique morphology and kinematics associated with the half-moon (lunate) tail. Unsteady swimming. Unsteady swimming (accelerations such as fast-starts and turns) involves large amplitude lateral movements of the tail, with trailing edge amplitudes commonly greater than 0.5L (Webb, 1978). Movements are non-periodic, and involve little more than two beats of the tail. The same general principles of steady swimming apply to unsteady swimming (Weihs, 1972, 1973) and forces acting on the body at any instant are formalized by equation 2 (Fig. 2). Unsteady swimming differs from steady swimming in that there is no significant temporal or spatial interaction between propulsive segments. As a result, the trailing edge is of no particular importance, so that this term of the steady swimming model disappears. Instead, both instantaneous and mean forces in turning and acceleration depend on the sum of contributions from all propulsive segments (the integral term of equation 2) plus any lift forces due to fins and body sections with sharp edges (second term in equation 2). Fast-start kinematics show little variability over a wide range of body forms (Gray, 1933; Hertel, 1966; Weihs, 1972, 1973; Webb, 1975*, 1976, 1978; Eaton et al, 1977; Eaton and Bombardieri, 1978; Wardie, 1975), and those differences observed do not affect acceleration rates (Weihs, 1972, 1973; Webb, 1976). As a result, the major variable affecting thrust is the distribution of depth (and hence added mass) along the body length (see the integral term in equation 2). Thrust due to each propulsive segment, and hence total thrust, is maximized when the body depth

6 334 PAUL W. WEBB is large along the whole length of the fish, resulting in a large body and fin area (Weihs, 1972, 1973; Webb, 1977a). However, because amplitudes of propulsive movements are greatest caudally, the greatest contributions to thrust are made by the area distant from the center of mass, the locus about which the forces act (Weihs, 1972). The large amplitude motions by large fins not only generate thrust forces in the direction of motion, but also substantial side forces. Those forces may be particularly large early in a turn or a fast-start because then thrust forces tend to be poorly aligned with the body axis (Weihs, 1972, 1973). As a result, a large couple acts on the center of mass causing it to yaw (lateral recoil) in proportion to the acceleration rate (Weihs, 1973). The recoil, plus body bending, is useful in a turn, but represents wasted energy in a fast-start. Recoil energy losses can be reduced by large body and fin depth over the center of mass, as in steady swimming. Such morphology would also reduce side-slip in unpowered turns. Drag The equation of drag for rectilinear motion of a body at constant depth in water is: where D M, D = M,a + V 2 psu 2 (kc D ) (3) drag = thrust, total mass of the body and water resisting acceleration, a = acceleration rate, p = density of water, S = wetted surface area, U = swimming speed, (kc D ) = drag coefficient, where k is a factor taking into account additions to the drag coefficient C D of a rigid body due to body shape and/or lateral body motions (Lighthill, 1975; Webb, 1975a; Bone, 1977; Alexander, 1979). In equation 3, the first resistance term is that due to inertia and the second is that due to friction. The magnitude of these two components differs between steady and unsteady swimming. In steady swimming, a is small and periodic or zero and therefore frictional drag dominates. In unsteady swimming, a is often very large relative to U and mass resistance dominates. These differences in the major components have distinct consequences for functional design. Steady swimming. The question of the drag on a steadily swimming fish is a topic of continuing debate. It now seems generally agreed that frictional drag is dominant, with little increment from pressure drag due to body shape. Frictional drag is determined by the nature of the boundary layer and is greater for turbulent boundary layer flow than for laminar boundary layer flow. Irrespective of the actual boundary layer flow conditions, swimming movements change the velocity gradients across the boundary layer compared to those on a geometrically similar non-flexing body. As a result, frictional drag will also be higher. There are several reasons for this higher drag. First, the lateral motion of the body and fins increases the incident velocity on propulsive segments above the mean swimming speed. Second, the mean velocity gradient and hence drag coefficient will also be increased because of boundary layer thinning (Lighthill, 1971) as there is insufficient time for the boundary layer to reach the thickness that would be expected on a steadily moving non-flexing body. The increased incident velocity of propulsive segments might increase drag by a factor of about 1.5. Boundary layer thinning probably increases the local drag coefficient by 5 to 10 times (Lighthill, 1971; Webb, 1973a). The mean drag of a flexing fish appears to be about 2 to 5 times greater than that of an equivalent nonflexing body (Alexander, 1967; Lighthill, 1975; Webb, 1973a, 1975a). The drag increment due to locomotor movements will be largest where the amplitude of propulsion movements is greatest. Therefore drag can be minimized by (1) holding the body rigid, permitting good anterior stream-lining, and concentrating large amplitude movements posteriorly, (2) minimizing body and fin area anterior to the trailing edge where lateral amplitudes are large; i.e., narrow necking

7 ACTINOPTERYGIAN LOCOMOTION 335 (Lighthill, 1977), (3) scooping out the center of the caudal fin reducing the area (Lighthill, 1975). The trend from anguilliform to thunniform modes is therefore not only a trend towards greater power and swimming efficiency, but also one towards reduced drag by reduction of unwanted area over the flexing portion of the body and by streamlining the more rigid anterior portion (Walters, 1962; Fierstine and Walters, 1968). Unsteady swimming. In a fast-start, the acceleration rate is large, with maximum values of the order of 4-5 G and mean values of 1-2 G (Webb, 1976, 1978). Speed increases through a fast-start and can reach values of nvsec" 1 in 50 to 150 milliseconds, but during that period the boundary layer will have to grow, and C D may be small. Conservative theoretical calculations (Webb, 1975a, 1978) and experimental studies (Webb, 1982) show that the frictional drag term is a small percentage of total drag during such periods of rapid acceleration. Thus, drag in a fast-start is dominated by the mass of the system, and the large area required for effective thrust generation adds little cost to drag. Drag reducing mechanisms for acceleration involve a reduction of non-essential mass. Reductions in non-muscle tissue density reduce the dead weight to be accelerated relative to the mass of the muscle motor. The resultant improved ratio of power-to-load represents the resistance reduction. All density saving adaptations, usually attributed to neutral buoyancy, will also contribute to improved acceleration; Webb and Skadsen (1979) describe mass reductions in the skin that appear to be related specifically to reducing acceleration resistance. Drag will be increased, probably substantially, by large body and fin area during accelerations and turns by fish that are already in motion. Compromises in functional morphology of caudal propulsion The hydrodynamic principles outlined above lead to exclusive optimum morphologies for steady and unsteady swimming. The optimum morphology for steady swimming is a large aspect ratio tail, narrow caudal peduncle and rigid streamlined body to maximize thrust and minimize drag. For unsteady swimming, the body should be flexible, with a large depth along its whole length, with emphasis on a large caudal area. Ray-finned fishes are unique in being able to modify body and fin area by means of their erectile/collapsible fins, and therefore actinopterygians have some capability to adjust body and fin shapes according to the competing demands of steady and unsteady propulsion. Nevertheless, this ability to compromise is not perfect as increased caudal fin depth usually results in little improvement of steady swimming, but does improve acceleration and turning performance (Webb, 1977a; Webb and Smith, 1980; Webb and Keyes, 1981). The early evolutionary appearance of large caudal area, often enhanced by a posterior location of dorsal and anal fins, and the regular recurrence of this morphology at each actinopterygian grade must therefore be interpreted as design favoring unsteady swimming (Lauder, 1980; Webb and Smith, 1980). This was probably due to the importance of faststarts and turns in avoiding predators and in catching elusive prey (Hoogland et al., 1956; Nursall, 1973; Neill and Cullen, 1974; Eaton and Bombardieri, 1978; Webb and Skadsen, 1980). All fish face predation at some time in their lives so that unsteady swimming performance is likely to be important for survival to reproduction. The recurring generalist form (fusiform body with large caudal area) during actinopterygian evolution thus appears to be the most effective compromise for caudal propulsion providing adequate steady swimming performance (Beamish, 1978) and good unsteady performance (Webb, 1978). Magnitude of effects of morphological variation on swimming performance and power It is important to consider the locomotor impact of variations in body and fin morphology. Hydromechanical theory (Lighthill, 1975; Weihs, 1972, 1973) and exper-

8 336 PAUL W. WEBB imental observations (Webb, 1977a) have clearly shown that relatively large increments in fast-start performance accrue with relatively small increases in body and fin depth, especially when that area is located caudally. Equivalent experimental observations have not been made for steady swimming. However, Hunter and Zweifel (1971) have measured tail beat frequencies and amplitudes for six teleosts from which some idea of the importance of body form can be deduced. The morphological variation among the species studied was not large (Fig. 3) and was towards the center of the larger anguilliform to thunniform range. Hunter and Zweifel showed that for fish of a given size, tail beat frequencies at a given speed varied among the six species up to 30 to 40%. Since tail beat amplitudes were constant (20% of length) the differences in tail beat frequency imply substantial variation in thrust, and hence drag, over the narrow range of morphologies studied. While it is apparent that external morphology alone will not dictate swimming performance, it is clear from Figure 3 that small variations in morphology can have large effects on locomotor mechanics and performance. Observations on a wide range of morphologies from gars to cetaceans suggest that more anguilliform swimmers have relatively higher tail beat frequencies than thunniform swimmers (Kayan et ai, 1978). These observations tend to support the arguments of increasing thrust efficiency and reduced drag associated with more thunniform morphologies. Therefore, small morphological changes are expected to be significant for both steady and unsteady swimming. Structural and functional patterns in actinopterygian evolution The importance of retaining good unsteady swimming performance and adequate steady swimming performance, characteristic of the recurring actinopterygian "generalist" form does not explain the succession of superficially similar external morphologies replacing each other throughout actinopterygian evolution. The succession from chondrosteans, through various halecostome and neopterygian levels to the teleosts shows remarkably little improvement in caudal propulsion morphology (at least before acanthopterygians). The major structural patterns involve internal anatomical changes, particularly in ossification of the axial skeleton and organization of the caudal skeleton which transmit thrust forces to the body (see Greenwood et al., 1966; Romer, 1966; Shaeffer, 1967; Patterson, 1968a, b; Lauder, 1980). The earliest chondrosteans, such as the paleonisciforms had a large heterocercal caudal fin. The caudal peduncle was deep, and dorsal and anal fins were inserted towards the tail {e.g., Cheirolepis in Fig. 1A). This is the basic "generalist" form favoring unsteady swimming. The presence of leading edge scales and scutes, a heavy fin ray skeleton, and more diffuse and weak axial support of median fin skeletal elements (Romer, 1966; Gosline, 1971; Moy-Thomas and Miles, 1971) suggest these early actinopterygians may have been less able to collapse their median fins for steady swimming. In addition, the notochord was unrestricted, lacked ossified centra, and had relatively weak neural and hemal arches (Schaeffer, 1967). These features would probably reduce the magnitude of compression and bending forces that could be tolerated. Furthermore, extension of the notochord to the caudal fin trailing edge and heavy scales probably reduced body flexibility (Aleyev, 1977) and hence the magnitude of propulsive forces that could be generated. Therefore, thrust was probably relatively low. The heavy ganoid scales would also increase mass resistance in acceleration (Webb and Skadsen, 1979) as well as side-slip forces during turns. Finally, the paired fins probably extended ventro-laterally like stiff planes, more analogous to modern sharks than modern actinopterygians (Romer, 1966), so that control in turns was probably relatively poor. Overall, unsteady swimming was proably emphasized (Lauder, 1980) but performance at all activity levels was probably poor in comparison to modern forms. Maximum locomotor power output was

9 ACTINOPTERYGIAN LOCOMOTION 337 Sardinops sagax Sal/no gairdneri Carassius aura/us SWIMMING SPEED (m.s"') Leuciscus leuciscus Trachurus symmetricus Scomber japonicus FIG. 3. Relationships between tail beat frequency and swimming speed for six species of teleost fish with various body forms. Data were taken from Hunter and Zweifel (1971) and calculations were based on a fish with a total length of 25 cm. With the exception of Sardinops, these species rank approximately from more anguilliform at the top with higher tail beat frequencies at a given speed, to more carangiform at the bottom, achieving higher speeds for a given tail beat frequency. All fish were tested individually except for Sarcknopi which was tested in groups of five; this may have influenced swimming kinematics. probably also limited by the anatomy of these early fish. This may have limited the evolution of specialized steady swimming morphologies which may have required compressive and bending forces over a narrow caudal peduncle in excess of skeletal tolerances. However, more elongate, anguilliform swimmers would not be excluded because thrust forces would undoubtedly be lower. Therefore, it is not surprising to see eel-like forms among chondrosteans (e.g., Tarrasius in Fig. 1A) nor to find they recur at each level of actinopterygian organization. If these arguments are correct, then the significance of morphological trends in successive levels of halecostome organization may be defined. Constriction of the notochord by increasingly ossified centra (Schaeffer, 1967) would increase compressive and bending strength. Greater body and fin flexibility through abbreviation of the notochord, reduction of skeletal material in the fin rays, and reduction in cosmoid and ganoid layers in the scales (Greenwood et al., 1966; Romer, 1966) could allow greater body flexibility leading to larger thrust forces for both steady and unsteady swimming. The more anterior insertion of the dorsal fin (Gosline, 1971) implies greater control of lateral recoil. The reduction in scale mass would reduce resistance in unsteady swimming. Increased fin flexibility would allow greater changes in caudal area to improve steady swimming, which would be further improved by the more frequent occurrence of "scooped out" tail fins {e.g., Caturus, Hypsocormus, Pholidophorus). The trends established among the halecostomes (greater constriction of the notochord by ossified centra, strong neural and hemal arches, abbreviation of the notochord, reduction in the number of caudal rays, improved articulation of fin rays with the axial skeleton and reduction in

10 338 PAUL W. WEBB scales) continue into the teleosts (Greenwood et al, 1966; Gosline, 1971). However, these changes also tended to weaken the support for the dorsal lobe of the caudal fin, by the formation of a "hinge" area, necessitating major structural changes which occurred at the pholidophorid/leptolepid level (Patterson, 1968a). At this level, the uroneurals of the ural centra at the base of the caudal fin extended over the preural centra to strengthen the caudal connection of the axial skeleton. At the same time this permitted full external homocercy as seen in the teleost tail fin. The structural changes probably improved transmission of thrust forces to the axial skeleton and also ensured symmetry of thrust forces in the vertical plane. Patterson (1968a) suggests the changes in caudal skeleton were associated with greater elasticity and flexibility of the trunk leading to more powerful and efficient swimming and greater exploitation of the advantages of neutral buoyancy. However, in spite of these apparent advantages of more powerful swimming forms, early teleostean external morphology shows little advance over the halecostomes. Radiation towards more specialized steady swimming modes after the early leptolepids is associated with greater ossification and strength in the preural vertebrate and in the articulation of reduced hypural bones on a single posterior half centrum. Reduced vertebral number, particularly in the trunk, probably serves to concentrate propulsive movements caudally. Such modifications occur throughout the actinopterygians (Greenwood etal, 1966) but it is not until the acanthopterygian level of organization that a sufficiently advanced stage is reached for large numbers of specialized steady swimming forms to occur. These include the appearance of the mechanically refined thunniform mode of propulsion (Fig. IE), previewed by an extinct shark, Cladoselache\ In summary, the recurring fusiform, large tailed generalist morphology in actinopterygians is probably a compromise between design criteria for unstead) and steadv swimming. The former area of performance is judged most important. The succession of these similar body forms throughout actinopterygian phylogeny is attributed to anatomical changes in strength and flexibility of the skeleton. Similarly, it is suggested that specialized steady swimmers would exceed the strength limits of the skeleton of early antinopterygians. As a result they are not common before the acanthopterygians. Elongate forms would not challenge design limits and hence regularly occur at all levels of actinopterygian radiation. Therefore, the most recent teleosts include the most diverse caudal propulsion morphologies, with some distinct new forms compared to previous radiations. The morphologically sophisticated fast cruising species that occur for the first time (Fig. IE) have evolved at the cost of unsteady swimming capabilities (Webb, 1977a; Webb and Keyes, 1981). In the other direction, recurring elongate forms are found swimming in anguilliform modes. Fish with this type of morphology eschew locomotor sophistication; for example the spiny eel, Mastacembelus loennbergi exposed to threatening stimuli withdraws its head instead of accelerating away (Eaton etal., 1977). Steady swimming performance is probably low (Beamish, 1978). However, the anguilliform body has permitted expansion into a wide variety of labyrinthine niches, in dense weeds, coral reefs, etc. and into soft substrates by burrowing. These habitats, and the associated body form, have not excluded anguilliform swimmers from making long pelagic migrations (e.g., Anguilla, Marshall, 1965), although the specialized thunniform cruisers are certainly excluded from the habitat of eels. In this respect, eel-like fish are more versatile, although less "glamorous." MEDIAN AND PAIRED FIN PROPULSION The most important and common functions of median and paired fin propulsion mechanisms are slow swimming and precise maneuver (Gosline, 1980). Variations in mechanisms have been classified in terms of morphology (Breder, 1926; Lindsey, 1978). There are currently insufficient comparative mechanical studies to provide a functional classification analogous to that

11 ACTINOPTERYGIAN LOCOMOTION 339 of caudal propulsion (Lighthill, 1975), in spite of major advances in theoretical and experimental studies by Blake (see review, 1981). The best integrative studies at this time remain those of Alexander (1967) and Gosline (1971) and the following discussion draws heavily on their insights. Mechanics and compromises The essential morphological features of slow swimming and precise maneuver are low or neutral buoyancy and flexible fins. Neutral buoyancy eliminates the need for fish to either swim fast enough to generate lift equal to their weight in water (Magnuson, 1978) or to rest on the bottom. Fin flexibility is required to pass controlled waves along the fins and to feather them as necessary. Slow swimming with median and paired fins is frequently associated with a deep truncate body. This may improve the effectiveness of the dorsal and anal fins when they are located along the trailing edge of the body (Webb, 1975a). The short body is postulated to reduce turning resistance by reducing the mass of the body and entrained water distant from the turning axis (Alexander, 1967), but would also allow fish to turn in a smaller space. Non-caudal slow swimming capabilities seem to be a secondary development in actinopterygians and marked radiation of slow swimming forms is only seen among higher teleosts. Some consideration must therefore be given to the questions of why median and paired fin propulsion occurs late in actinopterygian phylogeny, and of compromises and interactions between non-caudal and caudal swimming. Median and paired fin propulsion can be additive to caudal locomotion. Modern actinopterygians swim slowly to various degrees, with no obvious cost to caudal swimming performance (Webb, 1977a, 1978; Beamish, 1978; Dorn et ai, 1979). The use of pectoral and pelvic fins in an efficient "4 wheeled" braking system (Harris, 1937, 1953; Gosline, 1971) may enhance caudal propulsion because higher speeds are possible in cluttered habitats, such as among weeds, corals, etc. The paired fins can also be extended to aid high-speed caudal turning and maneuver by acting to increase drag on one side, and as vanes, keels, etc. (Gosline, 1971; Aleyev, 1977). Some fish may even replace caudal cruising with pectoral propulsion, as in the embiotocids without cost to cruising performance or costs of transport (Webb, 19736; Dorn et ai, 1979; Fish, 1980). This may permit specialization of the body and caudal fin for sprints and acceleration. Complete substitution of non-caudal median fin propulsion for caudal fin swimming (e.g., Mola, Fig. IF) is rare and the general adaptive significance is unclear. Perhaps greater maneuverability is possible at higher speeds. Specialization for slow swimming using non-caudal propulsion does appear to affect caudal propulsion. Such fish frequently have a deep body and caudal peduncle, and a large caudal fin area enhanced by the posterior insertion of dorsal and anal fins (e.g., Chaetodontidae, Pomacentridae). This morphology probably provides for good acceleration, but undoubtedly impairs steady swimming at high speeds. Data are not available, but observations by Hobson and Chess (1978) are instructive. They found that the body form of Enewetak Atoll (Marshall Islands) planktivores varied with the distance of their feeding stations above the reef. Fish with distant feeding stations were dependent on sprint swimming to return to the reef to escape predators, and these had fusiform bodies and forked tails. Fish with feeding stations close to the reef, requiring no more than a quick dart to reach refuge, had deep bodies with large caudal areas. The only exceptions were among some deep-bodied fish that foraged further from the reef, but which had longer spines than usual as passive predator defenses. To summarize, slow swimming capabilities can add to caudal propulsion performance increasing overall versatility, but specialization incurs a cost to caudal swimming. Phylogenetic trends The paired fins of chondrosteans were probably stiff and relatively inflexible. In spite of the presence of various air spaces,

12 340 PAUL W. WEBB these fish were probably negatively buoyant (Romer, 1966). They were therefore unlikely to be capable of very slow swimming. Occasional deep-bodied forms occurred (Fig. IB) but they were probably found in relatively open slow waters (Romer, 1966) and not in cluttered habitats. With the evolution of an effective suite of characters for neutral buoyancy (swimbladder, reduced armor) and greater fin mobility (Romer, 1966), some neopterygians were probably true slow swimmers. Initially, slow swimming and maneuver capabilities probably allowed the penetration of more weedy habitats and new options in stalking prey analogous to the behavior of modern Lepisosteus. More options would have become available in tortuous and labyrinthine habitats for more specialized deep-bodied forms, which were more common among the halecostomes (e.g., Dapedium, Proscinetes) than chondrosteans. Lower teleosts show little advance in slow swimming morphology and behavior over the halecomorphs, and deep-bodied forms only evolved to any marked degree in association with special habits, such as the "flying fish" Gastropelecus (Fig. ID). The major radiation of slow swimming modes occurs among the Acanthopterygii and to a small degree the Paracanthopterygii, associated with (1) the relocation of the pectoral and pelvic girdles so that the pectoral fins insert high on the body above, or even slightly behind the pelvics, which have migrated forward; and (2) the frequent rotation of the pectoral fin base towards the vertical plane (Greenwood et al, 1966; Romer, 1966; Gosline, 1971, 1980; Nelson, 1976). The pectoral and pelvic fins come to occupy strategic positions about the center of mass to generate a wide variety of propulsion and braking forces (Harris, 1937, 1953; Alexander, 1967; Gosline, 1971, 1980; Lindsey, 1978). The anus also migrates forward. The anal fin advances and more closely mirrors the dorsal fin, providing greater symmetry in median fin propulsors and extending the array of possible locomotor and maneuver forces. The new fin locations and extensions are also used as brakes and keels and increase versatility of caudal propulsion maneuvers (Gosline, 1971; Alevev, 1977). The rotation of the pectoral fin base to the vertical plane also introduces possibilities of interacting with the bottom in ways analogous to a helicopter. This ground effect can lead to substantial savings in energy costs by fish swimming close to the bottom (Blake, 1979). ACKNOWLEDGMENTS Much of the research reported here was made possible by grants from the National Science Foundation; BMS and PCM The manuscript was prepared during the tenure of an NRC/ NOAA fellowship at the National Marine Fisheries Service, Southwest Fisheries Center. I thank Dr. J. R. Hunter and Mr. R. S. Keyes for their hospitality and generous use of their facilities. I am indebted to Dr. W. A. Gosline for continuing to stimulate my thinking and for reviewing the manuscript, to Drs. G. V. Lauder and K. Liem for their comments on the manuscript, and to G. R. Smith, J. Humphreys and D. E. Rosen for interesting and conflicting discussions on historical hypotheses and confidence in cladograms. REFERENCES Alexander, R. McN Functional design in fishes. Hutchinson University Library, London, England. Alexander, R. McN Animal mechanics. Sidgewick and Jackson, London, England. Alexander, R. McN Swimming. In R. McN. Alexander and G. Goldspink (eds.), Mechanics and energetics of animal locomotion, pp John Wiley & Sons, New York. Aleyev, Y. G Nekton. Junk, The Hague, Netherlands. Atz, J. W., A. Epple, and P. K. T. Pang Comparative physiology, systematics and the history of life... Vertebrate endocrine systems. In P. K. T. Pang and A. Epple (eds.), Evolution of vertebrate endocrine systems, pp Texas Tech. Univ., Lubbock. Beamish, F. W. H Swimming capacity. In W. S. Hoar and D. J. Randall (eds.), Fish physiology, Vol. 7, pp Academic Press, New York. Bone, Q Muscular and energetic aspects of fish swimming. In T. Y. Wu, C. J. Brokaw, and C. Brennen (eds.). Swimming and flying in nature, pp Plenum Press, New York. Blake, R. W Energetics of hovering in the mandarin fish (Synchropuspicturatus). J. Exp. Biol. 82: Blake, R. W. 1980a. The mechanics oflabriform locomotion. 1. Labriform locomotion in the angelfish

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