VERTEBRATE EVOLUTION BEGAN in an aquatic environment in the early Paleozoic (500+ mya), followed by the evolution of tetrapods and then the evolution of terrestriality in the middle Devonian (390 mya) (Clack 2002; Nelson 2006). The aquatic and terrestrial environments occupied by vertebrate organisms offer their own sets of challenges and opportunities. For instance, unlike air, water is incompressible for all practical purposes and has much greater viscosity (the resistance of a fluid to deformation because of internal friction). Viscosity becomes increasingly significant as body size decreases and so is an especially important issue for larval stages of fishes (Webb and Weihs 1986). Because the viscosity and density of water are much greater than in air, movement in water must overcome greater drag compared to terrestrial vertebrates moving over land or flying. As a consequence, aquatic organisms, other than those where speed is not an issue, have streamlined body shapes to reduce the energy requirements of locomotion. Also, volume for volume, oxygen content in water is about a thirtieth of that in air (Kramer 1987), and obtaining oxygen from water is additionally challenging by the need to move a viscous medium across respiratory surfaces. Compared to movement on land, the lack of a solid surface to push against reduces the resultant force, although water is a much more efficient medium to push against compared to air. In contrast to terrestrial vertebrates, because their density is close to that of water, aquatic vertebrates gain all or a majority of their bodily support from water rather than having to invest in a skeletal system that can carry the weight of the body. In addition, little energy is required to move vertically. In a now-classic study, Schmidt-Nielsen (1972) provided a way of comparing some of the costs and benefits of movement in water, air, and on land. He determined that the net energetic cost of powering 1 gram of vertebrate over 1 km relative to body size was lowest for swimming, intermediate for flying, and greatest for running. The disciplines of fish biomechanics and hydrodynamics are presently very active, due in part to new technologies allowing the precise quantification of water flow patterns around swimming fishes (Lauder and Tytell 2006). This chapter explores the interaction of morphological evolution in fishes with their success in various freshwater habitats.

BASICS OF FISH PROPULSION

The body of a fish essentially consists of a compression resistant notochord or vertebral column, surrounded by lateral musculature, and wrapped in a complex arrangement of connective tissue and skin (Danos et al. 2008). In contrast to terrestrial locomotion, where the limbs involved in locomotion must also support the body, fishes can use a variety of mechanisms for locomotion, both independently and in concert, and can employ a variety of control surfaces such as scales, body projections, and fins to affect their posture and position in the water column (Webb 1994, 2006).

Forces to Overcome

To achieve forward motion, the force generated by a swimming fish must equal (constant swimming speed) or exceed (acceleration) the resistance to movement caused by drag (Webb 1975; Blake 1983a). The two components of drag are friction drag and pressure drag, both of which can best be understood by boundary-layer theory. Water moving across the body of a fish, either by the fish moving through water or holding position in flowing water, has a gradient in relative velocity that increases from 0, where water molecules are in contact with the fish, to that of the free-stream velocity, the velocity of the undisturbed water at some distance from the fish (Blake 1983a). The region between the free-stream velocity and the velocity at the fish is referred to as the boundary layer (Figure 7.1). Flow in the boundary layer can be laminar, resulting in low friction drag, or turbulent, where the resultant eddies form a thicker boundary layer compared to laminar flow and overall friction drag is increased (Webb 1975; Blake 1983a). The change from laminar to turbulent flow is predicted by the Reynolds number, a hydrodynamic measure calculated as

where L = fish length; U = speed; and ν = the kinematic viscosity of water, which is approximately 0.01 cm²s⁻¹ (Webb 1975; Purcell 1977).

Friction drag arises from the viscosity of water in the boundary layer. The greater the surface area of the body, the greater the friction drag. Friction drag also increases exponentially with swimming speed. For laminar flow, the exponent is 1.5, rising to 1.8 for turbulent flow in the boundary layer (Alexander 1967a). Pressure drag is caused by eddies generated along and behind the body by the separation of the boundary layer from the body of the fish (Figure 7.1A). The farther back that boundary separation occurs, the lower the underpressure and the size of the wake. Because turbulent boundary layers separate farther back than laminar boundary layers (Figure 7.1B), the pressure drag resulting from separation of a laminar boundary layer is higher than that for a turbulent one (Blake 1983a). Streamlining also reduces boundary layer separation and thus lowers pressure drag. Other things being equal, pressure drag increases at approximately the square of velocity (Alexander 1967c). Because of how friction and pressure drag are formed, a body shape that reduces friction drag has the opposite effect on pressure drag. Friction drag is related to surface area, so a body shape that minimizes the surface-to-volume ratio, such as a sphere, would have the lowest friction drag. Among freshwater fishes, a more globular shape, such as shown by some sunfishes, would have lower friction drag but a higher pressure drag in contrast to a more elongate, streamlined fish such as a trout, which would have higher friction drag but a lower pressure drag (Alexander 1967c).

FIGURE 7.1. Flow separation around a fish holding position in flowing water.

A. Flow lines, friction and pressure drag, and the boundary layer at a point tangential to the body. The relative thickness of the boundary layer is greatly exaggerated. The length of the arrows indicates the relative velocity of water, ranging from zero in contact with the body of the fish to the free-stream velocity indicated by the arrows of identical length on the right.

B. Changes in flow separation from the body in laminar (dashed lines, black arrows) and turbulent (dotted lines, white arrows) flow. Based on Webb (1975) and Blake (1983a).

Generated Forces

Water flowing over the body and fins of a fish can generate lift because the shapes are acting as hydrofoils—such lift is often referred to as dynamic lift. Bernoulli’s equation predicts that pressure will decrease as the velocity of fluid increases across a surface, so lift for a hydrofoil occurs when flow across the upper surface exceeds that of the lower, resulting in a pressure differential (Webb 1975). Such conditions occur when the angle incidence (α) of the hydrofoil increases from zero (Figure 7.2). The lift generated by a hydrofoil acts normal to the drag force and increases with the angle of incidence up to a point where flow lines begin to separate from the hydrofoil (usually about 15°), resulting in a sudden increase in pressure drag and a sudden decrease in lift so that a stall occurs. Because the amount of lift generated by turbulent flow is greater than for laminar flows, as a consequence of later separation of flow lines as described previously, higher values of lift occur at higher Reynolds numbers (Webb 1975; Blake 1983a).

FIGURE 7.2. Flow lines, lift, drag, and the resultant pressure force at three angles of incidence (α) of a hydrofoil. Drag is parallel to the axis of flow (or motion) while lift is normal to the axis of flow or motion. Based on Webb (1975) and Blake (1983a).

Freshwater fishes occupy a wide range of habitats with a correspondingly high range of current speeds and degrees of turbulence. To maintain hydrodynamic stability, change posture, initiate changes in course, or change location, fishes must control translational and rotational forces. Translational forces refer to movement of a body from one point in space to another without rotation and occur in three planes: surge, slip, and heave (Figure 7.3). Surge refers to movement forward or backward, slip refers to sideways movement, and heave refers to movement up or down. Rotational forces refer to movement around the center of mass and occur along three axes: yaw, pitch, and roll (Figure 7.3). Yaw describes the rotation about the center of mass from side to side, pitch is the rotation up or down, and roll is the rotation along the horizontal axis of the body. Some actions do not result in a change of rotational or translational state because they result in keeping the body in the same location (e.g., hovering) (Alexander 1967c; Webb 2006).

Body Shape, Fin Location, and Maneuverability

Control and maneuverability during hovering or active movement are related closely to fin placement relative to the center of mass, the control of fin rays and fin area by muscles, and swimming speed (Alexander 1967c; Webb 2006). Four zones are recognized relating to fin placement and function (Figure 7.4): (1) an anterior body zone of rudders and lift surfaces positioned anterior to the center of mass that are important in translational forces; (2) a zone of keels located at the center of mass that are particularly important in controlling roll; (3) a zone of stabilizers located immediately posterior to the center of mass and important in controlling yaw, pitch, and roll; and (4) a zone of locomotion and rudders located well posterior to the center of mass that is again important in translational forces (Aleev 1969; Gosline 1971). Anterior control surfaces (zone 1) can include pectoral fins, the head, or the anterior part of the spinous dorsal fin, with the head particularly important in turning motion in elongate body shapes (Webb 2006). A fin, such as the spinous dorsal in zone 1, acts to deflect the fish away from its forward course, but during rapid forward progress in a straight line, it is advantageous for it to be folded down, which also helps to reduce drag. Pectoral fins can also be furled during high swimming speeds (Webb 2006). A single dorsal fin located over the center of mass (zone 2) serves as keel but does not stabilize or deflect the forward course of the body. Many lower teleosts, such as herrings, minnows, suckers, catfish, and trout (groups in the Clupeomorpha, Ostariophysi, and Protacanthopterygii; Figure 7.5), have dorsal fins in this general position or in a position slightly posterior to the center of mass where the fin can also function as a stabilizer (rudder) or aid in propulsion (Figure 7.4B) (Aleev 1969; Gosline 1971). In higher teleosts, such as Moronidae, Centrarchidae, and Percidae (groups in the Acanthomorpha; Figure 7.4A), the dorsal fin consists of two parts, the more anterior spinous dorsal fin and the more posterior soft dorsal fin. The spines can be raised or lowered depending on need. It is important to remember, however, that fins can serve multiple purposes, including camouflage, communication, and in the case of spines, defense.

FIGURE 7.3. Terms used in describing translational (black font and arrows) and rotational (gray font and arrows) changes in state about the center of mass in fishes. Photograph of Colorado Pikeminnow (Ptychocheilus lucius) courtesy of Tom Kennedy. Based on Alexander (1967a) and Webb (2006).

FIGURE 7.4. Potential fin functions relative to the center of gravity in (A) higher teleosts illustrated by the Freckled Darter (Percina lenticula), and (B) lower teleosts illustrated by the Blacktail Shiner (Cyprinella venusta). Based on Aleev (1969) and Gosline (1971).

FIGURE 7.5. Major levels of fish evolution. Names at the base of the cladogram define inclusive groups (e.g., Osteoglossomorpha to Tetraodontiformes are included within the Teleostei). Names at the ends of branches refer to particular lineages. Black text identifies groups that have, or had, representation in North American freshwater habitats. The Sarcopterygii includes lobefin fishes as well as tetrapods. Based on Nelson (2006).

Many freshwater fishes achieve static lift (=buoyant lift) by having air bladders or low-density fatty inclusions within the body cavity so that the mass of water displaced approaches the mass of the fish (Gee 1983). However, because the vertebral column bounds the upper extent of the abdominal cavity, low-density inclusions result in the center of buoyancy being beneath the center of mass (Eidietis et al. 2003). The difference between the center of mass and the center of buoyancy is termed the metacentric height, and a negative value, typical of most fishes, results in a rolling torque (a reason why a recently dead or an incapacitated fish turns belly up). Fishes must use behavioral changes, such as resting on the bottom or leaning against structures, or fin movements, to compensate for this inherent instability. To a certain extent, this rolling torque likely was reduced by the location of the swimbladder dorsal to the gut in actinopterygians compared to the ventral position of the lung (the precursor to the swimbladder) in early bony fishes (the lobefin fishes within the Sarcopterygii) such as lungfishes (Lauder and Liem 1983; Webb 2002). Some actinopterygians also have a more anterior location of gas volume such that the pitching torque generated by the mass of the head skeleton is reduced (Webb 2006).

Types of Locomotion

Fish swimming modes can be divided into those involving the body and caudal fin (BCF) and those using various combinations of paired or median fins for locomotion (MPF) (Blake 2004). BCF locomotion is undulatory, involving alternate waves of contractions on either side of the body, because of sequential innervation of lateral body muscles (serial myomeres) that are three-dimensionally folded and divided into blocks by connective tissue (myosepta) (Danos et al. 2008). Furthermore, BCF swimming can be subdivided into steady, continuous swimming versus unsteady, transient (burst and coast) swimming (Blake 2004). Burst-and-coast propulsion occurs in many pelagic and nektonic fishes, and in fishes with streamlined bodies, it can provide considerable energy savings per distance traveled in contrast to steady swimming (Blake 1983b).

BCF swimming typically is categorized into three to five modes: anguilliform, subcarangiform, carangiform, thunniform, and ostraciiform (Breder 1926; Webb 1975; Lindsey 1978). The modes are named after exemplar species and characterized by increasing concentration of the propulsive force in the caudal fin, although they do not imply phylogenetic relationships (Webb 1975; Blake 2004). The ostraciiform mode has a complete, or nearly complete, absence of body undulation with all propulsive power generated by oscillation of the caudal fin. Because the ostraciiform swimming mode is exemplified by tropical marine box fishes, marine electric rays, and tropical African freshwater elephant fishes (Lindsey 1978; Helfman et al. 2009), and is not represented by any North American freshwater fish group, it will not be discussed further.

The remaining four modes were originally defined by perceived differences in swimming based on morphology and not on hydrodynamic analyses and, among other things, overlooked the three-dimensional geometry of the body during swimming. Recent research indicates that two-dimensional views of dorsal midline profiles of anguilliform, subcarangiform, carangiform, and thunniform modes are essentially indistinguishable, at least during certain swimming speeds. Because of this, the traditional modes of BCF swimming in fishes are not always representative of hydrodynamic differences and lack a functional basis (Blake 2004; Lauder and Tytell 2006). Current research suggests that thunniform and carangiform modes are quite similar in most, although not all, features. Because of the high similarity between the carangiform and thunniform modes (Blake 2004), and because I know of no North American freshwater fish using a thunniform swimming mode, it is not treated further. The remaining three BCF modes are not distinct in all attributes and are grouped differently based on different functional and morphological criteria, including propulsive wavelengths, wake patterns, tendon lengths, and red muscle activity (Table 7.1) (Lauder and Tytell 2006; Danos et al. 2008). Thus, although useful as general shorthand descriptors of BCF swimming, the taxon-named swimming modes are not totally distinct but share various features.

ANGUILLIFORM BCF LOCOMOTION In anguilliform swimming, which is ontogenetically and phylogenetically the basal mode of BCF swimming in ray-finned fishes, the Actinopterygii (Figure 7.5), the entire body is employed to generate thrust through a series of waves moving from head to tail (Gosline 1971). In contrast to early studies indicating that large amplitude undulations occurred all along the body over a range of swimming speeds, recent work indicates that body waves have increasing amplitude posteriorly, thus increasing water displacement toward the tail, and that the anterior body region only shows strong undulation during acceleration and not during steady swimming (Müller et al. 2001; Lauder and Tytell 2006). Fishes using anguilliform swimming are elongate and flexible, such as freshwater eels, lampreys, some catfishes, and the larvae of most fishes (Blake 1983a). In contrast to nonanguilliform swimming, anguilliform swimmers are also generally adept at backward locomotion (Webb 2006).

TABLE 7.1 Similarities and Differences among Commonly Recognized Modes of Body and Caudal Fin (BCF) Locomotion

Anguilliform swimming, at least as shown by eels, does differ from other swimming modes in several ways (Table 7.1). Red muscle activation tends to occur in short blocks ipsilaterally, in contrast to long blocks in the carangiform mode and intermediate blocks in the subcarangiform mode (Danos et al. 2008). One of the original descriptors of swimming modes, the propulsive wavelength adjusted for body length, is still useful, being short in anguilliform swimming, intermediate in subcarangiform modes, and high in carangiform modes (Tytell and Lauder 2004; Danos et al. 2008). Even though it tends to increase posteriorly, wave amplitude is also somewhat greater anteriorly in anguilliform swimming, in contrast to the other modes that are highly similar in this regard (Lauder and Tytell 2006). Wake form differs in anguilliform swimmers, with wakes having lateral momentum but not substantial downstream flow momentum (the momentum opposite the line of thrust of the body), in contrast to other swimming modes. The difference most likely is caused by the absence of a distinct caudal fin structure in eels in contrast to fishes having caudal fins that are distinct from the body (Lauder and Tytell 2006). In five other features, anguilliform and subcarangiform modes do not differ (Table 7.1). These include four features of the myosepta (the sheets of connective tissue separating blocks of myomeres and onto which muscle fibers insert) involving the lateral myoseptal tendon length, the presence of epineural (located on the dorsal surface of the vertebral centrum) and epipleural (located above the abdominal ribs) tendons, and the shape of the myosepta; the fifth similarity is in the firing duration of red muscle fibers (Danos et al. 2008). Red muscle fibers are oxidative and used in slow, prolonged swimming; as such, they are highly vascularized and contain abundant myoglobin, a red oxygen-binding pigment characteristic of muscle (Syme 2006).

LARVAL FISHES AND ANGUILLIFORM LOCOMOTION During their larval period, the majority of all North American freshwater fishes use anguilliform locomotion in the sense of generating more than one complete propulsive wavelength within the length of the body (Webb and Weihs 1986). Anguilliform swimming in larvae occurs because the musculature and axial skeleton are not sufficiently developed to use lift-based subcarangiform or carangiform modes, both of which would place greater compressive force on the axial skeleton and require more muscular power. In addition, because of their small size and speed, larval fishes operate in an environment dominated by viscous rather than inertial forces so that any cessation of swimming movement stops forward progress—there is no coasting in the absence of inertial forces. The balance between viscous and inertial forces is determined by the Reynolds number (Re), the same equation described previously for prediction of laminar versus turbulent flow in a boundary layer. Re<1 indicates a totally viscous environment and Re >1,000 indicates a totally inertial environment; at intermediate values both forces are represented (Lauder and Tytell 2006), but for values of Re below 300–450, viscous forces predominate over inertial forces (Webb and Weihs 1986; Fuiman 2002). It is difficult for us to really imagine life at low Reynolds numbers. Purcell (1977), in discussing swimming in microorganisms and the impact of the primacy of viscous over inertial forces, said: “If you are at [sic] very low Reynolds number, what you are doing at the moment is entirely determined by the forces that are exerted on you at that moment, and by nothing in the past.”

Once the yolk sac is absorbed, larval fishes generally swim at 1–3 body lengths per second (Fuiman 2002). Thus R_e of a 5-mm larval fish would be 25–75, at the lower end of the intermediate range, and subject to viscosity effects. In a viscosity-dominated environment, pushing against the water by an elongate body is more effective than using caudal fin propulsion (Webb and Weihs 1986), but because of the unimportance of inertial forces, larvae must swim continuously to move. (Recall that the law of inertia, or Newton’s first law, states that a particle at rest or moving in a straight line with a constant velocity will continue to do so, provided the particle is not subject to an unbalanced force.) As soon as the larvae stop actively swimming, they come to a halt (Purcell 1977; Blake 1983a). As fishes increase in size, the importance of inertial forces increase relative to viscous forces so that once Re reaches 300–450, they can employ an energy-saving burst-and-glide approach to locomotion (Fuiman 2002).

NON-ANGUILLIFORM BCF LOCOMOTION Increased posterior localization of body undulation and power and the development of distinct caudal fins characterize the traditional modes of subcarangiform and carangiform locomotion (Table 7.1). Subcarangiform swimming occurs in the majority of nonlarval North American freshwater fishes, including salmonids, cyprinids, catostomids, centrarchids, and percids; however, specific studies on swimming are limited to relatively few species of salmonids, cyprinids, and centrarchids (Blake 1983a; Lauder and Tytell 2006). Subcarangiform fishes typically have fairly flexible but low-aspect-ratio caudal fins, such as the fins of many minnows, suckers, catfishes, sunfishes, and darters (Figure 7.4). Aspect ratio expresses the amount of lift generated by a hydrofoil, with lift increasing with aspect ratio, and is determined by the square of fin span divided by fin area. Examples of carangiform swimmers within North American freshwater fishes are less common but potentially include herring and shad (family Clupeidae). Carangiform swimming also is likely approached by two large cyprinid fishes endemic to the Colorado River system, Humpback Chub (Gila cypha) and Bonytail Chub (G. elegans); both have high-aspect-ratio caudal fins and narrow caudal peduncles, although there are no supporting biomechanical or hydrodynamic studies on these species. Consequently, in terms of BCF swimming, the vast majority of North American freshwater fishes occupy the anguilliform-subcarangiform range of swimming modes.

FIGURE 7.6. A. Bluegill (Lepomis macrochirus), with the dotted line showing the outline of the pectoral fin used in labriform locomotion.

B. Gait change and relative metabolic power and cost as a function of swimming speed in Bluegill (mean length 19.5 cm). The gait transition occurs at approximately 1.3 body lengths per second. Based on data from Kendall et al. (2007).

MPF LOCOMOTION Similarly to categorization of BCF swimming modes, Breder (1926) recognized six undulatory modes of MPF locomotion and one oscillatory mode, based principally on the median or paired fins involved, the general appearance of the waveforms, and the length of the fin relative to body length, but not on functional aspects of fin kinematics (Blake 1980, 1983a). In a simplified system, Blake (1983a; 2004) recognized the distinction between undulatory and oscillatory modes and divided undulatory modes into two groups based on fin kinematics. Type I includes fishes using fins with high amplitude, low frequency, and long wavelengths, such as dorsal fin locomotion in the Bowfin (Amia calva). Amiiform locomotion is also advantageous in allowing backward as well as forward locomotion (Webb 2006). Type II includes fishes using fins with low amplitude, high frequency, and short wavelengths, such as pipefishes (Syngnathidae), a primarily marine group but with some species, such as the Gulf Pipefish (Syngnathus scovelli), entering into fresh water. Because thrust is achieved most efficiently by accelerating a large mass of water to a low velocity rather than the reverse, type I locomotion is more efficient than type II (Blake 1983a).

Oscillatory fin locomotion, also referred to as labriform swimming, is shown by fishes using pectoral fins for locomotion, such as mudminnows (Umbra spp.), sticklebacks (Gasterosteidae), and certain centrarchids (Lepomis and Pomoxis) (Figure 7.6; Drucker and Lauder 2000; Walker 2004; Jones et al. 2007). Fishes using MPF locomotion are common in complex habitats such as weedy ponds, lake margins, or streams with abundant submerged or emergent vegetation or woody debris and are adept at backward as well as forward locomotion (Webb 2006).

Ecology of North American Freshwater Fishes

Подняться наверх