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
