2 Locomotion and Biomechanics

Since Aristotle, the movement of fishes has fascinated scientists. Fish movements are fast, and the first classifications of fish swimming, made without high-speed video, are often criticized as being over generalized (Figure 2.1; Breder 1926; Webb 1975; Lindsey 1978). Although these early classifications are valuable as a general guide to the diversity of fish swimming styles, as technology improves and we study more animals, we find the distinction between groups becoming blurred.

FIGURE 2.1 Diversity of fish swimming. (a) Spectrum of swimming types: a – anguilliform, b – subcarangiform, c – carangiform, d – ostraciiform, e – thunniform, f – rajiform, g – diodontiform, h – mobuliform, i – labriform, j – amiiform, k – gymnotiform, l – balistiform, m – tetraodontiform. Red dashed line denotes the fin or body portion used in the stereotypical form of each locomotor mode. (b) Fish swimming kinematic parameters. Outline of Polypterus senegalus swimming at two points in a locomotor cycle. Tail amplitude (red), is measured from tail tip at its most lateral position to the fish’s midline (approximated by dashed grey line). Body wavelength (λ) is the distance between two body wave peaks. Specific wavelength is body wavelength divided by total body length (green).
(Panel A modified from Lindsey, C. C., in Fish Physiology, Academic Press, 1978, pp. 1–100.)

Fishes exhibit two broad categories of locomotion: body caudal fin (BCF) locomotion and median-paired fin (MPF) locomotion (Breder 1926). In the former, waves pass along the fish’s body, while in the latter, median (dorsal, anal) and paired (usually pectoral) fin motion provide propulsion. Fin or body motions can be oscillatory or undulatory as defined by the motion’s resultant wave amplitude, wave speed and specific wavelength (body wave length/body length [BL]) (Figure 2.1).

2.1.2 Body Caudal Fin Locomotion

Despite large species variation, generally, body wave amplitude is smallest at the fish nose and increases posteriorly to a maximum at the tail tip (Gray 1933; Gillis 1996). For most species, the body wave moves at a constant (or slightly accelerating) velocity towards the tail (Gillis 1997), and the specific wavelength changes between species depending on their body length, stiffness and general shape. Although the functional significance of specific wavelength is debated, it is used to help define sub-types of BCF locomotion (calculated as wavelength/body length) (Figure 2.1; Webb 1975).

Anguilliform locomotion, used by long, thin fishes, usually has a specific wavelength of less than one (meaning that more than one wave is on the body at a time) with a relatively large lateral amplitude along most of the body (max 0.3–0.4 BL at the tail; e.g. Anguilla anguilla; Lindsey 1978). Subcarangiform swimmers can have a specific wavelength of less than one; however, body waves occur along the posterior half or third of the body, increasing towards the tail (e.g. rainbow trout – Onchorynchus mykiss; Webb 1988; Bainbridge 1963; Webb 1992). Carangiform fishes usually have a specific wavelength greater than one, with waves confined to the posterior third of the fish (e.g. mackerel – Scomber scombrus; Lindsey 1978). Thunniform swimmers (named after the Thunnus) have a specific wavelength of 1–2 BL. This relatively long propulsive wavelength is likely due to the specialized morphology of these fishes. Since they have a rigid vertebral column with myotomes (groups of muscle fibers) that insert across a larger number of vertebrae, they are less able to bend locally, thereby increasing specific wavelength (Bainbridge 1958; Webb et al. 1984; Dewar and Graham 1994). Ostraciform swimmers, named after the boxfishes, tend to be armored anterior to the caudal fin, and so often only the caudal fin undulates (Lindsey 1978). These fish can use synchronous movements of their pectoral, dorsal, anal and caudal fins depending on their speed (Hove et al. 2001). For example, pectoral and anal fins power swimming at low speeds (<1 BL/s), anal and dorsal fins power swimming between 1 and 5 BL/s, and a caudal, kick-and-glide gait is used above 5 BL/s.

Many of the variables used to describe and quantify swimming are in two dimensions. Three-dimensional data on fishes is complex, and although relatively easy to acquire with modern high-speed video, remains difficult to quantify meaningfully. Recent work shows that the three-dimensional (3-D) motion or twist of fishes may also be important, particularly in elongate fishes (Donatelli et al. 2017). Computational fluid dynamists who integrate the 3-D shape and motion of fins and body to describe predicted flow patterns produced by swimming fishes are showing that a 3-D approach to fish swimming is essential to determine how unsteady movements influence fish locomotion (Ming et al. 2018; Liu et al. 2017). While the body and/or caudal fin are likely responsible for producing the majority of the thrust during BCF swimming, the fins are under active muscle control to help stabilize against perturbations that might otherwise cause roll, tilt or yaw (Standen and Lauder 2007; Drucker and Lauder 2005; Maia et al. 2017; Tytell et al. 2008).

2.1.3 Median and Paired Fin Locomotion

There is a diverse spectrum of median and paired fin (MPF) use, from undulatory motion (passing a wave along the fin surface) to oscillatory motion (rowing the fin back and forth). Fin motions often change depending on swimming speed, and individuals can switch between pectoral fin, median fin, and body and caudal fin use as required. MPF swimming modes are generally classified by the group of animals that tend to demonstrate the behaviour.

Labriform locomotion is powered by oscillatory pectoral fin flapping (Figure 2.2) and can be drag-based or lift-based (Walker and Westneat 2002b; Drucker and Jensen 1997; Bellwood and Wainwright 2001). The drag-based form consists of a power stroke followed by a recovery stroke and is used across a narrow range of swim speeds by a variety of fishes, from short-bodied Centrarchidae (Gibb et al. 1994) and Cichlidae (Blake 1979) to long-bodied Nototheniidae (Archer and Johnston 1989). During the power stroke, fins adduct through the water with their maximum surface area perpendicular to the axis of propulsion. During recovery, fins rotate and abduct with the maximum surface area parallel to the direction of travel to minimize drag. In contrast, lift-based labriform swimming orients the fin parallel to the flow and oscillates it in a dorso-ventral motion to create lift (Figure 2.2; Drucker and Jensen 1996a, 1996b; Webb 1993). Labridae (Westneat 1996; Walker and Westneat 2002a) and perciform fishes (i.e. Embiotocidae; (Webb and Weihs 1994; Drucker and Jensen 1997) use this form of motion; however, drag and lift-based modes are often used in conjunction with each other depending on the needs of the animal (Webb 1973; Westneat et al. 2017). The oddly shaped pectoral fins of skates and rays can also oscillate in what looks like underwater flapping flight (Mobuliform locomotion; Fish et al. 2018, 2016). Dorsal and anal fins can also be used in an oscillatory fashion (Tetraodontiform locomotion), as seen in the pufferfishes that flap their dorsal and anal fins from side to side in concert to power locomotion.

FIGURE 2.2 Pectoral fin swimming. Labriform swimming. (a) Lift-based, dorso-ventral fin motion acts like a flapping foil to produce lift and thrust. (b) Drag-based: fin adduction during the power stroke creates thrust (steps 1–3); during the recovery stroke, the fin is abducted parallel to the flow, minimizing drag (steps 3–5). (c) Rajiform pectoral fin undulation passes a wave anterior to posterior along the fin edge.
(Panels a and b modified from Walker and Westneat 2002a.)

Undulatory fin motion involves passing waves along the surface of the median fins (Gymnotiform – anal fin, Amiiform – dorsal fin, and Balistiform – both anal and dorsal fins) or the pectoral fins (Rajiform and Diodontiform locomotion)(Figure 2.1; Blake 1978; 1983, Jagnandan et al. 2014). Generally, during these forms of steady swimming, the body is straight, and additional fins are not used or are entirely absent. One notable characteristic of this form of swimming is the ability to swim both forward and backward with fluidity (Youngerman et al. 2014). Many species combine oscillatory and undulatory fin movements, the locomotion style correlating with the ecology and morphology of the fish (Rosenberger 2001).

2.1.4 Gait Changes

A fish may exhibit one type of swimming at slow speeds and transition into another at higher speeds (Hale 2006; Drucker and Jensen 1996a). For example, the bluegill sunfish oscillates its pectoral fins at speeds under 1.0 BL/s and changes to BCF swimming at higher speeds (Standen and Lauder 2005). In fact, most fishes (especially BCF swimmers) will use the “kick-and-glide” mode of locomotion when swimming at very high speeds. This behavior is composed of short bursts of caudal fin oscillation interspersed with glides where the body is straight, presumably to reduce drag (Jayne and Lauder 1996; Hove et al. 2001). At high swimming speeds, this gait appears to be more energy efficient than other modes of steady swimming (Wu et al. 2007). Different swimming modes may also be more or less efficient depending on the environment. For example, in an experiment where fishes were exposed to water flows that mimic coral reef wave-surges, it appeared that MPF swimmers were better able to reduce costs associated with increased wave surge frequency compared with BCF swimmers (Marcoux and Korsmeyer 2019).

2.2 Complexity of Fish Forces

2.2.1 General Biomechanics: Force, Power and Thrust

Before understanding how fishes produce forces and the consequences of those forces, it is important to clarify the basic relationship between force, work and power. Force is the product of an object’s mass and its acceleration (F = ma with units kgm/s² or N); therefore, the size and acceleration of an animal will determine the amount of force it must produce. The amount of work an animal performs, which may be considered a more important evolutionary metric, is the force produced times the distance travelled; W = F*d with units kgm²/s² or J. Finally, power is the amount of work done per unit time; P = W/t with units J/s or W. From an organismal perspective, you can consider that an animal experiences mechanical forces from the environment and produces biological forces with its muscles. Muscles can produce positive, negative or no work depending on the resultant motion of the muscles and/or animal, and finally, the speed with which the animal can perform the work will determine the power it can produce. Using a whole animal as an example, a fish accelerating from zero velocity in still water produces a force with its tail (mass × acceleration). The distance it travels with that amount of force determines the work it produces (F × d). The time it takes for it to cover that distance or complete the work tells you the power it took (W/t). This type of motion analysis can also be done at the muscle level, thinking about how far and how fast myosin and actin move relative to each other while producing force. With force, work and power concepts firmly in our minds, we can now discuss how fishes produce forces and what it means in evolutionary terms from the tissue level to the whole organism.

2.2.2 A Little about Muscle: Motor, Spring or Break?

All animals have excitable muscle tissue. Muscle cells are specialized with carefully organized myosin and actin filaments aligned such that they can move relative to one another within the cell to produce forces. The combination of fiber types and arrangement (muscle fiber architecture) on the skeleton impacts muscle fiber performance, dictating how fast they can contract, how long they can sustain a contraction, and where the force is applied on the animal’s skeleton. Although all muscle contractions involve the action of myosin and actin, muscles can act as motors (shortening during activation, concentric contraction), brakes (elongating during activation, eccentric contraction) or struts (remaining the same length during activation, isometric contraction (Figure 2.3; for a general biomechanics review see Vogel 2003; Dickinson et al. 2000). During each of these phases, the myosin and actin are busy ratcheting relative to one another and producing forces within the muscle cells, but the resistance of the external environment dictates the resultant muscle movement. Interestingly, the physiological performance, in this case measured as how much force a muscle can produce, changes depending upon the length of the muscle fiber; whether it is shortening or lengthening during activation and whether it is stretched prior to activation (Figure 2.3). The complexities of muscle performance are still being clarified, but it is important to keep this variable performance in mind when considering how fishes power swimming.

FIGURE 2.3 Muscle functional diversity. Work loops (a, b and c plots) visualize muscle length change and force production during cyclical activities. (a) Positive work is produced by the pectoralis muscle during flight. (b) Leg muscles act as brakes in running cockroaches. (c) The turkey gastrocnemius changes function between uphill and level ground running. (d) Fish body muscle can act as a motor or a strut, depending on cycle timing. Body muscle actively bends the fish (motor) or actively resists bending, permitting the transmission of force to more posterior positions on the fish (strut). (e) The amount of force a muscle can produce depends on its length and the optimal overlap of myosin and actin fibers (highlighted in red). (f) Muscle force production and power output vary with contraction velocity. The faster the contraction speed, the less force is produced, since actin and myosin cannot ratchet properly. Force continues to increase at negative velocities (active muscle lengthening). Power, the product of force and velocity, peaks near the middle of the force–velocity curve. Force in red, power in purple.
(Panels a–d modified from Dickinson, M. H. et al., Science, 288, 100–106, 2000).

2.2.3 Muscle Anatomy

How the muscle fibers attach to the skeleton is also exceptional in fishes and leads to an interesting passing of forces along the body. Fish body musculature is divided by muscle fiber type; the red muscle is located in a very small band along the side of the fish, and it is used for routine, continuous swimming (Hickman et al. 2018); Figures 2.4 and 2.5). The bulk of the body is white muscle, used for powerful maneuvers, burst swimming or escape response (Syme 2006), and consists of a series of nested units. Each unit is called a myomere, and they attach intricately with one another in a V or W nested cone configuration (Figure 2.4). A series of inter-myomere tendons and fascial sheets allow the contracting muscle to pass forces between the spinal vertebrae and the fish skin, as well as along the cones of the myomeres themselves, resulting in body stiffening and passing forces to augment tail motion (Gemballa and Vogel 2002; Gemballa et al. 2003). The unique structure of the myomeres in fishes, as well as the curved trajectories of the individual muscle fibers within the myomeres, has been explained via the uniform strain hypothesis, which suggests that this orientation allows all muscle fibers of a given type to contribute equally to force production during swimming (Alexander 1969). Because a swimming fish is essentially a bending beam, and because beam theory states that forces are greater the further you are from the neutral axis of the beam, if fish muscle ran parallel with the spine, the fibers located furthest from the spine would provide the most force, and those close to the spine would provide none. The uniform strain hypothesis states that for a fish to effectively use all of its muscle fibers, they must alter their orientation with respect to the spine. Subsequent modelling supports this idea by accurately predicting the trajectories seen in fish muscle fibers based on achieving mechanical stability of the fish (van Leeuwen 1999).

FIGURE 2.4 Fish muscle anatomy. (A) The arrangement of myomeres in a gnathostome. (B) Diagram showing how myomeres (pink) and myosepta (grey) nestle into one another. Tendons as part of the myosepta (grey) are indicated: epineural tendon (ENT), epipleural tendon (EPT), myorhabdoid tendons (MT) and lateral bands/tendons (LT). The attachment line of the myosepta to the skin is indicated by the red line.
(Tendon alignment adapted from Gemballa, S., et al., Journal of Evolutionary Biology, 16, 966–975, 2003; trout myomere image adapted from Hickman, C. L., et al., 2018. Laboratory Studies in Animal Diversity, 8th ed, McGraw-Hill Publishing, 2018.)

FIGURE 2.5 Muscle recruitment during swimming. Red muscle is active along the length of a fish at all swim speeds and increases contraction frequency with speed. White muscle is recruited at higher swimming speeds.
(Modified from Moyes, C.D. and Schulte, P.M., Principles of Animal Physiology, 2nd ed., Pearson, 2016.)

The anatomy of the fish musculature, in combination with the tuning capabilities of the muscle fibers themselves (white, red and intermediate fibers; for review see Syme 2006), allows fishes to engage all of their muscle mass for powerful burst swimming or only part of their muscle mass for moderate endurance swimming (Moyes and Schulte 2016; Figure 2.5). White and red fibers are more heterogeneously mixed in fin muscles; however, there is often a general pattern of centrally located aerobic fibers with surrounding white fibers (Du and Standen 2017). The functional implication of fiber regionalization in fins is not clear.

2.2.4 Diversity of Fin Anatomy and Structure

Most fishes have two sets of paired fins, the pectoral and the pelvic fins, and three median fins, the dorsal, anal and caudal fin (Figure 2.1). During the evolution of fishes, immense variation in fin number, shape and size has occurred. Many of the functions of ornate and elongate fins are for purposes other than locomotion, such as sexual selection (i.e. swordtails) or crypsis (i.e. sea dragons), and there is often a tradeoff between alternate functions and locomotion. Among the fins selected for locomotory performance, there are many shapes, sizes and levels of stiffness, and each is used in a different style of locomotion (Lauder and Drucker 2004). Although there are differences in the degree of fin element stiffness or fusion, they are all controlled in a similar way. Fins are composed of segmented boney elements, or fin rays, that are joined together by a flexible membrane (Figure 2.6). Each fin ray, termed a lepidotrichia, is made up of two hemitrichia. These bones are joined by elastic elements, which allows them to slide relative to one another and facilitates bending of the fin surface (Videler and Geerlink 1986; Alben et al. 2007). A set of muscles at the base of each fin ray controls the motion of the ray, moving it relative to the body but also moving hemitrichia relative to each other, allowing the fin to bend. In general, fish fins are incredibly deformable surfaces that are highly controlled. Fishes can increase or decrease fin surface area depending on the required force production and function. Fins are critical for stabilization and destabilization during locomotion and maneuvering.

FIGURE 2.6 Fish fin rays are under active muscle control to change fin shape. (a) Fin rays are segmented and branch near the tip, as can be seen in a cleared and stained fin. At rest (b), the two hemitrichia align, and the lepidotrichia is straight. (c) Under unequal muscle tension, the hemitrichia slide relative to each other, thereby bending the ray.
(Modified from Alben, S., et al. Journal of The Royal Society Interface, 4, 243–256, 2007.)

2.3 Muscle Activity and Neurocontrol

2.3.1 Muscle Activity

Swimming speed increases with tailbeat frequency, driven by an increase in muscle recruitment and an increase in the frequency of the muscle activation wave that passes along the body (Figure 2.5; Coughlin 2002). The timing of muscle strain cycles (the lengthening and shortening of muscle fibers) relative to muscle activity is essential to the functional performance of a muscle during locomotion (Altringham et al. 1993; Altringham and Ellerby 1999; Rome et al. 1993; Curtin and Woledge 1996). The state of the muscle fiber (its length and motion) before activation will influence the amount of force it can produce (Figure 2.3). Thus, the difference in timing of muscle activation within a strain cycle (i.e. the phase lag) is critical and varies both with species and along the length of a fish (Grillner and Kashin 1976; Williams et al. 1989; van Leeuwen et al. 1990; Wardle et al. 1995). At low speed, locomotion is powered exclusively by red muscle, and white muscle is progressively recruited as fish swim faster (Figure 2.5; Rome et al. 1993).

2.3.2 BCF Swimming

How red muscle is used during different swimming modes is still debated. The larger-amplitude wave that is found all along the body in anguilliform swimmers appears to be accompanied by more uniform head to tail muscle activity patterns (Wardle et al. 1995). In contrast, the anterior body muscle contractions of non-anguilliform swimmers do not accompany an anterior body wave; they produce forces that pass via stiffened muscle and tendon to the posterior body wave and tail to be subsequently turned into thrust (Wardle et al. 1995; Altringham and Ellerby 1999). The suggested functional outcome of this, which is supported by the hydrodynamic forces produced in the wake of fishes (Lauder and Tytell 2006), is that anguilliform swimmers produce power and thrust along the entire length of their bodies.

The passing of muscle effort posteriorly in non-anguilliform swimmers results in differences in muscle timing and behavior along the fish length that are much more noticeable. For example, as you approach the tail of the fish, there is a decrease in the duty cycle, the amount of time the muscle is on during a tailbeat (anguilliform swimmers have a constant duty cycle along their length; Gillis 1998). The amount by which a muscle shortens (strain) and the resultant body amplitude increase towards the tail. The phase lag in timing between muscle activation and resultant body amplitude also increases towards the tail (posterior muscles come on earlier relative to peak wave amplitude) (Figure 2.7; Altringham and Ellerby 1999; Rome et al. 1993; Shadwick et al. 1998). In essence, the wave of muscle activity passes anterior to posterior faster than the wave of body deflection. This is taken to an extreme in tunniform swimmers, where the wave of muscle activity passes along the anterior of a tuna so quickly that it is near synchronous, straightening and stiffening the anterior body and passing all of its force to caudal thrust production (Shadwick et al. 1999). Changes in muscle function along the fish body can be related to swimming speed as well as the ecology of the fish (Coughlin 2002).

FIGURE 2.7 Phase lag between muscle activation and body kinematic event. Maximum body amplitude occurs sooner following muscle activation at the fish’s anterior than at its posterior. Muscle position is denoted as a blue dot on the fish outline.

2.3.3 Labriform Locomotion

Much less work has been done on the muscle activation patterns in fin musculature during swimming. This is partly due to the very small size of many fin muscles and the difficulty in accurately implanting electrodes without damaging muscle function. Most work is on the anatomical function or free-swimming activation patterns in the pectoral fins of labriform swimmers (Williamson 1893; Danforth 1913; Westneat 1996). Although the large abductor and adductor muscles tend to be responsible for the larger-scale fin motions, a variable number of smaller fin muscles also contribute to the locomotor stroke (Drucker and Jensen 1997; Westneat and Walker 1997). The gait transition from pectoral fin swimming to BCF swimming is likely due to aerobic fin muscles reaching a limit in their power output, necessitating the recruitment of body muscle to swim faster (Drucker and Jensen 1996a).

2.3.4 Unsteady Swimming

All the above has been concerned with fishes swimming steadily, but of course, most fishes do not swim steadily, and most of their behaviour in the wild is composed of turns, escapes from predators, swimming through turbulent flow, etc. Limiting studies to steady swimming simplifies the system and allows basic observations of muscle patterns, kinematics and neural control; however, understanding the full range of kinematics and muscle activity that fishes use on a regular basis requires thorough quantification of unsteady swimming.

2.3.5 Escape Response

One of the best-studied unsteady behaviours that fishes perform is the fast start. Fast starts can be initiated either by the reticulospinal neurons (a slower response) or by the Mauthner neurons (a faster response) to escape predators and catch prey. This behaviour is composed of three kinematic stages: preparatory stage 1, propulsive stage 2 and variable stage 3 (Eaton and Hackett 1984). Stage 1 is generally defined as the formation of the initial starting position (either a “c” shape or an “S” shape). Stage 2 can be defined in a variety of ways but generally corresponds to the change in direction of the anterior body (Kasapi et al. 1993; Domenici and Blake 1991, 1993), the onset of forward propulsion (Foreman and Eaton 1993), and the onset of contralateral muscle activity (Jayne and Lauder 1993) (though each of these occur at slightly different times). Stage 3 is highly variable and loosely defined. Unlike steady swimming, the neural control that leads to a Mauthner fast start is relatively well established. Stage 1 is initiated by the triggering of the Mauthner neurons (Sillar 2009), which are connected to each other via gap junctions, direct cell–cell electrical connections that allow rapid transmission of neural signals. This neuroanatomy facilitates extremely rapid initiation of escape responses via sensory feedback.

2.3.6 Swimming in Unsteady Flow

While it might seem as though swimming through water with increased or turbulent flow would pose an inherent problem to fishes, in fact, they can gain some energetic advantage by swimming strategically through vortices in water. When objects obstruct flowing water, the water bends around the object and creates vortical flow that sheds in a characteristic pattern (the von Karman street). A series of experiments that swam fishes in flow behind a D-cylinder have demonstrated that, rather than fighting against the structure’s wake, fishes can actually use the regular vortical flow to reduce their energy expenditure, decreasing muscle activity while holding station (Liao 2003, 2002). In fact, slaloming between the vortices that form behind a cylinder is so effective at capturing energy from the flow that even a dead trout, pointing into the flow, can passively “swim” upstream in the wake of a structure (Liao 2004).

2.3.7 Neuro Control

Motor neurons send signals to the muscles to coordinate muscle contraction, which leads to locomotion. The pattern of the motor signals can be the result of a “top-down” signal from the brain and/or rhythmical signals from local central pattern generators (CPGs), both of which can be influenced by sensory feedback experienced by the fish as it swims through its environment. Our understanding of the importance and control of CPGs has improved since the initial descriptions that locomotion may be controlled by the spinal cord (Brown 1914). It is now known that CPGs are responsible for controlling a variety of behaviours, including breathing, chewing, swallowing and locomotion (Garcia-Campmany et al. 2010; Marder and Calabrese 1996). Locomotor CPGs are neural centers found in the spinal cord that can provide rhythmic motor output to the muscles, which is tuned via sensory and top-down input from a heterogeneous environment.

Much of our knowledge of CPG function is from work done on the lamprey (Grillner 1985). The swimming CPGs of the lamprey are along the entire length of the spinal cord, and an isolated spinal cord can produce motor patterns that closely resemble that of an intact lamprey (Cohen and Wallén 1980). This motor pattern is only created in response to an excitatory drive (e.g. brainstem stimulation, sensory stimulation or excitatory amino acids) (Grillner 1985). The presence of CPGs has also been demonstrated in spiny dogfish (Gray and Sand 1936), stingray (Leonard et al. 1979), carp (Kashin et al. 1974) the zebrafish (Downes and Granato 2006; Gabriel et al. 2008). While these CPGs create the intrinsic rhythm of swimming, they need additional input in order to adjust the fish’s behaviour appropriately. Usually, the excitatory drive to turn on the CPGs is provided by the mesencephalic locomotor region (MLR) and passed via the reticulospinal neurons to the spinal CPGs (Grillner et al. 1997). The MLR also receives top-down inputs, such as vision or hearing, from the cerebral cortex (pallium in fishes) (Le Ray et al. 2011; Daghfous et al. 2016). While these inputs historically are poorly characterized, recent work has shed some light on the pathway that carries olfactory information to the MLR. This sensory input appears to be able to influence the MLR output (and thus the resulting locomotor behaviour) in a graded way, thereby fine-tuning an animal’s behaviour (Ménard et al. 2007).

Proprioception in fishes has only recently started to become known, showing clear sensory feedback associated with fin use in fishes (Aiello et al. 2020).

2.4 Amphibious Locomotion in Fishes

2.4.1 Diversity of Terrestrial Locomotion

There are over 200 different species of extant amphibious fishes representing at least 17 genera. The diversity and range of morphological and behavioural phenotypes found among these fishes are large. There are many challenges associated with moving from an aquatic to a terrestrial environment: desiccation, gas exchange, pH balance and disposal of nitrogenous wastes are just a few (Wright and Turko 2016). Each of these affects locomotion indirectly by influencing muscle and tissue performance. Here, we will focus on the impacts a transition from an aquatic to a terrestrial environment has on the locomotor performance of an animal.

The mechanical environments of water and land are very different. Viscosity and drag are the major forces experienced by fishes in water, whereas gravity and friction become the major challenges on land. Fish body and fin function must be flexible in order to produce appropriate forces across environments. Different fishes have different strategies when moving about on land. There are three main categories of fish terrestrial locomotion (Pace and Gibb 2014, 2009): axial-based locomotion, where motion is produced entirely by the body (i.e. snake-like locomotion in elongate ropefish or eel, or jumping locomotion in blennies and rivulus); appendicular-based locomotion, where motion is derived entirely from the fin (i.e. mudskipper); and axial-appendicular-based locomotion, where the animal uses both fins and body to produce thrust (i.e. walking catfish and Polypterus). Some amphibious fishes have totally different strategies, such as climbing perch that use modified opercula to walk (Davenport and Abdulmatin 1990) or the waterfall climbing gobies that use their mouths as suckers to cling to rockfaces under rushing flow (Blob et al. 2006).

Often, fishes exhibit very different behaviours in one environment relative to the other (Pace 2017). For example, fin range of motion increases during walking in both bichir (Polypterus senegalus) and mudskipper (Periophthalmus argentilineatus); however, body oscillation increases for bichir and decreases for mudskipper (Figure 2.8; Standen et al. 2016, 2014; Kawano and Blob 2013). These differences between species illustrate that there are multiple ways to modify strategies for locomotion across environments.

FIGURE 2.8 Aquatic vs. terrestrial locomotion. (a) Polypterus senegalus swimming in water keeps the body relatively straight and uses fins to provide thrust; ventral view. (b) P. senegalus walking on land uses exaggerated body movements and alternating fin plants; dorsal view. (c) Periophthalmus argentilineatus swimming in water incorporates body bending with reduced fin motion; ventral view. (d) P. argentilineatus walking on land keeps body straight, and fins are planted simultaneously; dorsal view. (Panels a and b modified from Standen, E. M., et al., Nature, 513 54–58, 2014; c and d modified from Pace, C. M. and Gibb, A. C., Journal of Experimental Biology, 212, 2279–2286, 2009.)

2.5 Conclusion

Fishes and their broad diversity of form and locomotory function are an excellent example of vertebrate musculoskeletal flexibility. Both from an evolutionary perspective (many thousands of species) and an individual performance perspective (the ability to walk and swim) they provide insight into how to use anatomical form for different and diverse functions. As technological advances increase our ability to quantify animal motion, fishes will continue to provide important animal models to understand and mimic the performance of the natural world.

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