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Movement used by salamanders to traverse their environment.
The Caudata are amphibians that generally show the basal tetrapod body plan. They are lizard-like in appearance with slender bodies and short limbs (Girling 2013). They tend to have four toes on the forelimb and five on the hindlimb. Some fully aquatic species, like sirens and amphiumas, have reduced or absent hindlimbs. Like all amphibians, the Caudata have a distinct larval and adult stage. They have permeable skin that usually makes them reliant on habitats in or near water or other cool, damp places. Some salamander species are fully aquatic throughout their lives, while others take to the water intermittently, and others are entirely terrestrial as adults (Duellman and Trueb 1994; Stebbins and Cohen 1997).
Major Locomotor Modes
Literature on gait transitions (a speed related switch from walking to running) in Caudata is scant and it does not appear that the Caudata can adopt asymmetrical running gaits (e.g., gallop or bound). Experiments on tiger salamanders reveal that gait transitions are not visually detectable based on limb phase definitions (Reilly et al. 2006). It is the case though that if one bases the definition of a gait transition off of center of mass movements rather than limb phase definitions then both walking and running center of mass movements are present (Reilly et al. 2006). However, the use of these walking and running center of mass movements are not speed dependent (Reilly et al. 2006) and therefore are not synonymous with the gait transitions observed in birds and mammals (Granatosky et al. 2018).
Unlike mammals and birds, Caudata locomotion is characterized by a sprawling posture (Ashley-Ross 1994; Ashley-Ross et al. 2009; Karakasiliotis et al. 2013; Nyakatura et al. 2019). Sprawling postures are those in which the humerus and femur cannot attain an orientation with their long axes vertically directed. Limb movements during sprawling gaits are complex and limb posture changes considerably during a stride cycle. Rather than moving in a fore-aft arc underneath the body, the humerus and femur move backwards, outwards and downwards during stance phase. For sprawling Caudata, the highly abducted limb and lateral rotation of the zeugopod relative to the autopod results in a kinematic arrangement in which the ankle and wrist flexor musculature are not in line with the travel path at the end of stance phase (Ashley-Ross 1994; Karakasiliotis et al. 2016; Nyakatura et al. 2019).
Lateral body undulation plays an important part in Caudata locomotion and is integrated with limb movement (Karakasiliotis 2013). Standing wave patterns, where points of no lateral bending nodes alternate with areas of maximal bending internodes, are clearly present during terrestrial walking (Karakasiliotis et al. 2016; Nyakatura et al. 2019). At the start of a stride, the trunk between the forelimb and hindlimb is maximally displaced to one side, although lateral trunk displacement is substantially less than during aquatic swimming (see below), while the neck, head, tail are maximally displaced in the opposite direction. About halfway into the cycle, the trunk bends maximally in the opposite direction, forming a mirror image of the start of the cycle. Hence, during terrestrial walking, the body axis forms a single standing arc that undergoes one full oscillation during a locomotor cycle (Frolich and Biewener 1992).
The Caudata larval stage is entirely aquatic. Like the adults, these larvae have relatively elongate slender bodies making them closer in appearance to certain fishes rather than the short globular anuran tadpoles (Frolich and Biewener 1992; Hoff et al. 1989). Also, they are ambush predators like many fishes rather than herbivores like tadpoles (Hoff et al. 1989; Stebbins and Cohen 1997). However, Caudata larvae have exposed gills and well-developed limbs throughout most of their larval stage that distinguish them from fishes, and these limbs interfere with their swimming performance. In general, salamander larvae do not swim in a straight path at a constant velocity nearly as effectively as either tadpoles or fishes. They have far greater maximum amplitude at high swimming speeds, and far less anterior stability. The drag induced by exposed gills and limbs may account in part for the inferior performance of the salamanders (Hoff et al. 1989). The Caudata larvae are designed for movement among the rocks and vegetation of the substrate, and for high acceleration over short distances, such as those used during a lunge at prey (Duellman and Trueb 1994; Stebbins and Cohen 1997).
For adults, aquatic locomotion involves both walking and swimming gaits (Ashley-Ross et al. 2009; Frolich and Biewener 1992; Stebbins and Cohen 1997). Kinematics of aquatic walking appear to be largely similar to what is observed on land (Ashley-Ross et al. 2009). Therefore, this chapter will not discuss these gait kinematics in further detail. However, swimming represents a substantially differing motor pattern (Ashley-Ross et al. 2009; Frolich and Biewener 1992; Ijspeert and Cabelguen 2006; Karakasiliotis et al. 2016; Karakasiliotis et al. 2013). During swimming, individuals tuck arms and legs close to the body and use a traveling wave of lateral undulation (Ashley-Ross et al. 2009; Frolich and Biewener 1992; Ijspeert and Cabelguen 2006; Karakasiliotis et al. 2016). The propagation of this traveling wave can be clearly seen by the timing of maximal lateral displacements along the length of the trunk during a locomotor cycle. Maximal lateral displacements of the trunk tend to be dramatically higher during swimming compared to either terrestrial or aquatic walking. As the locomotor cycle begins, a wave of maximal lateral displacement is initiated on the right side near the shoulder girdle. This wave then travels with a constant velocity down the right side of the animal. As the locomotor cycle progresses, this right-side wave reaches a position posterior to the forelimbs and a new wave is initiated on the left side. As the next locomotor cycle begins, the first right-side wave is at the base of the tail, the left-side wave has reached the anterior region of the trunk, and a new wave is initiated on the right side. This pattern is repeated with waves passing alternately down the right and left sides of the animal (Frolich and Biewener 1992). As a result, the body axis is always thrown into an S-shaped curve that travels down the animal. Some Caudata species, such as sirens and amphiumas, have reduced or absent hindlimbs and become fully aquatic. As such, this undulatory locomotor mode is their primary means of movement (Gillis 1997).
Influence of Caudata Locomotion on Neuromechanics and Bio-inspired Robotics
Caudata locomotion has served as a model system for understanding the function of central pattern generators (CPGs), which are networks of neural circuitry that receive a single input signal and output a cyclical or rhythmic motor command in response. Locomotor CPGs generate from within the spinal cord as opposed to the brain (Andersson et al. 1981; Golubitsky et al. 1999; Kiehn and Butt 2003) and are found in nearly all vertebrate species (Golubitsky et al. 1999; Grillner and Zangger 1975; Grillner 1975; Guertin 2009). These neural networks result in rhythmic activities such as walking, running, swimming, and even chewing. Activation of salamander CPGs display rhythmic movements in both walking, trotting, and swimming as muscle activation travels from head to tail and between the left and right sides of the body (Ijspeert 2008; Ijspeert and Cabelguen 2006; Karakasiliotis et al. 2013; Knüsel et al. 2013). Sensory feedback in salamanders are instrumental for gait transition dynamics, where proprioceptive sensory inputs were essential for walking gait sequences, as opposed to trotting gait sequences which rely more on central CPG influence (Harischandra et al. 2011). Gait transition between the two may be induced by increasing activity of the descending drive originating from the mesencephalic locomotor region and can be aided by sensory inputs at the forelimb and hindlimb regions of the spinal cord. Progressively increasing the drive signal from a frequency of about 5 Hz to 20 Hz in mechanical models of salamanders with artificial mesencephalic locomotor regions has been shown to result in a transition from walking to swimming (Ijspeert et al. 2007).
The information derived from salamander CPGs has served as the foundation to develop bio-inspired salamander robots (Fig. 1). Most notable is Pleruobot developed by Karakasiliotis et al. (2016) to model the terrestrial and aquatic locomotor mechanics of the Iberian ribbed newt (Pleurodeles waltl). Pleurobot’s kinematics and anatomical scaling were inspired from biplanar cineradiography and high resolution micro computed tomography. Through these data, the degrees of freedom of the live animal’s musculoskeletal system were reduced in complexity to only the most essential and influential connections and joints. As a result, Pleurobot can achieve biological accurate terrestrial and aquatic locomotor mechanics with only 27° of freedom distributed throughout the spine, limbs, and two free unactuated joints (Ijspeert et al. 2007; Karakasiliotis et al. 2016).
Beyond just accurately recreating the locomotor movement and timing of Iberian ribbed newts, Pleurobot has been designed in a manner to replicate a functioning CPG (Harischandra et al. 2011; Ijspeert 2008; Ijspeert et al. 2007; Knüsel et al. 2013). From live-animal experiments, limb and spine kinematics were coded into the CPG and sent to the servomotors powering Pleurobot (Karakasiliotis et al. 2016). Pleurobot’s CPG has served a vital role in coordinating timing, efficiency, and accuracy of servomotor movements using incremental continuous rather than discreate input stimuli (Ijspeert 2008). Such a system allows Pleurobot to make gait transitions between terrestrial and aquatic mediums (Ijspeert and Cabelguen 2006), while maintaining biologically relevant internal and external limb forces, joint kinematics, and spatiotemporal gait characteristics (Karakasiliotis et al. 2016). Bio-inspired robotics allows researchers to alter aspects of the anatomy and motor control and directly assess how these changes alter overall system performance. Such manipulation is not possible with living animals.
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