Encyclopedia of Animal Cognition and Behavior

Living Edition
| Editors: Jennifer Vonk, Todd Shackelford

Caudata Locomotion

  • Aleksander B. Sawiec
  • Dan E. Gibbons
  • Peter Gagliano
  • Michael C. GranatoskyEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-47829-6_1005-1



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

Caudata locomotion can be broken down broadly into terrestrial and aquatic movement (Duellman and Trueb 1994; Karakasiliotis et al. 2016; Stebbins and Cohen 1997) (Fig. 1). Terrestrial gaits in the Caudata are highly variable and characterized by considerable variation in both limb-loading (Granatosky et al. 2020) and timing (Ross et al. 2013). All terrestrial Caudata locomotion involve symmetrical lateral-sequence walking gaits in which each hindlimb footfall is followed by an ipsilateral forelimb footfall (i.e., right hindlimb, right forelimb, left hindlimb, left forelimb) (Fig. 2). Commonly, during walking gaits the forelimbs and hindlimbs are traveling together as a slightly asynchronous couplet. When the contralateral forelimbs and hindlimbs are traveling together, this is referred to as a diagonal couplet. Very rarely do the limbs move together in perfect synchrony (Cartmill et al. 2002; Granatosky 2018). All the Caudata use a lateral-sequence diagonal-couplet footfall patterns (Karakasiliotis et al. 2016; Nyakatura et al. 2019; Reilly et al. 2006). This footfall sequence is inherently quite stable due to the generally low proportion of the stride spent as a unilateral bipod (~22%), and the relatively high proportion spent as a diagonal bipod (only two contralateral limbs in contact with the support) and large tripod (three widely splayed limbs in contact with the support).
Fig. 1

The Caudata are primarily restricted to (a) terrestrial and (b) aquatic quadrupedal gaits and (c) undulatory swimming. Biologically accurate (d) bio-inspired robotics have been developed to replicate and further understand Caudata locomotor patterns

Fig. 2

“Hildebrand” plot displaying diagonality against hindlimb duty factor collected during quadrupedal walking in Caudata (n = 14 species)

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.



  1. Andersson, O., Forssberg, H., Grillner, S., & Wallen, P. (1981). Peripheral feedback mechanisms acting on the central pattern generators for locomotion in fish and cat. Canadian Journal of Physiology and Pharmacology, 59(7), 713–726.CrossRefGoogle Scholar
  2. Ashley-Ross, M. (1994). Hindlimb kinematics during terrestrial locomotion in a salamander (Dicamptodon tenebrosus). Journal of Experimental Biology, 193(1), 255–283.PubMedGoogle Scholar
  3. Ashley-Ross, M. A., Lundin, R., & Johnson, K. L. (2009). Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 311A(4), 240–257.  https://doi.org/10.1002/jez.522.CrossRefGoogle Scholar
  4. Cartmill, M., Lemelin, P., & Schmitt, D. (2002). Support polygons and symmetricalgaits in mammals. Zoological Journal of the Linnean Society, 136(3), 401–420.  https://doi.org/10.1046/j.1096-3642.2002.00038.x.CrossRefGoogle Scholar
  5. Duellman, W. E., & Trueb, L. (1994). Biology of amphibians. JHU Press.Google Scholar
  6. Frolich, L. M., & Biewener, A. A. (1992). Kinematic and Electromyographic analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. Journal of Experimental Biology, 162(1), 107–130.Google Scholar
  7. Gillis, G. (1997). Anguilliform locomotion in an elongate salamander (Siren intermedia): Effects of speed on axial undulatory movements. Journal of Experimental Biology, 200(4), 767–784.PubMedGoogle Scholar
  8. Girling, S. J. (2013). Basic reptile and amphibian anatomy and physiology. In Veterinary nursing of exotic pets (pp. 245–265). Wiley.  https://doi.org/10.1002/9781118782941.ch17.
  9. Golubitsky, M., Stewart, I., Pietro-Luciano, B., & Collins, J. J. (1999). Symmetry in locomotor central pattern generators and animal gaits. Nature, 401(6755), 731–731.  https://doi.org/10.1038/44416.CrossRefGoogle Scholar
  10. Granatosky, M. C. (2018). Quadrupedal. In J. Vonk & T. Shackelford (Eds.), Encyclopedia of animal cognition and behavior (pp. 1–6). Springer International Publishing.  https://doi.org/10.1007/978-3-319-47829-6_1442-1.
  11. Granatosky, M. C., Bryce, C. M., Hanna, J., Fitzsimons, A., Laird, M. F., Stilson, K., Wall, C. E., & Ross, C. F. (2018). Inter-stride variability triggers gait transitions in mammals and birds. Proceedings of the Royal Society B, 285.  https://doi.org/10.1098/rspb.2018.1766.
  12. Granatosky, M. C., McElroy, E. J., Lemelin, P., Reilly, S. M., Nyakatura, J. A., Andrada, E., Kilbourne, B. M., Allen, V. R., Butcher, M. T., Blob, R. W., & Ross, C. F. (2020). Variation in limb loading magnitude and timing in tetrapods. The Journal of Experimental Biology, 223(Pt 2).  https://doi.org/10.1242/jeb.201525.
  13. Grillner, S. (1975). Locomotion in vertebrates: Central mechanisms and reflex interaction. Physiological Reviews, 55(2), 247–304.CrossRefGoogle Scholar
  14. Grillner, S., & Zangger, P. (1975). How detailed is the central pattern generation for locomotion? Brain Research, 88(2), 367–371.CrossRefGoogle Scholar
  15. Guertin, P. A. (2009). The mammalian central pattern generator for locomotion. Brain Research Reviews, 62(1), 45–56.  https://doi.org/10.1016/j.brainresrev.2009.08.002.CrossRefPubMedGoogle Scholar
  16. Harischandra, N., Knuesel, J., Kozlov, A., Bicanski, A., Cabelguen, J.-M., Ijspeert, A. J., & Ekeberg, Ö. (2011). Sensory feedback plays a significant role in generating walking gait and in gait transition in salamanders: A simulation study. Frontiers in Neurorobotics, 5, 3.CrossRefGoogle Scholar
  17. Hoff, K. V. S., Huq, N., King, V. A., & Wassersug, R. J. (1989). The kinematics of larval salamander swimming (Ambystomatidae: Caudata). Canadian Journal of Zoology, 67(11), 2756–2761.  https://doi.org/10.1139/z89-391.CrossRefGoogle Scholar
  18. Ijspeert, A. J. (2008). Central pattern generators for locomotion control in animals and robots: A review. Neural Networks : The Official Journal of the International Neural Network Society, 21(4), 642–653.  https://doi.org/10.1016/j.neunet.2008.03.014.CrossRefGoogle Scholar
  19. Ijspeert, A. J., & Cabelguen, J.-M. (2006). Gait transition from swimming to walking: Investigation of salamander locomotion control using nonlinear oscillators. In H. Kimura, K. Tsuchiya, A. Ishiguro, & H. Witte (Eds.), Adaptive motion of animals and machines (pp. 177–188). Springer.  https://doi.org/10.1007/4-431-31381-8_16.
  20. Ijspeert, A. J., Crespi, A., Ryczko, D., & Cabelguen, J.-M. (2007). From swimming to walking with a salamander robot driven by a spinal cord model. Science, 315(5817), 1416–1420.  https://doi.org/10.1126/science.1138353.CrossRefPubMedGoogle Scholar
  21. Karakasiliotis, K. (2013). Legged locomotion with spinal undulations. EPFL.Google Scholar
  22. Karakasiliotis, K., Schilling, N., Cabelguen, J.-M., & Ijspeert, A. J. (2013). Where are we in understanding salamander locomotion: Biological and robotic perspectives on kinematics. Biological Cybernetics, 107(5), 529–544.  https://doi.org/10.1007/s00422-012-0540-4.CrossRefPubMedGoogle Scholar
  23. Karakasiliotis, K., Thandiackal, R., Melo, K., Horvat, T., Mahabadi, N. K., Tsitkov, S., Cabelguen, J. M., & Ijspeert, A. J. (2016). From cineradiography to biorobots: An approach for designing robots to emulate and study animal locomotion. Journal of the Royal Society Interface, 13(119), 20151089.  https://doi.org/10.1098/rsif.2015.1089.CrossRefPubMedCentralGoogle Scholar
  24. Kiehn, O., & Butt, S. J. B. (2003). Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Progress in Neurobiology, 70(4), 347–361.  https://doi.org/10.1016/S0301-0082(03)00091-1.CrossRefPubMedGoogle Scholar
  25. Knüsel, J., Bicanski, A., Ryczko, D., Cabelguen, J.-M., & Ijspeert, A. J. (2013). A Salamander’s flexible spinal network for locomotion, modeled at two levels of abstraction. Integrative and Comparative Biology, 53(2), 269–282.  https://doi.org/10.1093/icb/ict067.CrossRefPubMedGoogle Scholar
  26. Nyakatura, J. A., Melo, K., Horvat, T., Karakasiliotis, K., Allen, V. R., Andikfar, A., Andrada, E., Arnold, P., Lauströer, J., Hutchinson, J. R., Fischer, M. S., & Ijspeert, A. J. (2019). Reverse-engineering the locomotion of a stem amniote. Nature, 565(7739), 351.  https://doi.org/10.1038/s41586-018-0851-2.CrossRefPubMedGoogle Scholar
  27. Reilly, S. M., McElroy, E. J., Odum, R. A., & Hornyak, V. A. (2006). Tuataras and salamanders show that walking and running mechanics are ancient features of tetrapod locomotion. Proceedings of the Royal Society of London B: Biological Sciences, 273(1593), 1563–1568.  https://doi.org/10.1098/rspb.2006.3489.CrossRefGoogle Scholar
  28. Ross, C. F., Blob, R. W., Carrier, D. R., Daley, M. A., Deban, S. M., Demes, B., Gripper, J. L., Iriarte-Diaz, J., Kilbourne, B. M., Landberg, T., Polk, J. D., Schilling, N., & Vanhooydonck, B. (2013). The evolution of locomotor rhythmicity in Tetrapods. Evolution, 67(4), 1209–1217.  https://doi.org/10.1111/evo.12015.CrossRefPubMedGoogle Scholar
  29. Stebbins, R. C., & Cohen, N. W. (1997). A natural history of amphibians. Princeton University Press.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Aleksander B. Sawiec
    • 1
  • Dan E. Gibbons
    • 2
  • Peter Gagliano
    • 3
  • Michael C. Granatosky
    • 2
    Email author
  1. 1.Department of Mechanical EngineeringNew York Institute of TechnologyOld WestburyUSA
  2. 2.Department of AnatomyNew York Institute of TechnologyOld WestburyUSA
  3. 3.Department of Electrical and Computer EngineeringNew York Institute of TechnologyOld WestburyUSA

Section editors and affiliations

  • Khalil Iskarous
    • 1
  1. 1.University of Southern CaliforniaLos AngelesUSA