skip to main content


Title: They like to move it (move it): walking kinematics of balitorid loaches of Thailand
ABSTRACT Balitorid loaches are a family of fishes that exhibit morphological adaptations to living in fast flowing water, including an enlarged sacral rib that creates a ‘hip’-like skeletal connection between the pelvis and the axial skeleton. The presence of this sacral rib, the robustness of which varies across the family, is hypothesized to facilitate terrestrial locomotion seen in the family. Terrestrial locomotion in balitorids is unlike that of any known fish: the locomotion resembles that of terrestrial tetrapods. Emergence and convergence of terrestrial locomotion from water to land has been studied in fossils; however, studying balitorid walking provides a present-day natural laboratory to examine the convergent evolution of walking movements. We tested the hypothesis that balitorid species with more robust connections between the pelvic and axial skeleton (M3 morphotype) are more effective at walking than species with reduced connectivity (M1 morphotype). We predicted that robust connections would facilitate travel per step and increase mass support during movement. We collected high-speed video of walking in seven balitorid species to analyze kinematic variables. The connection between internal anatomy and locomotion on land are revealed herein with digitized video analysis, μCT scans, and in the context of the phylogenetic history of this family of fishes. Our species sampling covered the extremes of previously identified sacral rib morphotypes, M1 and M3. Although we hypothesized the robustness of the sacral rib to have a strong influence on walking performance, there was not a large reduction in walking ability in the species with the least modified rib (M1). Instead, walking kinematics varied between the two balitorid subfamilies with a generally more ‘walk-like’ behavior in the Balitorinae and more ‘swim-like’ behavior in the Homalopteroidinae. The type of terrestrial locomotion displayed in balitorids is unique among living fishes and aids in our understanding of the extent to which a sacral connection facilitates terrestrial walking.  more » « less
Award ID(s):
1839915
PAR ID:
10379248
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Journal of Experimental Biology
Volume:
225
Issue:
6
ISSN:
0022-0949
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The rheophilic hillstream loaches (Balitoridae) of South and Southeast Asia possess a range of pelvic girdle morphologies, which may be attributed to adaptations for locomotion against rapidly flowing water. Specifically, the connectivity of the pelvic plate (basipterygium) to the vertebral column via a sacral rib, and the relative size and shape of the sacral rib, fall within a spectrum of three discrete morphotypes: long, narrow rib that meets the basipterygium; thicker, slightly curved rib meeting the basipterygium; and robust crested rib interlocking with the basipterygium. Species in this third category with more robust sacral rib connections between the basipterygium and vertebral column are capable of walking out of water with a tetrapod‐like lateral‐sequence, diagonal‐couplet gait. This behavior has not been observed in species lacking direct skeletal connection between the vertebrae and the pelvis. The phylogenetic positions of the morphotypes were visualized by matching the morphological features onto a novel hypothesis of relationships for the family Balitoridae. The morphotypes determined through skeletal morphology were correlated with patterns observed in the pelvic muscle morphology of these fishes. Transitions towards increasingly robust pelvic girdle attachment were coincident with a more anterior origin on the basipterygium and more lateral insertion of the muscles on the fin rays, along with a reduction of the superficial abductors and adductors with more posterior insertions. These modifications are expected to provide a mechanical advantage for generating force against the ground. Inclusion of the enigmatic cave‐adapted balitoridCryptotora thamicolainto the most data‐rich balitorid phylogeny reveals its closest relatives, providing insight into the origin of the skeletal connection between the axial skeleton and basipterygium.

     
    more » « less
  2. ABSTRACT

    The sacrum occupies a functionally important anatomical position as part of the pelvic girdle and vertebral column. Sacral orientation and external morphology in modern humans are distinct from those in other primates and compatible with the demands of habitual bipedal locomotion. Among nonhuman primates, however, how sacral anatomy relates to positional behaviors is less clear. As an alternative to evaluation of the sacrum's external morphology, this study assesses if the sacrum's internal morphology (i.e., trabecular bone) differs among extant primates. The primary hypothesis tested is that trabecular bone parameters with established functional relevance will differ in the first sacral vertebra (S1) among extant primates that vary in positional behaviors. Results for analyses of individual variables demonstrate that bone volume fraction, degree of anisotropy, trabecular number, and size‐corrected trabecular thickness differ among primates grouped by positional behaviors to some extent, but not always in ways consistent with functional expectations. When examined as a suite, these trabecular parameters distinguish obligate bipeds from other positional behavior groups; and, the latter three trabecular bone variables further distinguish knuckle‐walking terrestrial quadrupeds from manual suspensor‐brachiators, vertical clingers and leapers, and arboreal quadrupeds, as well as between arboreal and terrestrial quadrupeds. As in other regions of the skeleton in modern humans, trabecular bone in S1 exhibits distinctively low bone volume fraction. Results from this study of extant primate S1 trabecular bone structural variation provide a functional context for interpretations concerning the positional behaviors of extinct primates based on internal sacral morphology. Anat Rec, 302:1354–1371, 2019. © 2018 Wiley Periodicals, Inc.

     
    more » « less
  3. ABSTRACT

    Many derived aspects of modern human axial skeletal morphology reflect our reliance on obligate bipedal locomotion. Insight into the adaptive significance of features, particularly in the spine, has been gained through experimental studies that induce bipedal standing or walking in quadrupedal mammals. Using an experimental animal model (Rattus norvegicus), the present study builds on earlier work by incorporating additional metrics of the cranium, employing quantitative methods established in the paleoanthropological literature, and exploring how variation in mechanical loading regimes impacts axial anatomy. Rats were assigned to one of five experimental groups, including “fully loaded bipedal walking,” “partially loaded bipedal walking,” “standing bipedally,” “quadrupedal walking,” and “no exercise control,” and engaged in the behavior over 12‐weeks. From μCT data obtained at the beginning and end of the experiment, we measured foramen magnum position and orientation, lumbar vertebral body wedging, cranial surface area of the lumbar and first sacral vertebral bodies, and sacral mediolateral width. Results demonstrate that bipedal rodents generally have more anteriorly positioned foramina magna, more dorsally wedged lumbar vertebrae, greater articular surface areas of lumbar and first sacral vertebral bodies, and sacra that exhibit greater mediolateral widths, compared to quadrupedal rodents. We further document variation among bipedal loading behavior groups (e.g., bipedal standing vs. walking). Our experimental animal model reveals how loading behaviors and adaptations may be specifically linked, and implicates a potential role for developmental plasticity in the evolutionary acquisition of bipedal adaptations in the hominin lineage. Anat Rec, 2018. © 2018 American Association for Anatomy.

     
    more » « less
  4. Fishes exhibit an astounding diversity of locomotor behaviors from classic swimming with their body and fins to jumping, flying, walking, and burrowing. Fishes that use their body and caudal fin (BCF) during undulatory swimming have been traditionally divided into modes based on the length of the propulsive body wave and the ratio of head:tail oscillation amplitude: anguilliform, subcarangiform, carangiform, and thunniform. This classification was first proposed based on key morphological traits, such as body stiffness and elongation, to group fishes based on their expected swimming mechanics. Here, we present a comparative study of 44 diverse species quantifying the kinematics and morphology of BCF-swimming fishes. Our results reveal that most species we studied share similar oscillation amplitude during steady locomotion that can be modeled using a second-degree order polynomial. The length of the propulsive body wave was shorter for species classified as anguilliform and longer for those classified as thunniform, although substantial variability existed both within and among species. Moreover, there was no decrease in head:tail amplitude from the anguilliform to thunniform mode of locomotion as we expected from the traditional classification. While the expected swimming modes correlated with morphological traits, they did not accurately represent the kinematics of BCF locomotion. These results indicate that even fish species differing as substantially in morphology as tuna and eel exhibit statistically similar two-dimensional midline kinematics and point toward unifying locomotor hydrodynamic mechanisms that can serve as the basis for understanding aquatic locomotion and controlling biomimetic aquatic robots. 
    more » « less
  5. Abstract

    Bipedal locomotion over compliant terrain is an important and largely underexplored problem in the robotics community. Although robot walking has been achieved on some non-rigid surfaces with existing control methodologies, there is a need for a systematic framework applicable to different bipeds that enables stable locomotion over various compliant terrains. In this work, a novel energy-based framework is proposed that allows the dynamic locomotion of bipeds across a wide range of compliant surfaces. The proposed framework utilizes an extended version of the 3D dual spring-loaded inverted pendulum (Dual-SLIP) model that supports compliant terrains, while a bio-inspired controller is employed to regulate expected perturbations of extremely low ground-stiffness levels. An energy-based methodology is introduced for tuning the bio-inspired controller to enable dynamic walking with robustness to a wide range of low ground-stiffness one-step perturbations. The proposed system and controller are shown to mimic the vertical ground reaction force (GRF) responses observed in human walking over compliant terrains. Moreover, they succeed in handling repeated unilateral stiffness perturbations under specific conditions. This work can advance the field of biped locomotion by providing a biomimetic method for generating stable human-like walking trajectories for bipedal robots over various compliant surfaces. Furthermore, the concepts of the proposed framework could be incorporated into the design of controllers for lower-limb prostheses with adjustable stiffness to improve their robustness over compliant surfaces.

     
    more » « less