Integrating morphology andin vivoskeletal mobility with digital models to infer function in brittle star arms

Abstract

Brittle stars (Phylum Echinodermata, Class Ophiuroidea) have evolved rapid locomotion employing muscle and skeletal elements within their (usually) five arms to apply forces in a manner analogous to that of vertebrates. Inferring the inner workings of the arm has been difficult as the skeleton is internal and many of the ossicles are sub‐millimeter in size. Advances in 3D visualization and technology have made the study of movement in ophiuroids possible. We developed six virtual 3D skeletal models to demonstrate the potential range of motion of the main arm ossicles, known as vertebrae, and six virtual 3D skeletal models of non‐vertebral ossicles. These models revealed the joint center and relative position of the arm ossicles during near‐maximal range of motion. The models also provide a platform for the comparative evaluation of functional capabilities between disparate ophiuroid arm morphologies. We made observations on specimens of Ophioderma brevispina and Ophiothrix angulata. As these two taxa exemplify two major morphological categories of ophiuroid vertebrae, they provide a basis for an initial assessment of the functional consequences of these disparate vertebral morphologies. These models suggest potential differences in the structure of the intervertebral articulations in these two species, implying disparities in arm flexion mechanics. We also evaluated the differences in the range of motion between segments in the proximal and distal halves of the arm length in a specimen of O. brevispina, and found that the morphology of vertebrae in the distal portion of the arm allows for higher mobility than in the proximal portion. Our models of non‐vertebral ossicles show that they rotate further in the direction of movement than the vertebrae themselves in order to accommodate arm flexion. These findings raise doubts over previous hypotheses regarding the functional consequences of ophiuroid arm disparity. Our study demonstrates the value of integrating experimental data and visualization of articulated structures when making functional interpretations instead of relying on observations of vertebral or segmental morphology alone. This methodological framework can be applied to other ophiuroid taxa to enable comparative functional analyses. It will also facilitate biomechanical analyses of other invertebrate groups to illuminate how appendage or locomotor function evolved.

Morphology, shape variation and movement of skeletal elements in starfish (Asterias rubens)

“…These data could be used to model the interaction of all ossicle types during ray movement using 3D‐printed models or multibody simulations. For brittle stars ( Ophiuroidea ), promising methods for measuring the range of motion, creating 3D models from ossicle scans and quantifying joint flexions of ossicles, have been shown (Clark et al., ). Finally, a comparative study examining the skeleton of brittle stars would be of great interest, as their rays are even more flexible than in Asteroidea and contain more muscles because the rays are being used for locomotion (Ruppert et al., ; Okanishi et al., ).…”

<strong>Ophiuroid locomotion from fundamental structures to integrated systems</strong>

“…The arms of living ophiuroids, the primary units involved in locomotion, are made of repeating segments. Most extant ophiuroid arm segments consist of five main ossicles: the vertebra, a dorsal plate, a ventral plate, and two laterals (Clark et al 2018, Figure 1). The vertebra lies in the center flanked by the other plates.…”

“…There has been debate over whether or not the shape of the vertebrae is significant functionally (Litvinova 1994;LeClair & LaBarbera 1997). A novel framework utilizing 3D imaging and digital modeling has been developed to analyze the relationship between morphology and function of the skeletal elements of the ophiuroid arm (Clark et al 2018). Unlike scanning electron microscopy, the most widely used method for imaging ophiuroid ossicles, micro-CT imaging is non-destructive and allows for visualization of the ossicle in three dimensions, the surface structure in 360°, and the articulations between successive ossicles.…”

Arm waving in stylophoran echinoderms: three-dimensional mobility analysis illuminates cornute locomotion

“…The locomotory capabilities of stylophorans have typically been reconstructed by assigning functional attributes to specific morphological features [ 5 – 7 , 13 – 15 ]. However, evidence suggests that disparate morphological features in living echinoderms do not necessarily reflect a difference in function [ 16 ]: functional capabilities cannot be determined based on qualitative aspects alone. Biomechanical modelling of digitized fossil specimens has been used to calculate range of motion and analyse locomotion in extinct vertebrates [ 17 – 18 ].…”