Ariel L. Camp

Muscle shortening underpins most skeletal motion and ultimately animal performance. Most animal muscle generates its greatest mechanical output over a small, homogeneous range of shortening magnitudes and speeds. However, homogeneous muscle shortening is difficult to achieve for swimming fish because the whole body deforms like a bending beam: as the vertebral column flexes laterally, longitudinal muscle strain increases along a medio-lateral gradient. Similar dorsoventral strain gradients have been identified as the vertebral column flexes dorsally during feeding in at least one body location in one fish. If fish bodies also deform like beams during dorsoventral feeding motions, this would suggest the dorsal body (epaxial) muscles must homogenize both dorsoventral and mediolateral strain gradients. We tested this hypothesis by measuring curvature of the anterior vertebral column with XROMM and muscle shortening in 14 epaxial subregions with fluoromicrometry during feeding in rainbow trout (Oncorhynchus mykiss). We compared measured strain with the predicted strain based on beam theory's curvature–strain relationship. Trout flexed the vertebrae dorsally and laterally during feeding strikes, yet when flexion in both planes was included, the strain predicted by beam theory was strongly and significantly correlated with measured strain (P<0.01, R2=0.60). Beam theory accurately predicted strain (slope=1.15, compared with ideal slope=1) across most muscle subregions, confirming that epaxial muscles experience dorsoventral and mediolateral gradients in longitudinal strain. Establishing this deformation–curvature relationship is a crucial step to understanding how these muscles overcome orthogonal strain gradients to produce powerful feeding and swimming behaviours.

Deconstructing motion to better understand it is a key prerequisite in the field of comparative biomechanics. Since Marey and Muybridge's work, technical constraints have been the largest limitation to motion capture and analysis, which, in turn, limited what kinds of questions biologists could ask or answer. Throughout the history of our field, conceptual leaps and significant technical advances have generally worked hand in hand. Recently, high-resolution, three-dimensional (3D) motion data have become easier to acquire, providing new opportunities for comparative biomechanics. We describe how adding a third dimension of information has fuelled major paradigm shifts, not only leading to a reinterpretation of long-standing scientific questions but also allowing new questions to be asked. In this paper, we highlight recent work published in Journal of Experimental Biology and influenced by these studies, demonstrating the biological breakthroughs made with 3D data. Although amazing opportunities emerge from these technical and conceptual advances, high-resolution data often come with a price. Here, we discuss challenges of 3D data, including low-throughput methodology, costly equipment, low sample sizes, and complex analyses and presentation. Therefore, we propose guidelines for how and when to pursue 3D high-resolution data. We also suggest research areas that are poised for major new biological advances through emerging 3D data collection.