Congruence between muscle activity and kinematics in a convergently derived prey-processing behavior

Quantification of anatomical and physiological characteristics of the function of a musculoskeletal system may yield a detailed understanding of how the organizational levels of morphology, biomechanics, kinematics, and muscle activity patterns (MAPs) influence behavioral diversity. Using separate analyses of these organizational levels in representative study taxa, we sought patterns of congruence in how organizational levels drive behavioral modulation in a novel raking prey-processing behavior found in teleosts belonging to two evolutionarily distinct lineages. Biomechanically divergent prey (elusive, robust goldfish and sedentary, malleable earthworms) were fed to knifefish, Chitala ornata (Osteoglossomorpha) and brook trout, Salvelinus fontinalis (Salmoniformes). Electromyography recorded MAPs from the hyoid protractor, jaw adductor, sternohyoideus, epaxialis, and hypaxialis musculature, while sonomicrometry sampled deep basihyal kinesis and contractile length dynamics in the basihyal protractor and retractor muscles. Syntheses of our results with recent analyses of cranial morphology and raking kinematics showed that raking in Salvelinus relies on an elongated cranial out lever, extensive cranial elevation and a curved cleithrobranchial ligament (CBL), and that both raking MAPs and kinematics remain entirely unmodulateda highly unusual trait, particularly among feeding generalists. Chitala had a shorter CBL and a raking power stroke involving increased retraction of the elongated pectoral girdle during raking on goldfish. The raking MAP was also modulated in Chitala, involving an extensive overlap between muscle activity of the preparatory and power stroke phases, driven by shifts in hypaxial timing and recruitment of the hyoid protractor muscle. Sonomicrometry revealed that the protractor hyoideus muscle stored energy from retraction of the pectoral girdle for ca. 520 ms after onset of the power stroke and then hyper-extended. This mechanism of elastic recoil in Chitala, which amplifies retraction of the basihyal during raking on goldfish without a significant increase in recruitment of the hypaxialis, suggests a unique mechanism of modulation based on performance-enhancing changes in the design and function of the musculoskeletal system.