Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology, and phylogeny

Many studies of feeding behavior have implanted electrodes unilaterally (in muscles on only one side of the head) to determine the basic motor patterns of muscles controlling the jaws. However, bilateral implantation has the potential to achieve a more comprehensive understanding of modification of the motor activity that may be occurring between the left and right sides of the head. In particular, complex processing of prey is often characterized by bilaterally asynchronous and even unilateral activation of the jaw musculature. In this study, we bilaterally implant feeding muscles in species from four orders of elasmobranchs (Squaliformes, Orectolobiformes, Carcharhiniformes, Rajoidea) in order to characterize the effects of type of prey, feeding behavior, and phylogeny on the degree of asynchronous muscle activation. Electrodes were implanted in three of the jaw adductors, two divisions of the quadratomandibularis and the preorbitalis, as well as in a cranial elevator in sharks, the epaxialis. The asynchrony of feeding events (measured as the degree to which activity of members of a muscle pair is out of phase) was compared across species for capture versus processing and simple versus complex prey, then interpreted in the contexts of phylogeny, morphology, and ecology to clarify determinants of asynchronous activity. Whereas capture and processing of prey were characterized by statistically similar degrees of asynchrony for data pooled across species, events involving complex prey were more asynchronous than were those involving simple prey. The two trophic generalists, Squalus acanthias and Leucoraja erinacea, modulated the degree of asynchrony according to type of prey, whereas the two behavioral specialists, Chiloscyllium plagiosum and Mustelus canis, activated the cranial muscles synchronously regardless of type of prey. These differences in jaw muscle activity would not have been detected with unilateral implantation. Therefore, we advocate bilateral implantation in studies of cranial muscle function in fishes, particularly when investigating behaviors associated with processing complex prey. Incorporating this methodology will provide a more detailed understanding of the coordination and evolution of paired-muscle function in the feeding apparatus relative to behavioral and ecological performance.