Tadpole Locomotion: Axial Movement and Tail Functions in a Largely Vertebraeless Vertebrate

SYNOPSIS.Tadpoles are exceptional among vertebrates in lackingvertebrae along most of their body axis. Their caudal myotomesare also unusually simple for free-living vertebrates. Thisoverall morphological simplicity, in theory, makes tadpolesgood models for exploring how vertebrates control undulatorymovements. We used electromyography (EMG), high speed ciné,computational fluid dynamics (CFD), and mechanical tissue testingto understand how Rana tadpoles regulate their locomotion. Bullfrog (Rana catesbeiana) tadpoles have several patterns ofmuscle activity, each specific to a particular swimming behavior.Ipsilateral muscles in the tail were active either in seriesor simultaneously, depending on the tadpole's velocity, andlinear and angular acceleration. When R. catesbeiana larvaeswam at their natural preferred tail beat frequency, musclesat the caudal end of their tail were inactive. Mechanical testsof tissue further suggest that the preferred tail beat frequencyclosely matches the resonance frequency of the tail thus minimizingthe energetic cost of locomotion. CFD modeling has demonstrated that the characteristically highamplitude oscillations at a tadpole's snout during normal rectilinearlocomotion do not add to drag, as might be supposed, but ratherhelp generate thrust. Mechanical testing of the tadpole tailfin has revealed that the fin is viscoelastic and stiffer insmall rather than large deformations. This property (among others)allows the tail to be light and flexible, yet stiff enough togenerate thrust in the absence of a bony or cartilaginous skeleton. Many recent studies have documented predator-induced polyphenismin tadpole tail shape. We suggest that this developmental plasticityin locomotor structures is more common in tadpoles than in othervertebrates because tadpoles do not need to reform skeletaltissue to change overall caudal shape. Tadpole tail fins and tip, in the absence of any skeleton, arefragile and often scarred by predators. Based on the high incidenceof tail fin injury seen in tadpoles in the wild, we suggestthat the tadpole tail fin and tip may play an ecological rolethat goes beyond serving as a propeller to help tadpoles staybeyond predators' reach. Those soft tissue axial structures,by failing under very small tensile loads, may also allow tadpolesto tear free of a predator's grasp.