A gyroscopic advantage: phylogenetic patterns of compensatory movements in frogs

Abstract

Head and eye compensatory movements known as vestibulo-ocular and vestibulo-cervical reflexes are essential to stay orientated in space while moving. We have used a previously developed methodology focused on the detailed mathematical description of head compensatory movements in frogs without the need for any surgical procedures on the examined specimens. Our comparative study comprising 35 species of frogs from different phylogenetic backgrounds revealed species-specific head compensatory abilities ensuring gaze stabilization. Moreover, we found a strong phylogenetic signal highlighting the great ability of compensatory head movements in families of Pyxicephalidae and Rhacophoridae from the Natatanura group. By contrast, families of Dendrobatidae and Microhylidae exhibited only poor or no head compensatory movements. Contrary to our expectation, the results did not corroborate an ecomorphological hypothesis anticipating a close relationship between ecological parameters and the head compensatory movements. We did not find any positive association between more complex (3D structured, arboreal or aquatic) habitats or more saltatory behavior and elevated abilities of head compensatory movements. Moreover, we found compensatory movements in most basal Archeobatrachia, giving an indication of common ancestry of these abilities in frogs that are variously pronounced in particular families. We hypothesize that the uncovered proper gaze stabilization during locomotion provided by the higher head compensatory abilities can improve or even enable visual perception of the prey. We interpret this completely novel finding as a possible gyroscopic advantage in a foraging context. We discuss putative consequences of such advanced neuromotor skills for diversification and ecological success of the Natatanura group.