Terrestrial force production by the limbs of a semi-aquatic salamander provides insight into the evolution of terrestrial locomotor mechanics

Abstract

Amphibious fishes and salamanders are valuable functional analogs for vertebrates that spanned the water-to-land transition. However, investigations of walking mechanics have focused on terrestrial salamanders and, thus, may better reflect the capabilities of stem tetrapods that were already terrestrial. The earliest tetrapods were aquatic, so salamanders that are not primarily terrestrial may yield more appropriate data for modelling the incipient stages of terrestrial locomotion. In the present study, locomotor biomechanics were quantified from semi-aquatic Pleurodeles waltl, a salamander that spends most of its adult life in water, and then compared to a primarily terrestrial salamander (Ambystoma tigrinum) and semi-aquatic fish (Periophthalmus barbarus) to evaluate whether walking mechanics show greater similarity between species with ecological versus phylogenetic similarities. Ground reaction forces (GRFs) from individual limbs or fins indicated that the pectoral appendages of each taxon had distinct patterns of force production, but hind limb forces were comparable between the salamanders. The rate of force development ( yank) was sometimes slower in P. waltl but generally comparable between the three species. Finally, medial inclination of the GRF in P. waltl was intermediate between semi-aquatic fish and terrestrial salamanders, potentially elevating bone stresses among more aquatic taxa as they move on land. These data provide a framework for modelling stem tetrapods using an earlier stage of quadrupedal locomotion that was powered primarily by the hind limbs (i.e., "rear-wheel drive"), and reveal mechanisms for appendages to generate propulsion in three locomotor strategies that are presumed to have occurred across the water-to-land transition in vertebrate evolution. Summary statementSemi-aquatic salamanders had limb mechanics that were intermediate in magnitude yet steadier than the appendages of terrestrial salamanders and semi-aquatic fish, providing a framework to model semi-aquatic early tetrapods.