Propulsive Forces of Mudskipper Fins and Salamander Limbs during Terrestrial Locomotion: Implications for the Invasion of Land

Abstract

The invasion of land was a pivotal event in vertebrate evolution that was associated with major appendicular modifications. Although fossils indicate that the evolution of fundamentally limb-like appendages likely occurred in aquatic environments, the functional consequences of using early digited limbs, rather than fins, for terrestrial propulsion have had little empirical investigation. Paleontological and experimental analyses both have led to the proposal of an early origin of "hind limb-driven" locomotion among tetrapods or their ancestors. However, the retention of a pectoral appendage that had already developed terrestrial adaptations has been proposed for some taxa, and few data are available from extant functional models that can provide a foundation for evaluating the relative contributions of pectoral and pelvic appendages to terrestrial support among early stem tetrapods. To examine these aspects of vertebrate locomotor evolution during the invasion of land, we measured three-dimensional ground reaction forces (GRFs) produced by isolated pectoral fins of mudskipper fishes (Periophthalmus barbarus) during terrestrial crutching, and compared these to isolated walking footfalls by the forelimbs and hind limbs of tiger salamanders (Ambystoma tigrinum), a species with subequally-sized limbs that facilitate comparisons to early tetrapods. Pectoral appendages of salamanders and mudskippers exhibited numerous differences in GRFs. Compared with salamander forelimbs, isolated fins of mudskippers bear lower vertical magnitudes of GRFs (as a proportion of body weight), and had GRFs that were oriented more medially. Comparing the salamanders' forelimbs and hind limbs, although the peak net GRF occurs later in stance for the forelimb, both limbs experience nearly identical mediolateral and vertical components of GRF, suggesting comparable contributions to support. Thus, forelimbs could also have played a significant locomotor role among basal tetrapods that had limbs of sub-equal size. However, the salamander hind limb and mudskipper pectoral fin had a greater acceleratory role than did the salamander forelimb. Together, data from these extant taxa help to clarify how structural change may have influenced locomotor function through the evolutionary invasion of land by vertebrates.

Comparative limb bone loading in the humerus and femur of the tiger salamander Ambystoma tigrinum: testing the ‘mixed-chain’ hypothesis for skeletal safety factors

“…Bone-loading mechanics were analyzed for adult, male tiger salamanders (Ambystoma tigrinum Green 1825) used in a analog for coefficient of determination for LMMs previous study on GRF production (Kawano and Blob, 2013). Two trials from this earlier study were excluded herein because they generated unrealistic estimates of bone stress (e.g.…”

“…Methods for collecting synchronized 3D kinematic and kinetic data for salamanders have been documented (Kawano and Blob, 2013;, but are summarized with additional details herein. Dorsal and lateral views of animals walking across a custom-built, multi-axis force platform (K&N Scientific, Guilford, VT, USA) were recorded at 100 Hz with digitally synchronized high-speed digital video cameras (Phantom v4.1, Vision Research Inc., Wayne, NJ, USA).…”

“…A 4×9 cm aluminium insert reduced the contact area of the platform, facilitating data collection from isolated limbs (see fig. 1 of Kawano and Blob, 2013). The platform was covered with shelf liner to prevent damage to the salamander's skin.…”

“…Although hindlimbs provide the primary propulsion in many non-mammalian quadrupeds, forelimbs still make important contributions to locomotion (Kawano and Blob, 2013;Nyakatura et al, 2014), and loss of locomotor function may be more detrimental for the forelimb. Early work on salamander locomotion (Evans, 1946) demonstrated that forward propulsion could be achieved solely by the forelimbs but not the hindlimbs, suggesting that the forelimbs play a more important locomotor role than passive body support (at least in terrestrial salamanders such as Taricha and Ambystoma).…”

“…Through our tests of the 'mixed-chain' hypothesis of SFs between salamander limb bones, we evaluated (1) whether the femur bore greater stresses because of its greater contribution to acceleration (Kawano and Blob, 2013) or muscular configuration (Walthall and Ashley-Ross, 2006), and (2) whether variation in hardness across a limb bone corresponded with regional differences in locomotor stresses. Moreover, these data establish a foundation for considering 'mixed-chains' of limb bone SFs in generalized quadrupeds, in the context of transitions in limb function amongst stem tetrapods.…”