Conquering the world in leaps and bounds: hopping locomotion in toads is actually bounding

Abstract

Summary While most frogs maximize jump distance as an escape behaviour, toads have traded jump distance for endurance with a strategy of hopping repeatedly. This strategy has enabled toads to expand across the continents as one of the most diverse groups of anurans. Multiple studies have revealed physiological endurance adaptations for sustained hopping in toads, however, the kinematics of their sequential hopping behaviour, per se, has not been studied. We compared kinematics and forces of single hops and multiple hopping sequences and quantified field performance of hopping behaviours in free ranging toads of three species and discovered a novel aspect of locomotion adaptation that adds another facet to their exceptional terrestrial locomotor abilities. We found that bouts of repeated hopping are actually a series of bounding strides where toads rotate on their hands and then land on their extended their feet and jump again without stopping. In addition, free‐ranging toads appear to use bounding locomotion more frequently than single hops. Bounding in toads has the advantage of maintaining velocity and producing longer jump distances. In comparison to single hops, cyclic bounding steps reduce energy expenditure and appear to provide limb loading dynamics better suited for potential cycling of elastic energy from stride to stride than would be possible with repeated single hops. This is the first case of the common use of a bounding gait outside of mammals. Bounding adds a key terrestrial locomotor trait to the toad's phenotype that may help explain their history of global expansion and the challenges to modern faunas as introduced toads rapidly invade new ecosystems today.

Functional evolution of jumping in frogs: Interspecific differences in take‐off and landing

“…A novel feature of landing behavior in Rhinella is that the hindlimbs were almost completely folded when the hands‐hit the substrate. This observation is in accordance with previous reports of hopping behavior in R. marina (Azizi et al, ; Gillis et al, ; Reilly et al, ). In toads, the body rotated on the flexing humeri for about 4/5ths of the forelimb landing phase as the humeri became adpressed against the trunk.…”

“…Several studies of the landing per se have appeared more recently. The motor function and biomechanics of the limbs during landing have been studied primarily in the marine toad Rhinella marina of Hyloidea (Gillis et al, ; Akella and Gillis, ; Azizi and Abbott, ; Griep et al, ; Azizi, ; Azizi et al, ; Gillis et al, ; Cox and Gillis, ; Reilly et al, ). In addition, patterns of landing forces have been reported for two ranoid species ( Rana esculenta : Nauwelaerts and Aerts, ; Rana dybowski : Wang et al, ).…”

It is lonely at the front: contrasting evolutionary trajectories in male and female invaders

“…Hence, natural selection in the course of the toad's long march across tropical Australia may have favoured individuals with shorter-than-average arms and legs that moved by bounding rather than by leaping. The arms play a major functional role in bounding [63–65], consistent with the shifts seen in both forelimbs and hindlimbs.…”

Pre-landing wrist muscle activity in hopping toads

“…Their cyclic bounding locomotion has recently been described as energetically economical when compared with single hops (Reilly et al, 2015). This reduction in energy expenditure may be as a result of elastic energy cycling (Reilly et al, 2015).…”

“…Their cyclic bounding locomotion has recently been described as energetically economical when compared with single hops (Reilly et al, 2015). This reduction in energy expenditure may be as a result of elastic energy cycling (Reilly et al, 2015). Other research has shown that energy absorption within muscle and tendon -especially at the most distal joint of a landing limb, can change depending on the follow-up movement or lack thereof (Ambegaonkar et al, 2011;Biewener et al, 1998).…”