Do all frogs swim alike? The effect of ecological specialization on swimming kinematics in frogs

Abstract

Frog locomotion has attracted wide scientific interest because of the unusual and derived morphology of the frog pelvic girdle and hind limb. Previous authors have suggested that the design of the frog locomotor system evolved towards a specialized jumping morphology early in the radiation of the group. However, data on locomotion in frogs are biased towards a few groups and most of the ecological and functional diversity remains unexplored. Here, we examine the kinematics of swimming in eight species of frog with different ecologies. We use cineradiography to quantify movements of skeletal elements from the entire appendicular skeleton. Our results show that species with different ecologies do differ in the kinematics of swimming, with the speed of limb extension and especially the kinematics of the midfoot being different. Our results moreover suggest that this is not a phylogenetic effect because species from different clades with similar ecologies converge on the same swimming kinematics. We conclude that it is important to analyze frog locomotion in a broader ecological and evolutionary context if one is to understand the evolutionary origins of this behavior. KEY WORDS: Anura, Kinematics, Locomotion, Swimming INTRODUCTIONFrog locomotion has attracted wide scientific interest because of the unusual and highly derived morphology of these animals (Barclay, 1946; Estes and Reig, 1973;Zug, 1978; Frost et al., 2006). Frogs are characterized by a shortened trunk and tail, elongated ilia and elongated hind limbs. This morphology has been interpreted as being associated with a jumping life style and thus it has been suggested that jumping evolved early in the evolution of the lineage (Gans and Parsons, 1966;Shubin and Jenkins, 1995; Jenkins and Shubin, 1998) and many recent studies have attempted to infer locomotion in basal frogs (Prikryl et al., 2009; Essner et al., 2010;Reilly and Jorgensen, 2011;Sigurdsen et al., 2012;Venczel and Szentesi, 2012; Jorgensen and Reilly, 2013). However, kinematic and electromyographic studies indicate strong similarities between the mechanics of swimming and jumping in some frogs (Emerson and De Jongh, 1980;Peters et al., 1996; but see Nauwelaerts and Aerts, 2003), implying that morphological features associated with these two locomotor modes may not be that different. This may, in turn, complicate inferences of locomotor modes from anatomy as is often done for extinct animals. Despite their rather uniform morphology, frogs are an ecologically diverse and speciose group with over 5000 known species (Frost et al., 2006). Moreover, animals with different ecologies have evolved different morphologies and show different levels of locomotor performance (Moen et al., 2013), suggesting that locomotion differs in animals with different ecologies. RESEARCH ARTICLETo date, most of our knowledge on frog locomotion is based on data for a limited set of derived frogs including ranoids [mostly ranids and bufonids (Calow and Alexander, 1973; Lutz and Rome, 1994;Kamel et al., 1996;Pet...

Digital dissection of the model organism Xenopus laevis using contrast‐enhanced computed tomography

“…; Gurdon & Hopwood, ; Burggren & Warburton, ; Wheeler & Brändli, ; Harland & Grainger, ; Cline & Kelly, ; Clemente & Richards, ; Richards & Clemente, ; Robovská‐Havelková et al. ; Burgess, ). Xenopus laevis is easy to house and maintain, and its eggs and embryos are large, tolerate manipulation and are produced in large quantities (Wheeler & Brändli, ).…”

“…The African clawed frog, Xenopus laevis Daudin, 1802, is one of the most widely used organisms in biological research, including applications in cell and molecular biology, genetics, physiology, embryology, development and morphogenesis, neuroscience, biomechanics, toxicology and medicine (Gurdon et al 1971;Gurdon & Hopwood, 2000;Burggren & Warburton, 2007;Wheeler & Br€ andli, 2009;Harland & Grainger, 2011;Cline & Kelly, 2012;Robovsk a-Havelkov a et al 2014;Burgess, 2016). Xenopus laevis is easy to house and maintain, and its eggs and embryos are large, tolerate manipulation and are produced in large quantities (Wheeler & Br€ andli, 2009).…”

Introduction to the special issue “Contributions in honour of Zbyněk Roček”

“…Kolesová et al 2007;Královec et al 2010;Roček et al 2015), functional morphology (e.g. Delfino et al 2009;Přikryl et al 2009;Robovská-Havelková et al 2014) and classical descriptive and systematic palaeontology (e.g. Roček 2008;Wuttke et al 2012;Dong et al 2013;Roček et al 2014).…”

Pelvic function in anuran jumping: Interspecific differences in the kinematics and motor control of the iliosacral articulation during take‐off and landing

“…). Anteroposterior translation has also been shown during swimming (Videler and Jorna, ; Robovska‐Havelkova et al, ), however, the focus of this study is to investigate the pelvic function during terrestrial jumping locomotion. Recent phylogenetic reviews of a suite of pelvic traits across Anura have shown that the “lateral‐bender” configuration is both basal and generalized for walker/hoppers, whereas the rod‐like “sagittal hinge” configuration has appeared independently multiple times within several crown group neobatrachian anurans (Reilly and Jorgensen, ; Jorgensen and Reilly, ).…”

“…1). Anteroposterior translation has also been shown during swimming (Videler and Jorna, 1985;Robovska-Havelkova et al, 2014), however, the focus of this study is to investigate the pelvic function during terrestrial jumping locomotion. Recent phylogenetic reviews of a suite of pelvic traits across Anura have shown that the "lateral-bender" configuration is both basal and generalized for walker/hoppers, Fig.…”