Erratum to: Bridging “Romer’s Gap”: Limb Mechanics of an Extant Belly-Dragging Lizard Inform Debate on Tetrapod Locomotion During the Early Carboniferous

Devonian stem tetrapods are thought to have used ‘crutching’ on land, a belly-dragging form of synchronous forelimb action-powered locomotion. During the Early Carboniferous, early tetrapods underwent rapid radiation, and the terrestrial locomotion of crown-group node tetrapods is believed to have been hindlimb-powered and ‘raised’, involving symmetrical gaits similar to those used by modern salamanders. The fossil record over this period of evolutionary transition is remarkably poor (Romer’s Gap), but we hypothesize a phase of belly-dragging sprawling locomotion combined with symmetrical gaits. Since belly-dragging sprawling locomotion has differing functional demands from ‘raised’ sprawling locomotion, we studied the limb mechanics of the extant belly-dragging blue-tongued skink. We used X-ray reconstruction of moving morphology to quantify the three-dimensional kinematic components, and simultaneously recorded single limb substrate reaction forces (SRF) in order to calculate SRF moment arms and the external moments acting on the proximal limb joints. In the hindlimbs, stylopodal long-axis rotation is more emphasized than in the forelimbs, and much greater vertical and propulsive forces are exerted. The SRF moment arm acting on the shoulder is at a local minimum at the instant of peak force. The hindlimbs display patterns that more closely resemble ‘raised’ sprawling species. External moment at the shoulder of the skink is smaller than in ‘raised’ sprawlers. We propose an evolutionary scenario in which the locomotor mechanics of belly-dragging early tetrapods were gradually modified towards hindlimb-powered, raised terrestrial locomotion with symmetrical gait. In accordance with the view that limb evolution was an exaptation for terrestrial locomotion, the kinematic pattern of the limbs for the generation of propulsion preceded, in our scenario, the evolution of permanent body weight support.

[1]  Ashley-Ross HINDLIMB KINEMATICS DURING TERRESTRIAL LOCOMOTION IN A SALAMANDER (DICAMPTODON TENEBROSUS) , 1994, The Journal of experimental biology.

[2]  P. Ahlberg,et al.  The origin and early diversification of tetrapods , 1994, Nature.

[3]  C. Sullivan,et al.  Function and evolution of the hind limb in Triassic Archosaurian reptiles , 2007 .

[4]  Ashley-Ross,et al.  METAMORPHIC AND SPEED EFFECTS ON HINDLIMB KINEMATICS DURING TERRESTRIAL LOCOMOTION IN THE SALAMANDER DICAMPTODON TENEBROSUS , 1994, The Journal of experimental biology.

[5]  J. A. Nyakatura,et al.  Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linné 1758) , 2010, Frontiers in Zoology.

[6]  J. Hutchinson,et al.  Three-dimensional limb joint mobility in the early tetrapod Ichthyostega , 2012, Nature.

[7]  D. B. Baier,et al.  X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[8]  C. Janis,et al.  Modes of ventilation in early tetrapods: Costal aspiration as a key feature of amniotes , 2001 .

[9]  John R. Hutchinson,et al.  Vertebral architecture in the earliest stem tetrapods , 2013, Nature.

[10]  J. Hutchinson,et al.  Historical perspectives on the evolution of tetrapodomorph movement. , 2013, Integrative and comparative biology.

[11]  O. A. Lebedev,et al.  The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev , 1995 .

[12]  Peter Aerts,et al.  Toe function and dynamic pressure distribution in ostrich locomotion , 2011, Journal of Experimental Biology.

[13]  M. Coates,et al.  ROMER's gap: tetrapod origins and terrestriality , 1995 .

[14]  Richard W Blob,et al.  Propulsive forces of mudskipper fins and salamander limbs during terrestrial locomotion: implications for the invasion of land. , 2013, Integrative and comparative biology.

[15]  J. Clack,et al.  Tetrapod appendicular skeletal elements from the Early Carboniferous of Scotland , 2013 .

[16]  T. Kubo Extant Lizard Tracks: Variation and Implications for Paleoichnology , 2010 .

[17]  J. Marshall,et al.  Earliest Carboniferous tetrapod and arthropod faunas from Scotland populate Romer's Gap , 2012, Proceedings of the National Academy of Sciences.

[18]  N. Emery,et al.  Tyrannosaurus was not a fast runner , 2002 .

[19]  J. Clack,et al.  An amniote-like skeleton from the Early Carboniferous of Scotland , 1999, Nature.

[20]  Martin S Fischer,et al.  Functional morphology and three-dimensional kinematics of the thoraco-lumbar region of the spine of the two-toed sloth , 2010, Journal of Experimental Biology.

[21]  J. Landsmeer The mechanism of forearm rotation in Varanus exanthematicus , 1983, Journal of morphology.

[22]  P. Senter,et al.  Vestigial structures in the appendicular skeletons of eight African skink species (Squamata, Scincidae) , 2011 .

[23]  J. Clack,et al.  An early tetrapod from ‘Romer's Gap’ , 2002, Nature.

[24]  A. A. Biewener,et al.  Biomechanics-- structures and systems : a practical approach , 1992 .

[25]  M. Ashley-Ross,et al.  Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa , 2004, Journal of Experimental Biology.

[26]  J. Clack Devonian tetrapod trackways and trackmakers; a review of the fossils and footprints , 1997 .

[27]  J. Willey,et al.  The tale of the tail: limb function and locomotor mechanics in Alligator mississippiensis , 2004, Journal of Experimental Biology.

[28]  O. R. Barclay The mechanics of amphibian locomotion. , 1946, The Journal of experimental biology.

[29]  G. E. Goslow,et al.  The functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus) , 1983, Journal of morphology.

[30]  S. Hsieh,et al.  Vertebrate land invasions-past, present, and future: an introduction to the symposium. , 2013, Integrative and comparative biology.

[31]  A. Biewener,et al.  Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). , 2001, The Journal of experimental biology.

[32]  P. Aerts,et al.  Scaling of plantar pressures in mammals , 2009 .

[33]  R. Carroll,et al.  Westlothiana lizziae from the Viséan of East Kirkton, West Lothian, Scotland, and the amniote stem , 1993, Earth and Environmental Science Transactions of the Royal Society of Edinburgh.

[34]  John A. Nyakatura,et al.  Ichnology of an Extant Belly-Dragging Lizard—Analogies to Early Reptile Locomotion? , 2014 .

[35]  M. Butcher,et al.  Locomotor loading mechanics in the hindlimbs of tegu lizards (Tupinambis merianae): comparative and evolutionary implications , 2011, Journal of Experimental Biology.

[36]  S. C. Rewcastle,et al.  Fundamental Adaptations in the Lacertilian Hind Limb: A Partial Analysis of the Sprawling Limb Posture and Gait , 1983 .

[37]  S. Reilly,et al.  Tuataras and salamanders show that walking and running mechanics are ancient features of tetrapod locomotion , 2006, Proceedings of the Royal Society B: Biological Sciences.

[38]  J. Edwards The Evolution of Terrestrial Locomotion , 1977 .

[39]  Alexander Petrovitch,et al.  Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. , 2010, Zoology.

[40]  David B Baier,et al.  Scientific rotoscoping: a morphology-based method of 3-D motion analysis and visualization. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[41]  Auke Jan Ijspeert,et al.  Where are we in understanding salamander locomotion: biological and robotic perspectives on kinematics , 2012, Biological Cybernetics.

[42]  R. Full,et al.  Dynamics of geckos running vertically , 2006, Journal of Experimental Biology.

[43]  C. Pace,et al.  Mudskipper pectoral fin kinematics in aquatic and terrestrial environments , 2009, Journal of Experimental Biology.

[44]  R. Blickhan,et al.  Leg design in hexapedal runners. , 1991, The Journal of experimental biology.

[45]  N. A. Wakefield,et al.  Trackways of Tetrapod Vertebrates from the Upper Devonian of Victoria, Australia , 1972, Nature.

[46]  Robert T. Barker DINOSAUR PHYSIOLOGY AND THE ORIGIN OF MAMMALS , 1971, Evolution; international journal of organic evolution.

[47]  L. McBrayer,et al.  The correlation between locomotor performance and hindlimb kinematics during burst locomotion in the Florida scrub lizard, Sceloporus woodi , 2012, Journal of Experimental Biology.

[48]  A. Biewener Scaling body support in mammals: limb posture and muscle mechanics. , 1989, Science.

[49]  R. Blob,et al.  Loading mechanics of the femur in tiger salamanders (Ambystoma tigrinum) during terrestrial locomotion , 2011, Journal of Experimental Biology.

[50]  R. Full,et al.  Differential leg function in a sprawled-posture quadrupedal trotter , 2006, Journal of Experimental Biology.

[51]  S. Turner,et al.  The First Stem Tetrapod from the Lower Carboniferous of Gondwana , 2004 .

[52]  Reinhard Blickhan,et al.  Adjustments of global and local hindlimb properties during terrestrial locomotion of the common quail (Coturnix coturnix) , 2013, Journal of Experimental Biology.

[53]  A. Garrod Animal Locomotion , 1874, Nature.

[54]  Richard W Blob,et al.  Hindlimb function in the alligator: integrating movements, motor patterns, ground reaction forces and bone strain of terrestrial locomotion , 2005, Journal of Experimental Biology.

[55]  J. Bolt,et al.  A new primitive tetrapod, Whatcheeria deltae, from the Lower Carboniferous of Iowa , 1995 .

[56]  Marcelo R. de Carvalho,et al.  GAINING GROUND. THE ORIGIN AND EVOLUTION OF TETRAPODS , 2004, Copeia.

[57]  M. Ashley-Ross,et al.  New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma , 2013, Biological reviews of the Cambridge Philosophical Society.

[58]  L. M. Frolich,et al.  KINEMATIC AND ELECTROMYOGRAPHIC ANALYSIS OF THE FUNCTIONAL ROLE OF THE BODY AXIS DURING TERRESTRIAL AND AQUATIC LOCOMOTION IN THE SALAMANDER AMBYSTOMA TIGRINUM , 1992 .