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Evolutionary BiologyEvolutionary Biology ISSN 0071-3260 Evol BiolDOI 10.1007/s11692-013-9266-z

Bridging “Romer’s Gap”: Limb Mechanicsof an Extant Belly-Dragging Lizard InformDebate on Tetrapod Locomotion Duringthe Early Carboniferous

John A. Nyakatura, Emanuel Andrada,Stefan Curth & Martin S. Fischer

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FOCAL REVIEWS

Bridging ‘‘Romer’s Gap’’: Limb Mechanics of an Extant Belly-Dragging Lizard Inform Debate on Tetrapod Locomotion Duringthe Early Carboniferous

John A. Nyakatura • Emanuel Andrada •

Stefan Curth • Martin S. Fischer

Received: 9 July 2013 / Accepted: 3 December 2013

� Springer Science+Business Media New York 2013

Abstract Devonian stem tetrapods are thought to have

used ‘crutching’ on land, a belly-dragging form of syn-

chronous 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 (Ro-

mer’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 dis-

play 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 evolu-

tionary 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.

Keywords Tiliqua scincoides � XROMM � X-ray

motion analysis � Substrate reaction force � Moment arm �External moment � Belly-dragging � Early tetrapods

Romer’s Gap Obscures Late Stem Group Tetrapod

Locomotor Evolution

In 1956, A.S. Romer recognized a hiatus in the continental

fossil record spanning the Early Carboniferous. During this

Tournaisian to mid-Visean time span, later called ‘‘Ro-

mer’s Gap’’ (Coates and Clack 1995), some key features of

the first terrestrial vertebrates were acquired (e.g., Ahlberg

and Milner 1994; Clack 2002a, b; Smithson et al. 2012).

Prior to the gap, late Devonian early tetrapods retained a

predominantly aquatic lifestyle and had very limited ter-

restrial locomotor capabilities (Clack 2002b; Pierce et al.

2012). Known late Devonian stem-group tetrapods such as

the iconic fossils Acanthostega and Ichthyostega were

relatively large animals (measuring between 0.5 and 1.2 m

in length), with the main bony elements of the tetrapod

Electronic supplementary material The online version of thisarticle (doi:10.1007/s11692-013-9266-z) contains supplementarymaterial, which is available to authorized users.

J. A. Nyakatura (&) � S. Curth � M. S. Fischer

Institut fur Spezielle Zoologie und Evolutionsbiologie mit

Phyletischem Museum, Friedrich-Schiller-Universitat,

Erbertstraße 1, 07743 Jena, Germany

e-mail: john.nyakatura@uni-jena.de

E. Andrada

Institut fur Sportwissenschaft, Bewegungswissenschaft,

Friedrich-Schiller-Universitat, Seidelstraße 20, 07743 Jena,

Germany

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DOI 10.1007/s11692-013-9266-z

Author's personal copy

limbs already present, but with paddle-like feet and large,

heavy heads (Clack 2002b). By the mid-Carboniferous a

wide range of representatives of the lineages now assigned

to the crown-group of tetrapods were present and had

evolved varied morphologies including penta- or tetra-

dactylus limbs, secondary limb reduction or even loss,

different skull shapes, and smaller-bodied forms of about

0.1 m in length (Carroll et al. 1998; Paton et al. 1999; Janis

and Keller 2001; Clack 2002b; Smithson et al. 2012).

Importantly, species that seem to have lived predominantly

terrestrially were clearly present by the mid-Visean

(Smithson et al. 1994; Paton et al. 1999).

Although Romer’s Gap is increasingly being filled by

spectacular fossil findings such as Pederpes (Clack 2002a),

Ossinodus (Warren and Turner 2004), and various tetra-

pods from Tournaisian localities of Scotland (Smithson

et al. 2012; Smithson and Clack 2013), our understanding

of early tetrapod locomotor evolution close to the crown-

group node remains uncertain. For the predominantly

aquatic late Devonian stem tetrapod Ichthyostega, Pierce

et al. (2013a) propose a form of belly-dragging, synchro-

nous forelimb action-driven terrestrial locomotion with

little contribution from the hindlimbs, a locomotor mode

they hypothesize to have been widespread amongst

Devonian stem tetrapods on the occasions they ventured

onto land (Pierce et al. 2013a). Modern mudskippers

(Periophthalmini: Actinopterygii) are cited as functional

analogues to this inferred locomotor mode (Pierce et al.

2012, 2013a; see also Pace and Gibb 2009). In contrast, the

primitive (i.e., crown-group node) tetrapod condition (e.g.,

Edwards 1977; Gans and de Gueldre 1992) is often con-

sidered to be most closely approximated by the locomotion

of modern terrestrial salamanders. Salamander locomotion

is marked by (1) a symmetrical walking gait (either in

lateral sequence or trot; see Hildebrand 1966, Pridmore

1994), (2) hindlimb-driven propulsion (Kawano and Blob

2013), and (3) the ability to lift the belly off the ground.

Kawano and Blob (2013) point out that from the perspec-

tive of locomotor mechanics there is a striking difference

between the locomotor mode recently inferred for Devo-

nian stem tetrapods and that of extant salamanders. This

paper aims to help conceptualize this evolutionary transi-

tion in locomotor mechanics.

Given the low limb length to body mass ratios of early

crown-group tetrapods compared to extant sprawling liz-

ards (approximated from the ratio of limb length to hum-

eral and femoral shaft diameter put forward by Bakker

1971), early crown-group tetrapod locomotion has been

suggested to have been more clumsy, lumbering and less

agile (e.g., Bakker 1971; Reilly et al. 2006). Pridmore

proposes that late Devonian (predominantly aquatic) tet-

rapods were certainly belly-dragging on land because at

least three limbs would have had to be down at all times

just to support and lift the early tetrapod and prevent it

from falling over, and because this would necessitate more

complex brain control, it may not have been achieved

immediately (Pridmore 1994). Some support for the belly-

dragging theory is provided by potential body drag marks

tentatively assigned to tetrapod track makers in the pre-

served trackways of the Genoa River locality in Australia

(trackway II) and the Hoy Sandstone of Orkney in Scotland

(Warren and Wakefield 1972; Clack 1997). Subsequent

evolutionary transformation by terrestrially adapted mid-

Carboniferous crown-group tetrapods towards salamander-

like terrestrial locomotion remains obscured by the per-

sisting scarcity of body fossils and lack of unequivocal

terrestrial fossil tracks (e.g., Clack 1997).

The body mass of an approximately 1 m-long animal

such as Pederpes or Ossinodus (fossils which are closer to

the crown-group node of tetrapods than the stem tetrapods

Acanthostega and Ichthyostega mentioned above) would

have been many times greater than that of a 60 g extant

terrestrial salamander (such as Dicamptodon tenebrosus or

Ambystoma tigrinum, species often used to study salaman-

der locomotor mechanics, see Edwards 1977; Frolich and

Biewener 1992; Ashley-Ross 1994a, b; Ashley-Ross and

Bechtel 2004; Reilly et al. 2006; Ashley-Ross et al. 2013;

Kawano and Blob 2013). Body mass scales with the third

power of length, whereas the cross-sectional area of bone

and muscle (associated with structural strength and force

exertion) scale with the second power of length. It would

therefore need to be shown that specific compensatory

morphological differences in the musculoskeletal system of

relatively large early tetrapods were present before it could

be fully accepted that they were functionally similar to

extant salamanders in terrestrial, weight-bearing locomo-

tion. As an alternative view, we propose that early tetrapods

in the Early Carboniferous were not able to permanently

raise their belly off the ground when on land. While similar

on the whole, belly-dragging sprawling locomotion has

different functional demands than ‘raised’ sprawling loco-

motion without ventral trunk-ground contact (Fig. 1).

Analysis of Limb Mechanics During Belly-Dragging

Sprawling Locomotion in the Blue-Tongued Skink

Sprawling locomotion with belly-dragging potentially

represents an intermediate stage between the locomotor

mode inferred by Pierce et al. (2012, 2013a) for Devonian

stem tetrapods and the salamander-like locomotion pro-

posed to be primitive to crown tetrapods (e.g., Edwards

1977; Gans and de Gueldre 1992). We here use a relatively

large, belly-dragging lizard—the blue-tongued skink (Til-

iqua scincoides intermedia: Scincidae, Mitchell 1955)—to

study limb mechanics during belly-dragging sprawling

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locomotion. T. scincoides shares various features with late

Devonian stem tetrapods, including fore- and hindlimbs of

similar length, and manus and pes that point forward during

locomotion (Kubo 2010; Curth et al., in press). The skink

also shares low limb length to body length ratios with early

tetrapods (see supplemental information), and while not

quite equaling the size of the known *1 m fossils,

northern blue-tongued skinks reach up to 60 cm in total

length and more than 1.3 kg in body mass (Horner 2000).

Additionally, in contrast to many other skinks, T. scinco-

ides possess girdles and limbs that are not vestigial, and

full pentadactyl autpodia (Moch and Senter 2011).

Detailed three-dimensional (3D) kinematics, especially

long axis rotation (LAR) in the humerus and femur, have

rarely been studied in vivo and have never been quantified

in a belly-dragging lizard (Jenkins and Goslow 1983;

McElroy et al. 2012; Karakasiliotis et al. 2012). Neither

has any previous study examined the substrate reaction

forces (SRFs) exerted by the limbs during locomotion in a

belly-dragging lizard. To fill this gap in our knowledge, we

quantified the 3D stance-phase kinematics of the proximal

limb joints (shoulder, elbow, hip and knee) using X-ray

reconstruction of moving morphology (XROMM; Brainerd

et al. 2010; Gatesy et al. 2010). Simultaneously, we mea-

sured the SRFs exerted by individual limbs, and calculated

the SRF moment arms for each joint. Finally, these data

were combined and the external moments acting on the

proximal limb joints during locomotion were inferred. We

use the data to address the following questions regarding

comparative limb function in belly-dragging and ‘raised’

sprawling locomotion:

A. Do kinematic differences in fore- and hindlimbs to

‘raised’ sprawlers exist? Gray (1968) identified three

components that simultaneously contribute to progres-

sion: girdle rotation, active limb retraction and limb

rotation. Limb rotation propels the body forward by

means of the ‘double crank mechanism’(Barclay 1946),

in which the LAR of the stylopodia caused by the

contraction of the muscles that insert on the crista

ventralis of the humerus and femur, respectively, is

transmitted back to the manus and pes (see Edwards 1977;

Ashley-Ross 1994a for illustrative figures). We quantify

the relative contribution to the progression of the body of

the major kinematic aspects of sprawling tetrapod

locomotion in the fore- and hindlimbs, respectively.

B. Do the SRF profiles of the fore- and hindlimbs differ

in non-belly-dragging sprawlers? Chen et al. (2006),

Willey et al. (2004), and Kawano and Blob (2013)

certainly found differential leg function in trotting

geckos, alligators, and tiger salamanders, respectively,

with net-braking forelimbs (i.e., the limbs exert a

negative impulse during stance) and net-propulsive

hindlimbs (i.e., the limbs exert a positive impulse

during stance) during near-constant locomotion. On

the basis of these findings Kawano and Blob suggest

this to be a general pattern with an ancestry deep in the

use of stepping locomotion (Kawano and Blob 2013).

C. Are the moment arms of the net SRF vector-modulated

during stance? When SRF magnitudes are identical,

decreasing the moment arm will reduce external moments.

To maintain equilibrium, muscles must exert opposing

and equal net moments about the joints to balance

moments incurred by SRFs, gravity and inertia (e.g.

Biewener and Full 1992; Hutchinson and Garcia 2002).

Net musculo-skeletal forces at the joints will decrease if

the SRF moments about the joints are minimized.

Finally, we synthesize our findings with previous work

to infer aspects of the locomotor mechanics of a hypo-

thetical, belly-dragging evolutionary phase in tetrapod

locomotion that occurred during the Early Carboniferous.

Fig. 1 Schematic drawings to illustrate the differences in functional

demands between a belly-dragging (e.g., T. scincoides) and b non-

belly-dragging (e.g., green iguana) sprawling locomotion. During

belly-dragging sprawling locomotion the animal’s weight partially

rests on the trunk via direct contact to the substrate (see supplemen-

tary material). During non-belly-dragging sprawling locomotion

larger moments (blue arrows) need to be produced by the musculo-

skeletal system about the shoulder/hip and elbow/knee joints to bear

the animal’s weight. Thus, elbow/knee extensors and shoulder/hip

adductors need to be stronger. Schematic drawing not to scale (Color

figure online)

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Our results can be regarded as predictive and remain to be

validated by future fossil finds that add to the ‘population’

of Romer’s Gap.

Materials and Methods

Experimental Subjects

A pair of T. scincoides was purchased from an authorized

dealer (M&S Reptilien, Weigheim, Germany). The animals

were legal captive offspring from 2009 and were kept

separately in spacious terrariums (2.0 9 0.6 9 0.6 m).

Each terrarium contained sand as a substrate and various

places for the animals to hide. The terrariums were lit and

heated (12 h/day) by an ultraviolet lamp and a metal halide

lamp controlled by a clock timer. Temperatures were kept

at 28–35 �C during the day and 22�–25� at night. Water

was available ad libitum and the animals were given

appropriate food once a week. The female (body mass

1,150 g; total length 56 cm) was slightly larger than the

male (965 g; 54 cm). All animal care and experiments

were carried out in strict adherence to the animal welfare

regulations of the federal state of Thuringia, Germany and

were approved by the Thuringian committee for animal

research (license for husbandry: J-SHK-2684-05-04/11-1;

license for experiments: Reg.-Nr. 02-008/11).

Experimental Design

The experimental setup combined biplanar, high-speed

X-ray videography (for the specifics of the equipment see

Nyakatura et al. 2010) with the simultaneous measurement

of single limb SRFs using two synchronized, custom built

radiolucent force plates (for details see Andrada et al.

2013) which were placed within the capture volume of the

biplanar X-ray. The animals were motivated to traverse the

instrumented trackway (1.0 9 0.3 m) by gentle touches

with a stick on the tail that usually resulted in a series of up

to eight consecutive strides. To distinguish limb SRFs from

those resulting from ventral body contact, the forceplates

were arranged side-by-side relative to the direction of

motion to maximize the likelihood of a single limb making

contact. Synchronized X-ray sequences from the ventral

and lateral projection were recorded by the 38 cm diameter

image intensifiers at 500 frames per second at a resolution

of 1,536 9 1,024 pixels.

All trials in which more than a single limb made contact

with a plate were discarded. 43 successful trials were

recorded (often containing useful data from both forelimbs

and hindlimbs), on the basis of which the kinematics and

spatio-temporal characteristics of 20 forelimb strides and

20 hindlimb strides were analyzed. As the overall speed

range was minimal and inter-individual differences in gait

parameters consistently non-significant (Table 1), forelimb

and hindlimb data from the two individuals were pooled.

From this dataset, the ten hindlimb (four from the male and

six from the female) and ten forelimb (seven from the male

and three from the female) contact phases most similar in

speed were selected for further dynamic analysis. In this

step, kinematics and SRF vectors, magnitudes and moment

arm lengths were combined to determine the external

moments acting on the limb joints (see below).

X-ray Reconstruction of Moving Morphology

‘‘X-ray reconstruction of moving morphology’’ (XROMM,

Brainerd et al. 2010) was performed to estimate the kine-

matics of the fore- and hindlimbs. We made use of the

totally non-invasive approach known as ‘‘scientific roto-

scoping’’ (SR, Gatesy et al. 2010) which removes the need

to implant internal markers. In SR, an articulated 3D model

of the specimen’s skeleton (derived from computed

tomography in our case) is manually posed using the 3D

animation package Autodesk Maya� 2012 (Autodesk, San

Rafael, CA, USA) so that it overlays the individual’s X-ray

Table 1 Spatio-temporal parameters of the two experimental subjects

Female (average ± SD;

N = 10)

Male (average ± SD;

N = 10)

t test Average ± SD

(N = 20)

Speed (m/s) 0.095 ± 0.010 0.100 ± 0.011 P = 0.721* 0.097 ± 0.010

Diagonality 0.472 ± 0.025 0.482 ± 0.029 P = 0.415* 0.477 ± 0.027

Forelimb duty factor 0.679 ± 0.034 0.664 ± 0.040 P = 0.381* 0.672 ± 0.037

Forelimb stride length (m) 0.099 ± 0.019 0.097 ± 0.017 P = 0.801* 0.098 ± 0.018

Hindlimb duty factor 0.604 ± 0.045 0.579 ± 0.051 P = 0.264* 0.592 ± 0.048

Hindlimb stride length (m) 0.076 ± 0.016 0.082 ± 0.018 P = 0.440* 0.079 ± 0.017

Unpaired t tests were used to check for significant differences between the individuals (significance level P \ 0.05). Because none were found,

we decided to pool data from the two individuals

* Non-significant

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shadow in both biplanar views. This process is repeated for

key frames of the X-ray video which can then be interpo-

lated between (cubic–spline interpolation) to produce

smooth movements that closely approximate the recorded

kinematics.

Prior to SR, raw X-ray videos must be corrected for

distortion (Brainerd et al. 2010; Gatesy et al. 2010) and the

orientation of the X-ray image intensifiers in relation to the

subject is determined by recording a calibration object

(0.2 9 0.12 9 0.12 m) with metal beads inserted at regu-

lar distances that is placed within the biplanar field of view.

We used the freely available MATLAB routine developed

at Brown University, Providence, USA (www.xromm.org).

In order to obtain bone models, both individuals were

cooled to ca. 15 �C to reduce movement and scanned using

a scanner belonging to the Friedrich Schiller University

Hospital, Jena, Germany. Sedation was not necessary.

Virtual reconstruction of bones was performed using the

segmentation editor in the Amira software package (VSG,

Burlington, MA, USA).

In SR, bone models are linked to form a hierarchical

chain (Gatesy et al. 2010). Anatomical coordinate systems

are implemented at each joint to measure the movement of

the distally adjacent bone relative to the proximal bone

directly from the Maya animation. In theory, a whole six

degrees of freedom (DOF) can be derived for each joint

using this method, but since translations within limb joints

were too small to be reliably measured we only considered

the rotations. All movements are measured relative to a

reference pose. The reference pose was aligned to a

right-handed global coordinate system placed in the

trackway with positive x pointing in the direction of

movement, positive y pointing to the animals’ right, and

positive z pointing upwards. All bone model coordinate

systems were aligned to the axes of the global coordinate

system (see Nyakatura and Fischer 2010a). In order to

obtain anatomically meaningful data we used non-physio-

logical fully extended reference poses for both the fore-

and the hindlimbs (Sullivan 2007; Nyakatura and Fischer

2010a, b). To avoid the singularity problem, the rotation

order in each joint was set to have the largest expected

movement as the dominant axis (cf. Sullivan 2007).

For the pectoral model reference pose, coordinate sys-

tems were placed in (1) the interclavicle to measure the

movement of the girdle relative to the global coordinate

system (the girdle was oriented to have both shoulder joints

at the same height and the x-axis running through the

cranial tip of the interclavicle and the caudal tip of the

mesosternum), (2) the shoulder joint to measure humeral

movement relative to the pectoral girdle (the long axis of

humerus pointed in the direction of positive global x with

the flexor side of the elbow joint pointing ventral), (3) the

elbow joint to measure ulnar movement relative to the

humerus (the long axis of the ulna pointed in the direction

of positive global x), and (4) the wrist joint to be able to

animate manus placement.

For the pelvic model reference pose, coordinate systems

were placed (1) midway between the ilia to measure pelvic

movement relative the global coordinate system (the girdle

was oriented to have both hip joints and the ishiadic

tuberosity at the same height), (2) in the hip joint to

measure femoral movement relative to the pelvis (the long

axis of the femur was oriented to point in the direction of

positive global x with the flexor side of the knee facing

ventral), (3) in the knee joint to measure tibial movement

relative to the femur (the long axis of the tibia pointed in

the direction of positive global x), and (4) in the joint space

distal to the tibia to be able to animate pes placement.

In SR, the quality of the results is highly dependent on

the fidelity of the X-ray images (visibility of the bony

structures) and—since the mapping of the model onto the

X-ray-images is an approximation—the experience and

skill of the investigator. We were unable to reliably mea-

sure the movements of the bony elements of the pectoral

girdle relative to one another and of the diminutive carpal

and tarsal bones, and nor did we analyze the movement of

the pectoral girdle relative to the vertebral column. Our

analysis is thus restricted to the shoulder, hip, elbow and

knee joints—the constituent kinematic components of the

double crank mechanism. We also quantified the overall

movements of the pectoral girdle (treating it as one object)

and the pelvic girdle relative to a global coordinate system

placed in the midpoint of the runway. All data was

exported into Excel (v. 2010, Microsoft, Redmond, WA,

USA) and each trial was normalized to the same duration

(101 points; Nyakatura et al. 2010) in order to make the

kinematic profiles (i.e., plots of kinematic data vs. percent

of stance) of trials of slightly different duration directly

comparable.

One of the merits of XROMM is the opportunity it

affords to conduct ‘virtual experiments’. This enabled us to

work out the relative contribution of individual kinematic

components of complex movements (e.g., LAR vs.

retraction in the shoulder and hip) as a percentage of total

manus and pes displacement, respectively, relative to the

body as it is moved over the fixed manus and pes during

stance. Because the autopodia are fixed to the ground

during stance, this percentage is a proxy for the contribu-

tion of a kinematic component to the progression of the

body. To work it out, we used the XROMM animation of

each trial and ‘muted’ (inactivated) the movement com-

ponent under consideration at touch-down, while all the

other components were kept active during stance (Nyaka-

tura and Fischer 2010a). The relative trunk displacement

that resulted was then compared to the displacement

observed in the original trial. The relative contribution of

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the inactivated kinematic component to trunk progression

is defined herein as the difference between the virtual

experimental trial and the original trial.

Substrate Reaction Forces and External Moments

In order to avoid having metal in the runway (and hence the

occlusion of the X-ray beam) the force plates were custom-

built from carbon fiber (Andrada et al. 2013). As transducer

elements, we used 6-DOF force-torque transducers (ATI

nano17; ATI Industrial Automation, Apex, NC, USA). The

force plates were flush with the runway and, to prevent the

lizards from slipping, the runway was covered with emery

paper. The set-up permitted the resolution of the SRF into

antero-posterior (or cranio-caudal; Fx), medio-lateral (Fy)

and vertical (Fz) components. To match the kinematic data

sampling rate, we collected SRFs at 500 Hz using cus-

tomized software for LabView 2009 (NI USB-6229,

National Instruments Germany GmbH, Munich, Germany).

We synchronized force and X-ray data acquisition by

matching the X-ray frame of apparent touch-down with the

initial spike of Fz. After smoothing using a low pass zero-

phase filter, the components of the SRF force trace were

again normalized to the same duration (101 points, see

above) using a custom MATLAB routine provided by B.

Hesse (FSU Jena, Germany). All SRFs were normalized to

body weight units (BW). To be able to pool data for the left

and right body sides, we set positive Fy to always point

medially.

External moment is the product of the moment arm, or

distance vector, and the SRF vector. The orientation of the

SRF vector for every 5 % increment in stance duration was

animated in Maya using a Maya ‘‘locator’’ in accordance

with the magnitudes of Fx, Fy, and Fz relative to a coordi-

nate system placed at the center of pressure (CoP) and in

line with the inherent coordinate system of the force plate

(Fig. 2). The positions of this locator were spline interpo-

lated in Maya for all in-between frames. An irregular tri-

angle was spanned between the CoP, the SRF orientation

locator and the joint. We used the Maya distance mea-

surement tool to measure, over time, the lengths a, b and c

(Fig. 2) of the triangle (it has previously been shown using

the known span of a caliper that measuring lengths in the

virtual experimental environment is relatively accurate; see

Nyakatura and Fischer 2010a). In accordance with the law

of cosines, the known lengths were used to calculate the

angle a, where

a ¼ arccosb2 þ c2 � a2

2bc

� �ð1Þ

The external moment arm (R) in 3D space, then, is part

of a right-angled triangle in which b is the hypotenuse and

R is opposite the angle a. The moment arm was calculated

as R = sin a 9 b (Fig. 2). Finally, the moment acting on a

joint was calculated as R 9 magnitude of SRF vector. R is

the shortest distance between the SRF vector and the joint,

but does not relate to any anatomical frame of reference

and can be regarded as a 3D moment arm of the instanta-

neous SRF. External moment, induced by load and inertia,

is here used as an indicator of the magnitude of net mus-

culoskeletal forces that exert opposing and equal net

moments to maintain equilibrium.

Fig. 2 Estimating external moments acting on limb joints during

stance phase—method shown here for the left shoulder for one frame.

The SRF vector (orange) of a trial was animated within the

corresponding XROMM animation. The origin of the SRF vector

(CoP) was assumed to be underneath the third metacarpal-phalangeal

(third metatarsal-phalangeal in the hindlimb) of digit III. CoP center

of pressure; a distance between joint and tip of SRF vector; b distance

between CoP and joint; c distance between CoP and tip of SRF vector.

For further explanation see text (Color figure online)

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We assumed the initial CoP to be underneath the third

metacarpal-phalangeal joint and third metatarsal-phalan-

geal joint, respectively. It has been shown for several taxa

that during roll-off, the CoP has a trajectory from this area

towards the tip of the manus or pes, respectively (e.g.,

Michilsens et al. 2009; Schaller et al. 2011). Therefore,

from lift off of the third metacarpal-phalangeal or third

metatarsal-phalangeal joint to lift off of the digit’s tip, we

animated the CoP in Maya to translate linearly from its

initial position to the tip of digit III, in an approach similar

to that taken by Sheffield and Blob (Sheffield and Blob

2011). We tested the influence of the initial position of CoP

using a sensitivity analysis and found that cranial and

caudal shifts of 2 mm (roughly 20 % of pes length) in the

position of the CoP result in a 5.5 % difference in the

external moment at peak vertical force (Fig. 3).

Results

Spatio-Temporal Gait Characteristics

In the trials analyzed, T. scincoides displays relatively slow

walking speeds (0.10 ± 0.01 m/s; or 0.28 ± 0.03 body -

lengths/s) and diagonal coupling of the limbs (Fig. 4a). The

forelimb usually touches down slightly prior to the diago-

nal hindlimb. Lift-off occurs at approximately the same

time in the fore- and hindlimbs. Thus, forelimb stance, on

average, is slightly longer than hindlimb stance (Table 1).

According to the Hildebrand gait formula (Hildebrand

1966), the gait can be classified as a walking trot (diago-

nality and duty factor shown in Table 1).

3D Stance Phase Kinematics

Overall stance phase kinematics are very similar in the

fore- and hindlimbs, but interesting differences do exist

(Figs. 4b, 5, 6). During the forelimb stance phase, the

pectoral girdle rotates, due to the lateral bending of the

vertebral column, about a dorso-ventral axis (an axis per-

pendicular to a line connecting the glenoids and to a line

connecting the cranial tip of the interclavicle and the

caudal tip of the mesosternum). This causes the shoulder of

the limb under consideration to rotate caudally. Towards

the end of a limb’s contact phase the pectoral girdle starts

to rotate in the opposite direction. The contact phases of the

two forelimbs overlap (Fig. 4a). The rotation of the pec-

toral girdle contributes an average of 28 % of the overall

displacement of the manus relative to the body as the body

moves over the fixed manus (Fig. 7). Throughout the

stance phase the humerus is abducted enough for the elbow

to be placed dorsolaterally to the shoulder joint (value

constantly below 0�). LAR of the humerus and humeral

retraction are the main movements to occur in the shoulder

joint (Fig. 4b; Table 2). Given the degree of LAR that

occurs it is surprising that it contributes just 10 % on

average to the displacement of the manus relative to the

body. In contrast, humeral retraction contributes 32 % to

manus displacement during stance. During the first quarter

of the stance phase no humeral LAR occurs and the manus

is displaced caudally (relative to the body) mainly by

humeral retraction (together with the pectoral girdle rota-

tion mentioned above). The elbow is initially flexed to

approximately 80� (from the fully extended reference pose)

and flexion increases to an average maximum of 114� at

approximately mid-stance. During the second half of the

stance phase continuous elbow extension occurs. The

overall contribution to progression of elbow flexion/

extension is also limited (10 %).

The pelvic girdle is also affected by the lateral undula-

tion of the vertebral column, with the hindlimb’s acetab-

ulum after touch-down more caudal than that of the

opposite side (Fig. 4b). On average, pelvic girdle rotation

has a less pronounced influence than pectoral girdle rota-

tion, contributing only 17 % to pes displacement (Fig. 7).

Like the elbow, the knee remains dorsolateral to the hip

almost throughout the stance phase, though its orientation

at touch-down is slightly more adducted than the elbow as

it is more extended. Femoral LAR sets in immediately after

touch-down and continues throughout most of the stance

phase. LAR in the femur is much smaller than LAR in the

humerus (53� vs. 78� on average, respectively; Table 2).

Nevertheless, LAR in the stylopod contributes just 8–10 %

to manus and pes displacement in the fore- and hindlimbs.

In contrast, femoral retraction is more pronounced than

humeral retraction (82� vs. 54� on average, respectively).

Fig. 3 Sensitivity of the position of CoP in deriving the external

moment. Sensitivity analysis was performed for a representative

hindlimb trial. Note that reasonable shifts of about 20 % of pes length

from the initial CoP position at the metatarsal-phalangeal (MTP) joint

result in just 5.5 % difference in peak external moment

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Fig. 4 Integration of

mechanical characteristics of

fore- and hindlimbs during

stance in T. scincoides

locomotion. a Two generalized

footfall patterns of a walking

trot. Note that forelimbs usually

touch down earlier than

hindlimbs. Period of diagonal

support enlarged. All other

graphs (b–d) are arranged to

reflect lengths and overlap of

average diagonal fore- and

hindlimb stance phases in order

to visualise mechanical

characteristics occurring

concurrently. Hindlimbs shown

on grey background.

b Averaged kinematic profiles

for the most substantial

movements in the proximal

joints and pectoral and pelvic

girdle, respectively. c Average

support reaction force traces in

cranio-caudal, medio-lateral,

and dorso-ventral direction.

Positive SRF components point

cranially, medially and dorsally.

d SRF moment arms (solid

lines) and external moments

(dashed lines)

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Fig. 5 Schematic illustration of

a forelimb stride cycle in T.

scincoides based on X-ray

motion analysis. Ventral aspect,

touch-down (TD) shown in dark

grey

Fig. 6 Schematic illustration of

a hindlimb stride cycle in T.

scincoides based on X-ray

motion analysis. Ventral aspect,

touch-down (TD) shown in dark

grey

Fig. 7 Virtual experiments to test the relative contributions of

kinematic components to the displacement of the manus and pes,

respectively, during the contact phase. Results obtained by inactivat-

ing kinematic components one by one in the XROMM animation.

Manus and pes are fixed to the ground during stance and any

displacement of the manus or pes relative to the body will lead to

displacement of the body. All kinematic components except that

under investigation remained activated. All virtual experiments start

with the instant of touch down. A full kinematics (control),

B inactivated rotation about a dorso-ventral axis of the girdle element

(y-axis; see text), C inactivated stylopod movement (movement in

shoulder and hip joints, respectively), D inactivated rotation about

long axis of stylopod, E inactivated retraction of stylopod, F inacti-

vated flexion/extension of elbow and knee, respectively. For each bar

an error bar representing one standard deviation is provided and the

percentage by which inactivation of the kinematic component in

question reduces displacement is shown. Taken together, the contri-

butions of the pectoral/pelvic girdle, stylopod movement and elbow/

knee movement do not add up to 100 % because the contributions of

distal limb joints were not considered

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This difference is reflected in the relative contributions to

pes displacement of femoral retraction (57 %) and humeral

retraction (32 %). Like the elbow, the knee undergoes

initial flexion followed by extension later in stance

(Fig. 4b). However, starting from a more extended initial

pose (angle at touch-down 64� vs. 94� in the elbow;

Table 2), maximal flexion (84�) is already reached by

about 25 % of stance. The contributions of elbow and knee

flexion/extension to pes displacement are relatively small

(Fig. 7).

Substrate Reaction Forces

In contrast to the kinematic aspects documented here,

substrate reaction forces differ substantially between the

fore- and the hindlimbs (Fig. 4c). Forces are much greater

in the forelimbs, with the vertical component being the

largest in both the fore- and the hindlimbs. In the forelimb,

Fz increases moderately but not abruptly after touch-down

and reaches its maximum shortly after mid-stance (peak

Fz = 0.51 ± 0.11 BW; Table 3). Peak Fz occurs concur-

rently with maximum elbow flexion, but as humeral

rotation already has positive values, the forearm is some-

what ventro-caudally orientated. On average, Fx is always

positive (peak Fx = 0.21 ± 0.08 BW; Fig. 4c), exerting a

propulsive impulse throughout stance. Fy is comparatively

small (average peak Fy is just 0.13 ± 0.16 BW) and, on

average, medially directed throughout the stance phase.

In the hindlimb, peak Fz is exerted much earlier in the

stance phase (at 26.4 ± 8.6 % of stance). Just as peak

forelimb Fz and maximum elbow flexion coincide, peak

hindlimb Fz coincides with peak flexion of the knee

(Fig. 4). At peak Fz, less than a quarter of the body weight

is brought to bear on the support (Table 3). Values for peak

Fx and peak Fy are smaller than in the forelimb (Table 3),

but like in the forelimb there is a constant propulsive

impulse, even though it is smaller in overall magnitude.

Medio-lateral forces are small and slightly laterally direc-

ted after midstance.

The pattern of forces exerted on the ground during

stance means that the share of the total body weight carried

by the limbs is non-constant. The remaining share is car-

ried by the trunk via ventral contact with the support.

Neglecting the effects of inertia (assuming quasi-static

Table 2 Kinematic parameters at touch down, mid contact and lift off

Touch down angle (�) Mid contact angle (�) Lift off angle (�)

Average (±SD) Range Average (±SD) Range Average (±SD) Range

Pectoral girdle

x-Axis rotation 1.2 ± 2.1 -2.7 to 4.3 2.8 ± 3.6 -3.4 to 7.6 1.0 ± 7.6 -12.6 to 10.9

y-Axis rotation -5.0 ± 3.8 -9.7 to 1.6 -4.9 ± 4.9 -8.9 to 7.8 -9.5 ± 2.7 -12.6 to -4.0

z-Axis rotation 2.0 ± 9.4 -17.8 to 14.8 6.6 ± 1.5 3.7 to 8.5 -12.2 ± 9.1 -23.5 to 4.4

Shoulder

x-Axis rotation -24.3 ± 6.3 -36.2 to -10.2 19.5 ± 12.4 3.5 to 46.8 54.7 ± 12.2 43.7 to 75.7

y-Axis rotation -17.9 ± 9.5 -31.8 to -3.5 -22.3 ± 10.9 -43.8 to -7.1 -4.6 ± 4.1 -11.8 to 8.8

z-Axis rotation 72.9 ± 13.8 54.9 to 89.4 111.3 ± 16.1 92.7 to 129.5 126.0 ± 6.6 117.5 to 137.4

Elbow

x-Axis rotation 9.7 ± 8.3 -0.5 to 23.8 10.2 ± 6.6 -0.1 to 25.0 13.2 ± 8.3 -3.3 to 26.7

y-Axis rotation 94.2 ± 22.4 69.4 to 131.2 114.3 ± 10.1 97.7 to 134.8 45.4 ± 12.9 26.9 to 67.5

z-Axis rotation 45.4 ± 12.9 -26.8 to 7.2 7.9 ± 9.9 -9.4 to 25.1 12.4 ± 13.2 -11.3 to 41.9

Pelvic girdle

x-Axis rotation -0.4 ± 0.9 -1.7 to 1.1 -4.6 ± 2.2 -7.3 to -1.1 6.9 ± 5.6 0.9 to 15.4

y-Axis rotation -15.5 ± 0.5 -16.8 to -14.9 -15.5 ± 0.9 -16.7 to -13.7 -18.3 ± 0.5 -19.1 to -17.4

z-Axis rotation 7.5 ± 2.5 4.2 to 11.2 -5.4 ± 2.2 -8.9 to -1.9 -12.2 ± 4.5 -17.4 to -5.5

Hip

x-Axis rotation -5.2 ± 7.2 -14.7 to 6.0 24.7 ± 6.8 13.7 to 35.1 40.6 ± 6.0 32.1 to 52.8

y-Axis rotation 1.2 ± 3.6 -6.4 to 6.8 -4.5 ± 2.9 -8.9 to 1.8 -15.7 ± 5.4 -22.8 to -5.1

z-Axis rotation 58.9 ± 4.0 52.2 to 65.7 104.7 ± 7.9 99.8 to 126.2 136.2 ± 16.2 105.9 to 161.4

Knee

x-Axis rotation -19.9 ± 9.1 -24.5 to 5.0 -19.7 ± 6.7 -29.5 to -4.3 -15.1 ± 9.8 -32.4 to 1.9

y-Axis rotation 64.6 ± 7.2 53.3 to 77.1 76.5 ± 5.9 69.2 to 89.6 36. 2 ± 21.3 8.0 to 81.8

z-Axis rotation -2.5 ± 2.9 -5.9 to 1.7 -5.8 ± 7.5 -18.9 to 4.2 -3.2 ± 6.1 -14.9 to 8.3

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locomotion), the share carried by the limbs varies from

about 20 % around touch-down and lift off to 65 % at mid-

stance (see supplemental information).

External Moment Arms and External Moments

External moment arm lengths and the pattern of external

moments exerted by the SRF again differ substantially

between the fore- and the hindlimbs. The external moment

arm of the SRF vector acting on the shoulder at touch-

down is larger than the external moment arm acting on the

elbow (Fig. 4d). The situation is the same at lift-off.

Interestingly, the moment arm acting on the shoulder is

smallest around mid-stance at the instant of peak Fz, dis-

playing values well below the SRF moment arm lengths of

the elbow (0.0173 ± 0.0044 vs. 0.0227 ± 0.0025 m;

Table 3). The external moment arm at the elbow is much

more constant throughout stance and does not display a

pronounced local minimum at any point during the contact

phase. The small external moment arm acting on the

shoulder at peak Fz leads to an external moment of less

than 0.05 Nm which remains, on average, at a relatively

low level (below 0.06 Nm) for most of stance. In com-

parison, the external moment acting on the elbow at peak

vertical force is greater than 0.08 Nm (Fig. 4d). Peak

external moment at the elbow roughly coincides with peak

vertical force (Table 3).

In the hindlimb, the SRF moment arms acting on both

the hip and the knee are relatively constant throughout

stance. On average, the moment arm acting on the hip is

consistently larger than that acting on the knee (Fig. 4d).

Unlike in the shoulder, then, the external moment arm at

the hip does not drop to a minimum at peak vertical force.

The peak external moment at the knee is approximately

0.1 Nm on average. The peak external moments acting on

both hip and knee coincide with peak vertical force much

earlier in stance (Fig. 4d). Because the moment arms are

larger, the external moment acting on the hindlimb reaches

similar values as in the forelimb despite the fact that

overall SRF forces are lower.

Discussion

Similarities and Differences in Limb Mechanics

Between Belly-Dragging and Non-belly-dragging

Sprawling Locomotion

Kinematics

The overall limb kinematic pattern in T. scincoides is

similar to that in non-belly-dragging sprawling tetrapods.

The contribution to forward propulsion of stylopod LAR in

the fore- and hindlimbs of the skink has been found to be

10 % or less. In terrestrial salamanders, the contribution of

stylopod LAR to forward propulsion has been estimated to

be greater (26–28 %, Edwards 1977). In contrast, the

estimated contribution to progression of the pectoral girdle

Table 3 Peak SRF components, minimum SRF moment arm lengths, maximum external moment and their respective timing during the contact

phase

Parameter Averages and range Timing in % of stance phase

Average ± SD Range Average (±SD) Range

Forelimb

Peak vertically directed SRF (BW) 0.51 ± 0.11 0.36–0.69 54.2 ± 9.5 46–78

Peak cranially directed SRF (propulsive) (BW) 0.21 ± 0.08 0.14–0.43 59.8 ± 9.9 45–74

Peak medially directed SRF (BW) 0.13 ± 0.16 0.01–0.45 47.9 ± 25.3 5–86

Minimum SRF moment arm length shoulder (cm) 1.73 ± 0.44 1.01–2.37 49.0 ± 11.5 35–75

Minimum SRF moment arm length elbow (cm) 2.27 ± 0.25 1.91–2.66 79.5 ± 9.0 75–95

Maximum external moment shoulder (Nm) 0.10 ± 0.02 0.07–0.14 47.0 ± 22.9 20–80

Maximum external moment elbow (Nm) 0.11 ± 0.02 0.08–0.15 48.0 ± 14.9 20–75

Hindlimb

Peak vertically directed SRF (BW) 0.22 ± 0.04 0.15–0.28 26.4 ± 8.6 16–48

Peak cranially directed SRF (propulsive) (BW) 0.07 ± 0.03 0.05–0.12 31.6 ± 20.5 16–86

Peak medially directed SRF (BW) 0.05 ± 0.07 0.00–0.22 33.7 ± 19.4 11–64

Minimum SRF moment arm length hip (cm) 3.07 ± 0.48 2.20–3.53 34.5 ± 16.2 15–55

Minimum SRF moment arm length knee (cm) 2.18 ± 0.29 1.57–2.40 67.5 ± 13.2 55–80

Maximum external moment hip (Nm) 0.10 ± 0.02 0.09–0.15 31.0 ± 14.1 15–65

Maximum external moment knee (Nm) 0.08 ± 0.01 0.06–0.10 26.5 ± 5.8 15–35

SRFs normalized to body weight (BW)

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in T. scincoides (28 %) is slightly higher than the 10–18 %

estimated by Edwards (1977) for salamanders. The esti-

mated contribution to progression of the pelvic girdle in T.

scincoides is 17 %, while that in salamanders is again

10–18 % (Edwards 1977). The retraction of the humerus

and femur contributes the most to the progression of the

body during stance in both blue-tongued skinks and sala-

manders (56–62 % in salamanders, Edwards 1977). How-

ever, while we found a large difference in the contributions

of humeral retraction (32 %) and femoral retraction

(57 %), Edwards (1977) does not mention any differences

between the fore- and the hindlimbs.

3D forelimb kinematic data on sprawling locomotion is

largely absent from the published literature, but Karaka-

siliotis et al. (2012) recently published a detailed X-ray

motion analysis of the terrestrial locomotion of the Iberian

ribbed newt (Pleurodeles waltl) using the same equipment

we used. In comparison to the blue-tongued skink in our

study, the newts displayed greater amplitudes of femoral

LAR. Furthermore, unlike the belly-dragging skink they

also displayed greater amplitudes of humeral retraction

than femoral retraction (Karakasiliotis et al. 2012). Inter-

estingly, the observation that humeral LAR is much greater

than femoral LAR in T. scincoides coincides with the

observation that the forelimbs produce greater overall

forces and the SRF moment arm acting on the shoulder is

smallest at peak SRF (see ‘‘Discussion’’ below).

Data on femoral LAR and femoral retraction during burst

locomotion in the Florida scrub lizard (Sceloporus woodi)

show overall values comparable to T. scincoides (McElroy

et al. 2012). Tiger salamanders (Ambystoma tigrinum) also

displayed constant limb adduction and similar femoral

retraction amplitudes as T. scincoides (Sheffield and Blob

2011). White tegus (Tupinambis merianae), green iguanas

(Iguana iguana) and American alligators (Alligator missis-

sippiensis) all have even larger amplitudes of femoral pro-

and retraction (Blob and Biewener 2001; Sheffield et al.

2011). According to our quantitative data, the LAR of the

stylopodia contributes less to the progression of the body

than the rotation of the pectoral and pelvic girdles (Fig. 7)—

even in a skink characterized by comparatively little exter-

nally visible undulation of the vertebral column (Daan and

Belterman 1968; supplemental information). LAR is an

essential factor in overall limb kinematics and has effects on

the function of the lower arm and leg (Rewcastle 1983;

Landsmeer 1983). In our virtual experimental trials in which

stylopodial long-axis rotation was inactivated, autopodia

swept through the ground at all times.

SRF Patterns and Their Timing in Fore- and Hindlimbs

With regard to weight support distribution between the

fore- and the hindlimbs, geckos (Hemidactylus garnotii)

studied by Chen and coworkers (Chen et al. 2006) expe-

rienced greater vertical forces in their forelimbs than in

their hindlimbs. The running gait used by these geckos

makes the data in question difficult to compare to this

study, but greater forelimb support was also evident in T.

scincoides. Walking salamanders studied by Kawano and

Blob (2013) carried around 0.5 BW on their forelimbs

(Fig. 1 in Kawano and Blob 2013)—a figure similar to that

found in T. scincoides. However, the Fz exerted by a single

tiger salamander hindlimb also peaked at *0.5 BW

(Sheffield and Blob 2011; Kawano and Blob 2013). Thus,

support in salamanders is distributed approximately

equally between the fore- and the hindlimbs. In contrast,

the forelimbs of the skink carried more than double the

load of the isolated hindlimbs (which bore just *0.2 BW

at peak Fz). In the slow trotting or lateral sequence gait of

salamanders, where the duty factors are high, the consid-

erable time spent with all four appendages in simultaneous

ground contact apparently permits a slight lifting of the

trunk off the ground. Other available hindlimb data per-

taining to ‘raised’ sprawlers also exceeds the peak Fz of the

skink’s hindlimbs in every case [gecko: *1 BW (Chen

et al. 2006); green iguana: *1 BW (Blob and Biewener

2001); white tegu: *0.45 BW (Sheffield et al. 2011)].

Although peak Fz occurs much earlier during the contact

phase in the hindlimb than the forelimb in T. scincoides, it

coincides in both cases with maximum flexion in the knee

or elbow (Fig. 4). In geckos, on the other hand, peak Fz

occurs earlier in the forelimb, and well within the first half

of contact (Chen et al. 2006). In tiger salamanders and

white tegus, as in T. scincoides, peak Fz occurs much

earlier during contact in the hindlimbs than it does in the

forelimbs (Sheffield and Blob 2011; Sheffield et al. 2011).

American alligators and green iguanas, in contrast, exert

peak Fz at approximately mid-stance (Blob and Biewener

2001; Reilly et al. 2005). In none of these species do

maximum knee flexion and peak Fz seem to coincide as in

the hindlimbs of T. scincoides. In species that do not have

constant ventral contact to the substrate, no clear pattern

exists, with peak Fz occurring before (tiger salamander,

white tegu; Sheffield and Blob 2011; Sheffield et al. 2011)

or after (green iguana, American alligator; Blob and

Biewener 2001; Reilly et al. 2005) maximum knee flexion.

However, in those species that exert Fz before or at max-

imum knee flexion, the femur is not yet retracted and still

points somewhat cranio-laterally (tiger salamander, white

tegu, blue-tongued skink). Vice versa, in those species that

exert peak Fz after maximum knee flexion (i.e., as the knee

is extending), the femur is already in a retracted position

and pointing somewhat caudo-laterally (American alliga-

tor, green iguana). More belly-dragging species need to be

analyzed to test whether a clearer pattern may be detectable

during this type of sprawling tetrapod locomotion.

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While geckos (Chen et al. 2006; Autumn et al. 2006)

and salamanders (Kawano and Blob 2013) both exerted a

braking impulse with the forelimbs, T. scincoides did not

brake (on average), but very slightly propelled the body in

the direction of movement with both fore- and hindlimbs

on a constant basis. As the animals were not observed to

accelerate, this propulsive impulse clearly just offsets the

constant braking effected by the belly as a consequence of

ventral contact. The hindlimbs of tiger salamanders and

white tegus were not found to exert braking impulses either

(Sheffield and Blob 2011; Sheffield et al. 2011; Kawano

and Blob 2013). In stark contrast to these non-belly-drag-

ging species, however, T. scincoides produces more pro-

pulsive impulse in the forelimbs than in the hindlimbs,

making it an exception among sprawling tetrapods,

according to the available data.

SRF Moment Arms and External Moments Acting

at Proximal Limb Joints

Reducing the moment arm of the SRF acting at a specific

joint by directing the SRF vector more closely to the joint

is, to some extent, a way of reducing the muscle moments

acting at the same joint (Biewener 1989; Full et al. 1991).

However, in multi-segmented bent limbs, simultaneously

minimizing the moment arms of the SRF vector at all joints

would be impossible and counterproductive. It would also

complicate joint control, because the closer the SRF vector

passes to a joint, the easier it switches sides, thus triggering

the need for net joint moments to switch between flexion

and extension. In T. scincoides the minimum moment arm

length of the SRF vector acting at the shoulder occurred at

the moment of peak Fz, but this did not apply to the SRF

moment arm acting at the hip (Fig. 4). Unlike T. scinco-

ides, geckos and salamanders seem not to direct the SRF

vector to pass close to the shoulder and thus experience

relatively short external moment arms at the elbow (Chen

et al. 2006; Kawano and Blob 2013). Given that a shorter

external moment arm in the elbow is partially offset by

higher peak vertical forces in ‘raised’ sprawlers, the mus-

cular force required at the elbow will not differ dramati-

cally between belly-dragging and ‘raised’ sprawlers

(Fig. 8). In contrast, ‘raised’ sprawlers seem to be able to

generate—thanks to strong pectoral muscles—a much lar-

ger adducting moment in the shoulder, especially given the

large external moment arm and larger peak vertical force

they exert compared to the belly-dragging T. scincoides.

The small external moment arm at the shoulder at peak

vertical force might, then, simply reflect the inability of the

pectoral muscles of T. scincoides to produce more ad-

ducting moment. In the hindlimbs, the SRF vector at peak

force is directed to pass more closely to the knee than the

hip in geckos (Chen et al. 2006), tiger salamanders

(Sheffield and Blob 2011), green iguanas (Blob and

Biewener 2001), white tegus (Sheffield et al. 2011), and the

blue-tongued skink.

Functional Consequences of the Adoption of Belly-

Dragging Locomotion in Early Tetrapod Evolution

The patchy fossil record near the crown-group node and the

apparently rapid radiation and diversification of tetrapods

in the Early Carboniferous (e.g., Smithson and Clack 2013)

mean caution is called for when attempting to reconstruct

the last common ancestor of crown-group tetrapods.

However, the notion of a belly-dragging phase is substan-

tiated by the considerable size of fossils such as Pederpes

(Clack 2002a), Whatcheeria (Lombard and Bolt 1995),

Tulerpeton (Lebedev and Coates 1995) and Ossinodus

(Warren and Turner 2004), and by low limb length to body

mass ratios (see Bakker 1971). The dramatic change in

functional role from pectoral appendages that drag the

body via in-phase crutching, as proposed for Devonian

stem tetrapods, to those that contribute to propulsion via

stepping, as proposed for crown-group node tetrapods, has

been pointed out by Kawano and Blob (2013). This reflects

the notion that the similarity in function between fore- and

hindlimbs was initially absent in Devonian tetrapods and

later evolved convergently (see Diogo et al. 2013). Anal-

yses of the locomotor mechanics in belly-dragging T.

scincoides reveal an intermediate character combination

that potentially affords insights into a transformational

state of early tetrapods close to the crown-group node.

According to Pierce et al. (2012), the forelimbs played a

crucial role in terrestrial locomotion much earlier than the

hindlimbs during the fin-to-limb transition. In this regard it

is interesting to note that T. scincoides generate more

propulsive thrust in their forelimbs than in their hindlimbs.

Kawano and Blob (2013) suggest that while propulsion was

‘‘hindlimb-driven’’, the forelimbs of early tetrapods with

heavy tails probably still made a substantial contribution.

Our data demonstrates that sprawling locomotion is not

always ‘‘hindlimb-driven’’.

The relatively large and heavy Devonian stem tetrapods

usually had their weight supported by water and were

likely to be lacking the strong shoulder and hip adductors

and knee and elbow extensors needed for non-belly-drag-

ging sprawling locomotion (Fig. 1). An explanation for the

ability of ‘raised’ sprawlers to produce large adducting

moments in the shoulder might lie in the more vertical

orientation of the SRF vector documented in ‘raised’

sprawling tetrapod forelimbs compared to belly-dragging

T. scincoides (Chen et al. 2006; Kawano and Blob 2013;

this study). In T. scincoides the vertical component of the

SRF reaches a maximum of only about 50 % of body

weight in the forelimbs and considerably less in the

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hindlimbs, leading to smaller overall magnitudes of the

SRF vector. With similar mechanics as documented here

for T. scincoides, a belly-dragging early tetrapod would

have been able to move on land with relatively weakly

developed pectoral muscles (Fig. 8). Having body weight

partially supported by direct substrate contact can be con-

sidered an intermediate condition between having it sup-

ported by water and having to raise it off the ground against

gravity. In the light of the considerable size of known early

tetrapods and the relationship between cross-sectional area

and muscle volume, we suggest that belly-dragging meant

that smaller, and thus initially more attainable, anti-gravity

muscles were needed to achieve terrestrial locomotion.

A Scenario of Tetrapod Locomotor Evolution During

the Early Carboniferous

Accepting the possibility of a belly-dragging phase in early

tetrapod evolution during the Early Carboniferous, the

study of the extant belly-dragging T. scincoides or other

belly-dragging tetrapods (e.g., gharials, giant salamanders)

has the potential to help conceptualize an evolutionary

scenario for the transition of early tetrapod locomotor

mechanics. The transition starts with locomotion marked

by ventral contact and synchronous forelimb action-gen-

erated propulsion—the form of locomotion presumably

embodied by Ichthyostega (and likely other tetrapods) of

the Devonian (Pierce et al. 2012, 2013a, b; Kawano and

Blob 2013). Later, the salamander-like ‘raised’ terrestrial

locomotion inferred for diverse Early- and mid-Carbonif-

erous terrestrial tetrapods evolved (e.g., Clack 2002b),

marked by symmetrical gaits, hindlimb propulsion and full

support of body weight by the limbs. The present study

suggests a link between belly-dragging and forelimb

dominance in weight bearing and provision of propulsion.

We thus propose that during the hypothesized belly-drag-

ging phase of tetrapod locomotor evolution, locomotion

was still forelimb-driven with regard to provision of pro-

pulsion, initially with little assistance from the hindlimbs.

Dragging substantial parts of the body along increases the

propulsive role of the limbs as a means of countering the

net braking effect of the body (Willey et al. 2004). After

this intermediate, forelimb-dominated belly-dragging

phase, intermittent and later permanent lifting of the trunk

(effected by the action of the shoulder adductors and elbow

extensors in the forelimb and the hip adductors and knee

extensors in the hindlimb) evolved, while the role of the

hindlimbs in weight-bearing and the provision of propul-

sion gradually increased. Salamander-like terrestrial loco-

motion was finally achieved either by an increase in the

relative mass of muscles with an anti-gravity role and/or an

overall reduction in body size (documented in the fossil

record by the first appearance of very small-sized animals

such as Casineria in the Mid-Visean; Paton et al. 1999, for

example). Hence, in the concept of evolutionary transition

proposed herein, the locomotor mechanics of initially

belly-dragging Devonian tetrapods were gradually modi-

fied, as opposed to the de-novo appearance of salamander-

like terrestrial locomotion in the alternative scenario.

Importantly, our hypothesis predicts that the mode of

propulsion generation, i.e., the overall kinematic pattern,

precedes the evolution of permanent body weight support

by the limbs. That is, we suggest, in accordance with

accepted accounts, that limbs and initial limb kinematics

likely evolved to serve purposes in water (Clack 2002b;

Pierce et al. 2012), with subsequent smaller modifications

of limb mechanics representing an exaptation for terrestrial

locomotion.

This evolutionary scenario based on a biomechanical

analysis of an extant lizard needs to be shown to be in

agreement with biomechanical inferences about the ter-

restrial locomotor capabilities of specific fossil specimens.

Dynamic musculoskeletal modeling of the limbs in belly-

dragging and non-belly-dragging extant sprawlers could be

used to anchor musculoskeletal models of available

Fig. 8 Functional consequences of a non-belly-dragging and b belly-

dragging locomotion. The nearly vertical orientation of the SRF

vector (orange arrows) documented in the forelimbs of non-belly-

dragging sprawling tetrapods (Chen et al. 2006; Kawano and Blob

2013) results in a short moment arm (R) at the elbow, but long R at the

shoulder and a high external moment. The shortened R at peak Fz and

low overall SRFs during belly-dragging locomotion documented here

result in a moderate external moment. Please note that the combi-

nation of a 50 % reduction in SRF magnitude and a 50 % reduction in

R will result in just 25 % of the net joint torque needed to maintain

equilibrium (Color figure online)

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well-preserved fossil specimens (e.g., Tulerpeton, Peder-

pes or Ossinodus) close to the crown-group tetrapod node.

However, no stem group specimen can be claimed to

represent an immediate ancestor: they are offshoots from

the lineage leading to the last common ancestor of modern

tetrapods. Hopefully, future findings of ichnofossils and

fossil specimens that further populate Romer’s Gap (see

Smithson et al. 2012) will help to narrow down possible

scenarios of locomotor evolution in early tetrapods.

Acknowledgments The authors would like to thank Rommy Pet-

ersohn and Ingrid Weiss for technical help during X-ray motion

analyses. Vivian R. Allen and Brandon M. Kilbourne provided

helpful comments on earlier versions of the manuscript. Professional

language polishing by Lucy Cathrow improved the final version of the

manuscript. CT scans were recorded at the Institut fur Interventionelle

und Diagnostische Radiologie at the University Hospital of the

Friedrich-Schiller-Universitat Jena. This project is financed by the

Volkswagen Foundation (Grant No.: AZ85857 to JAN and MSF).

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