Biomechanics
How moles walk; it’s all thumbs
royalsocietypublishing.org/journal/rsbl
Research
Cite this article: Lin Y-F, Konow N, Dumont
ER. 2019 How moles walk; it’s all thumbs. Biol.
Lett. 15: 20190503.
http://dx.doi.org/10.1098/rsbl.2019.0503
Downloaded from https://royalsocietypublishing.org/ on 16 August 2023
Received: 12 July 2019
Accepted: 7 October 2019
Subject Areas:
biomechanics, behaviour, evolution
Keywords:
tetrapod, locomotion, walk, forelimb, humerus,
sesamoid bone
Author for correspondence:
Nicolai Konow
e-mail: nicolai_konow@uml.edu
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.4700111.
Yi-Fen Lin1, Nicolai Konow2 and Elizabeth R. Dumont3
1
Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, Amherst,
MA 01003, USA
2
Department of Biological Sciences, University of Massachusetts Lowell, Lowell, MA 01852, USA
3
School of Natural Sciences, University of California Merced, Merced, CA 95340, USA
Y-FL, 0000-0002-4645-8821; NK, 0000-0003-3310-9080
A recurring theme in the evolution of tetrapods is the shift from sprawling
posture with laterally orientated limbs to erect posture with the limbs extend-
ing below the body. However, in order to invade particular locomotor niches,
some tetrapods secondarily evolved a sprawled posture. This includes moles,
some of the most specialized digging tetrapods. Although their forelimb anat-
omy and posture facilitates burrowing, moles also walk long distances to
forage for and transport food. Here, we use X-ray Reconstruction Of Moving
Morphology (XROMM) to determine if the mole humerus rotates around its
long axis during walking, as it does when moles burrow and echidnas walk,
or alternatively protracts and retracts at the shoulder in the horizontal plane
as seen in sprawling reptiles. Our results reject both hypotheses and demon-
strate that forelimb kinematics during mole walking are unusual among
those described for tetrapods. The humerus is retracted and protracted in
the parasagittal plane above, rather than below the shoulder joint and the
‘false thumb’, a sesamoid bone (os falciforme), supports body weight during
the stance phase, which is relatively short. Our findings broaden our under-
standing of the diversity of tetrapod limb posture and locomotor evolution,
demonstrate the importance of X-ray-based techniques for revealing hidden
kinematics and highlight the importance of examining locomotor function at
the level of individual joint mobility.
1. Introduction
Early tetrapods had a sprawling posture with limbs extending laterally, but
throughout the evolution of tetrapods, the limbs have often migrated to a pos-
ition beneath the body, in order to provide an upright stance [1–4]. Erect posture
is one of many vertebrate transitions associated with energy savings that
evolved in concert with ever-increasing metabolic demands; it confers energy
savings by supporting body weight more directly along the long axes of limb
bones, reducing the forces and energy required of limb extensors [2,5]. Erect
posture also relaxes constraints on limb–substrate interactions by reducing lat-
eral body undulations associated with a sprawling gait, decoupling breathing
from locomotion [6], improving stamina [7] and allowing animals with erect
posture to move faster [1,8]. Despite the apparent advantages of an upright
stance, a few mammals have undertaken the evolutionary invasion of loco-
motor niches associated with a secondarily derived, sprawling posture. These
include semi-aquatic species that use their limbs to swim, such as seals, sea
lions, walrus, otters and platypus, and true moles (family Talpidae), which
live their lives almost completely underground.
Moles are highly specialized digging vertebrates and exhibit a highly exag-
gerated sprawling stance (figure 1). Their short, broad humerus (upper arm
bone) extends dorsally and cranially (upward and forward, respectively)
from the shoulder joint. Their palm, which is significantly widened by a
‘false thumb’ (os falciforme or sixth digit), faces laterally and away from the
body. With this forelimb anatomy and posture, moles can compress loose soil
© 2019 The Author(s) Published by the Royal Society. All rights reserved.
 terrestrial small mammals
echidna
opossum
rat
humeral excursion
during walking
cat
lateral view
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cat
opossum
rat
echidna
dorsal view
Figure 1. Humeral excursion and manus (hand) orientation during walking differs between moles and other terrestrial mammals. Lateral and dorsal views of
humeral movements are illustrated as excursion arcs around the shoulder joint (light blue) relative to the horizontal plane in small mammals [9] and moles
(this study). The mole manus (gold) faces laterally with the ‘false thumb’ lateral to Digit I (the homologue of the human thumb).
into the walls of their tunnels [10] instead of transporting soil
to the surface [10,11] at the expense of metabolic energy [12].
Eastern moles occupy home ranges exceeding 10 000 m2 [13],
which is 23–42 times larger than the home ranges of burrow-
ing pocket gophers of similar size [14]. Individuals negotiate
over 400 m of tunnel daily to forage for and transport food
[13]. This distance is more than 2650 times a mole’s body
length and is equivalent to a 4.5 km walk for a 1.75 m tall
human. Walking is probably a significant portion of a
mole’s daily energy budget. A recent kinematic study
revealed that mole forelimb kinematics involve a significant
component of long-axis rotation during burrowing [10], but
we know little about how this extremely specialized forelimb
moves during walking.
Here, we use the X-ray Reconstruction Of Moving Mor-
phology (XROMM [15]) to test two hypotheses about
kinematics at the mole shoulder joint during walking. The
first hypothesis is that the primary movement is rotation
around the long axis of the humerus (humeral pronation/
supination), which is the main driver of mole burrowing
movements [10,16] and of walking in echidnas [9,17]. The
second hypothesis is that movement at the shoulder is domi-
nated by retraction/protraction in the horizontal plane,
compared with the long-axis rotation, as seen in reptiles
with sprawling postures [18–20]. We test these hypotheses
by quantifying relative movements at the shoulder, elbow
and the ‘false thumb’ across the stance and swing phases of
the walking gait cycle.
2. Results
Moles walk at a speed of 20.8 ± 2.2 cm s−1 Supplemental
video S1 - video mole walking with a duty factor of 0.56 ± 0.02
(table 1). The dominating humeral motion is protraction/
retraction (62–109°; range-of-motion = 47°), compared with
fossorial mole 2
royalsocietypublishing.org/journal/rsbl
mole V
IV
III
II
I
sixth digit
Biol. Lett. 15: 20190503
mole
pronation/supination (93–122°; range-of-motion = 28°) at the
shoulder joint (table 1). Humeral movements mainly occur
above the horizontal plane (see excursion arc in figure 1, top
right and Supplemental video S2 - XROMM dorsal) and in the
parasagittal plane (see excursion arc in figure 1, bottom right
and Supplemental video S3 - XROMM lateral).
During the swing, the humerus is protracted (figure 2a)
and reaches maximum protraction before the ‘false thumb’
contacts the ground (figure 2c). During stance, the ‘false
thumb’ always remains cranial to the shoulder and elbow
joints (figure 2b, middle panel). Only the ‘false thumb’ and
Digit I make ground-contact during walking (figure 2b,
bottom panel). The ‘false thumb’ makes the first contact,
followed by Digit I, together forming a stable support.
3. Discussion
Moles walk with forelimb movements that are unusual in
several ways, compared with tetrapods with sprawling pos-
tures [17,18,21], and with terrestrial quadrupedal mammals,
including those with a more upright posture [1,9,22–24].
Similar to sprawling reptiles and salamanders [18,25] as
well as terrestrial mammals [9,26], the mole humerus is
protracted and retracted during walking. Particularly note-
worthy, however, is the fact that humeral retraction occurs
above, rather than in or below the horizontal plane (figure 1).
Throughout the mole walking gait cycle, the ground-con-
tact point remains cranial to the shoulder and elbow joints
(figure 2). This pattern is akin to how humans use a cane
or walker to assist ambulation. The sixth digit is placed on
the ground in front of the body, which then moves forward
to meet it. This ambulatory pattern differs fundamentally
from all other terrestrial tetrapods studied to date, where
the distal-most forelimb element (hoof, pad or palm) stays
caudal to the shoulder during stance [17–21,27]. Only Digit
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Table 1. Stride parameters and movements of humerus (mean ± s.e.m.) during mole walking. Rx, movement along x-axis (abduction/adduction); Ry, movement along y-axis (protraction/retraction); Rz, movement along z-axis
(supination/pronation); ROM, range-of-motion (max. angle–min. angle). Trials: four cycles from each of three individuals (total of 12 cycles).

stride parameter shoulder joint angle

individual speed (cm s−1) contact time (s) swing time (s) stride length (cm) stride frequency (Hz) duty factor individual Rx Ry Rz

no. 1 21.9 ± 3.7 0.08 ± 0.01 0.08 ± 0.01 3.4 ± 0.3 6.6 ± 1.0 0.51 ± 0.03 max. no. 1 6.7 ± 1.9 108.2 ± 0.6 131.5 ± 1.1
no. 2 12.9 ± 1.1 0.11 ± 0.01 0.07 ± 0.01 2.3 ± 0.1 5.6 ± 0.5 0.61 ± 0.02 no. 2 14.6 ± 2.1 103.8 ± 3.1 111.1 ± 2.0
no. 3 27.6 ± 1.7 0.08 ± 0.00 0.06 ± 0.01 3.9 ± 0.1 7.0 ± 0.4 0.56 ± 0.01 no. 3 7.7 ± 0.4 114.8 ± 1.7 123.7 ± 1.9
mean 20.8 ± 2.2 0.09 ± 0.01 0.07 ± 0.01 3.2 ± 0.2 6.4 ± 0.4 0.56 ± 0.02 mean 9.7 ± 1.4 108.9 ± 1.7 122.1 ± 2.7
min. no. 1 −11.9 ± 5.2 54.1 ± 2.0 101.4 ± 1.7
no. 2 0.88 ± 0.6 66.2 ± 3.4 88.0 ± 1.0
no. 3 −3.7 ± 3.4 65.4 ± 6.1 92.4 ± 2.5
mean −4.9 ± 2.5 61.9 ± 2.8 93.9 ± 1.9
ROM no. 1 18.7 ± 3.6 54.1 ± 1.7 30.1 ± 2.2
no. 2 13.7 ± 2.2 37.7 ± 4.9 23.2 ± 1.6
no. 3 11.4 ± 3.0 49.4 ± 6.6 31.3 ± 1.2
mean 14.6 ± 1.8 47.0 ± 3.3 28.2 ± 1.4
3

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 (a) joint coordinate system (b) anatomical coordinate system 4

parasagittal plane

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elbow
Z shoulder joint
x joint walking
0° Y direction
90° (0, 0, 0) sixth digit
y X X
lateral view 90° touchdown
z horizontal plane
mole no. 1 axis_X shoulder joint
shoulder joint mole no. 2 axis_Y parasagittal plane elbow joint
40 mole no. 3 axis_Z Z

translation along z-axis (cm)

abduct (+)/adduct (–)
sixth digit
20 humeral abduction 2.0

Biol. Lett. 15: 20190503

0 1.6

–20
+ 1.2
–40
x
0.8
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130
humeral protraction 0.4
protract (+)/retract (–)

touchdown
110
angle (°)

0
90
X
–2 –1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
70 + translation along x-axis (cm)
50 y palm
130
supinate (+)/pronate (–)

humeral supination
110 ulna
90
sixth
70
digit
stance phase swing phase +
50
0 25 50 75 100
z
cycle (%) Digit I
implanted marker horizontal
ground
(c) consecutive forelimb movements in one walking cycle
lateral view walking direction
max. retraction max. protraction

horizontal
ground
stance phase swing phase
walking direction

dorsal view

Figure 2. Forelimb kinematics during walking. (a) Joint coordinate system (JCS) of humeral movements during mole walking. The coordinate system origin is
defined as the midpoint of a line connecting the lateral and medial sides of the humeral head (a) [16]. The JCS z-axis is aligned with the humerus long
axis (supination (+z) /pronation (−z)) and the y-axis is parallel with the plane that passes through the width of the relatively flat humerus (humeral plane;
protraction (+y)/retraction (−y)) (a, top panel). A JCS reference angle is defined as describing joint movements relative to a neutral position in which the humeral
plane is perpendicular to the scapular long axis and the humeral long axis is parallel to the glenoid fossa (shoulder joint). In this position, the humeral XYZ relative
to scapula is 0°, 90°, 90°. Humerus movements relative to scapula are then described along x- (red, abduction+/adduction−), y- (green, extension+/flexion−) and
z-axes (blue, supination+/pronation−). The dotted line indicates toe-off. (b) Displacements of the shoulder (blue sphere) and elbow (green sphere) joints and the
pivot (orange sphere) of the ‘false thumb’ in the anatomical coordinate system (ACS). The ACS origin is defined as the location of the ‘false thumb’ at the initiation of
the contact phase during the first gait cycle. The ACS x-axis is aligned with the walking direction, defined as a line intersecting each point at which the ‘false thumb’
first contacted the ground (small orange spheres in b); the z-axis is perpendicular to the horizontal plane (i.e. vertical). The displacements of joint centres and ‘false
thumb’ along x-, y-, z-axes were tracked to illustrate their movements in the cranial (+x) and caudal (−x), lateral (+y) and medial (−y), and dorsal (+z) and
ventral (−z) directions. Middle panel: Locations of each joint/pivot in the x- and z-axes projected onto the parasagittal plane (light orange plane in the top panel)
during movement along the x-axis. Arrows indicate ‘false thumb’ touchdowns and beginning of stance phase. Bottom panel: White broken circle represents the mole
palm area that touched an inkpad on the ground during walking. Bones that make ground-contact are coloured black. (c) Forelimb movements during a walking gait
cycle; top panel: in a lateral view, bottom panel: in a dorsal view. Grey arcs illustrate peak shoulder flexion and extension. White line indicates the long axis of
humerus. Scapula (green), humerus (red), ulna (blue) and manus (gold).
 I (homologous to the human thumb) and the ‘false thumb’,
on the medial aspect of the mole palm touch the ground,
suggesting that the ‘false thumb’, a sesamoid bone, supports
the mole’s body weight much like the radial sesamoid
bone of elephants bears body weight when foot posture is
altered [28,29].
Humeral movements during mole walking differ substan-
tially from the major element of humeral long-axis rotation
seen during burrowing [10,16]. Changes in humeral orien-
tation and kinematics between burrowing and walking
likely require muscles of the shoulder and forelimb to operate
across very different ranges of fibre lengths. The lower force
requirements for walking compared with burrowing may
mean that muscles of the shoulder can stretch beyond their
optimal length for force generation during walking [30].
This may, in turn, facilitate the exaggerated extension at the
shoulder maintained during walking. Studies are needed to
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determine how muscle and joint operating lengths and
ranges are altered with respect to burrowing and locomotion
patterns in moles.
Humerus long-axis rotation is not a key kinematic com-
ponent of mole walking, as previously documented for
another burrowing locomotor specialist with sprawling pos-
ture, the echidna [9,17]. Differences in mole and echidna
forelimb movements may be linked to their fundamentally
different gaits; echidnas use a pace-like walking gait,
moving limbs on one side together, resulting in a noticeable
side-to-side (yaw) motion of the trunk [31]. By contrast,
moles have a symmetrical gait with diagonal limbs making
synchronous ground-contact (electronic supplementary
material, videos S1–S3). Lateral body undulations are
reduced as a result, and similar in magnitude to those
generally observed during walking in upright tetrapods [6,32].
Moles walk at speeds similar to ‘high walking’ alligators,
geckos, skinks and similarly sized ground squirrels and chip-
munks (10–20 cm s−1, [32–35]). However, the significantly
lower duty factor of mole walking compared with ‘high-
walkers’ and slow-moving mammals such as sloths and
lorises (0.56 compared with 0.70–0.90 [36–38]) means that
moles walk more like race-walking humans, and approach
the kinematics cut-off defining running (less than 0.5 [32]).
The fact that moles do not extend their stance phase by letting
the shoulder move past the hand may be linked to the rela-
tively low duty factor, and provide the narrow-body profile
that enables moles to move quickly in their expansive yet
tight tunnel networks during foraging. Whether moles use
their forelimbs to generate propulsion during walking, like
vampire bats [39], or propel themselves with their hind
limbs like generalized tetrapods [40] including dogs [41],
squirrels and chipmunks [33] warrants further study.
Our results broaden our understanding of the evolution-
ary diversity of tetrapod limb posture and locomotion,
demonstrate the importance of X-ray techniques in revealing
hidden movements during tetrapod locomotion, and high-
light the power of examining how joint mobility contributes
to locomotor function [42,43].
4. Methods
(a) Animals
Three eastern moles (Scalopus aquaticus, 94.7 ± 10.2 g) were
captured in Hadley, MA, and housed in accordance with
Institutional Animal Care and Use protocols at University of 5
Massachusetts Amherst and Brown University. At Brown
University, subjects were anaesthetized for implantation of
royalsocietypublishing.org/journal/rsbl
radio-opaque markers by sterile surgery. The procedure is
described in depth elsewhere [10], but briefly: we implanted a
1 mm spherical tantalum marker in the right scapula, three to
four 0.5 mm tantalum makers in the right humerus, and two
0.5–1 mm markers in the right ulna. Three 0.5 mm tantalum
markers were implanted subcutaneously in the palm: under-
neath the medially positioned ‘false thumb’ and at the base of
the third (mid) and fifth (lateral) digits. The three moles recov-
ered from surgery and resumed normal feeding and burrowing
within 3 days. The sample is minimal owing to difficul-
ties inherent to keeping moles and getting them through the
research pipeline.
Biol. Lett. 15: 20190503
(b) Data collection
Animals voluntarily walked in a rectangular box-enclosure,
custom-fashioned from radiotranslucent polycarbonate (20H ×
7W × 50L cm), and fitted with anti-slip tape on the flat ground
surface, to encourage normal locomotion while facilitating the
use of biplanar video fluoroscopy (Imaging Systems and Service,
55 kVp/250 mA, retrofitted with Phantom, v.10 high-speed cam-
eras (Vision Research; 90 Hz frame rate, 1/250 s shutter speed) to
determine how the mole forelimb made ground-contact. The box
was wide enough for animals to walk without touching the walls
but narrow enough to keep them walking forward in a straight
line. The world coordinate axis was marked using tantalum mar-
kers in the enclosure floor. After walking trials, subjects were
euthanized for computed tomography scanning to build 3D
models of the forelimb skeletal elements (scapula, humerus,
ulna and manus) as well as the marker implants (Mimics
v. 16.0 and Geomagic Studio v. 12).
(c) Forelimb motion analysis
We used established marker-based videofluoroscopy workflows
[15,44,45] to construct digital models and calculate forelimb joint
kinematics for four consecutive walking cycles from each indi-
vidual. The XROMM workflow [15] was used for bones
implanted with at least three markers (humerus, manus). Scien-
tific Rotoscoping [44] was used to align 3D models of bones
with fewer than three markers (scapular and ulna) to match
their positions in both X-ray images.
We ran two analyses. One describes humeral movements at
the shoulder joint within a joint coordinate system (figure 2a).
The second analysis sought to determine the trajectory of the
forelimb joints and the ‘false thumb’ relative to the ground as
well as the movement trajectory of the animal. Therefore, we
visualized the relative 3D locations of the shoulder, elbow and
‘false thumb’ (blue, green and orange spheres in figure 2b,
respectively), tracking their global coordinates over time.
We calculated mean values and standard errors for angular
movements at the shoulder joint and XYZ displacement of the
shoulder and elbow joint centres and the ‘false thumb’ from each
individual by normalizing data over each gait cycle to 0–100% of
the stroke cycle using cubic spline interpolation [46]. Stance and
swing phase durations and the contact duty factor ( percentage
of the stride where the forelimb touches the ground) were calcu-
lated for each gait cycle. Walking speed was defined as the 3D
displacement of a body landmark per second (cm s−1), averaged
across all strides within a given trial, and stride frequency was
defined as the inverse of stride duration.
Data accessibility. Data analysed for this study is provided on Dryad
(http://dx.doi.org/10.5061/dryad.5qp11c9) [47].
Authors’ contributions. Study conceptualization and design: Y.-F.L., E.R.D.
Data acquisition: Y.-F.L., E.R.D., N.K. Analysis and interpretation of
 data: Y.-F.L. Drafting of the manuscript: Y.-F.L., N.K. Editing: Y.-F.L., Research G2012162703 and the Natural History Collections, and the 6
E.R.D., N.K. Final approval of the version to be published: Y.-F.L., Graduate Program in Organismic and Evolutionary Biology at the
E.R.D., N.K. All authors agree to be accountable for all aspects of the University of Massachusetts Amherst.

work in ensuring that questions related to the accuracy or integrity of
any part of the work are appropriately investigated and resolved.
Competing interests. The authors declare no competing or financial
interests.
Funding. Funding was provided by the National Science Foundation
grant no. IOS-1407171, Sigma Xi Committee on Grants-in-Aid of
royalsocietypublishing.org/journal/rsbl
Acknowledgements. We thank Thomas Roberts for assistance with sur-
geries, Angela Horner for discussion of the experimental design,
Elizabeth Brainerd, David Baier, Ariel Camp and Peter Falkingham
for XROMM support, and Paul Spurlock, Joanne Huyler and
Animal Care Services of the University of Massachusetts Amherst
and Brown University for animal husbandry.

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