Morphological Changes in Pedal Phalanges Through
Ornithopod Dinosaur Evolution: A Biomechanical
Approach
Karen Moreno,1* Matthew T. Carrano,2 and Rebecca Snyder3
1Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK
2Department of Paleobiology, National Museum of Natural History, Smithsonian Institution,
Washington, District of Columbia 20013-0121
3Applied Morphometrics Laboratory, National Museum of Natural History, Smithsonian Institution,
Washington, District of Columbia 20013-0121
ABSTRACT The evolution of ornithopod dinosaurs pro-
vides a well-documented example of the transition from
digitigrady to subunguligrady. During this transition, the
ornithopod pes was drastically altered from the plesiomor-
phic dinosaurian morphology (four digits, claw-shaped
unguals, strongly concavo-convex joints, phalanges longer
than wide, excavated collateral ligament fossae, presence
of sagittal ridge, and prominent processes for the attach-
ment of tendons) to a more derived condition (tridactyly,
modi?cation of the unguals into hooves, phalanges wider
and thinner than long, lack of collateral ligament fossae,
loss of sagittal ridge and tendon attachment processes,
relatively ?attened articular surfaces). These changes are
particularly noteworthy given the overall conservatism in
pedal morphology seen across Dinosauria. But what are
the functional consequences of these speci?c morphologi-
cal transitions? To study them, we examine a wide range
of pedal morphologies in four non-avian dinosaurs and
two birds. Our analyses of the external morphology, two-
dimensional models (using Finite Element Analysis), and
internal bone structure demonstrate that this evolution-
ary shift was accompanied by a loss of digit mobility and
?exibility. In addition, pedal posture was modi?ed to bet-
ter align the pes with the main direction of the ground
reaction force, thus becoming well suited to support high
loads. These conclusions can be applied to other, parallel
evolutionary changes (in both dinosaurs and mammals)
that involved similar transitions to a subunguligrade pos-
ture. J. Morphol. 268:50?63, 2007. 
 2006 Wiley-Liss, Inc.
KEY WORDS: biomechanics; functional morphology;
kinematics; foot; ?nite element analysis; trabecular
structure; stress distribution
Ornithopods were a diverse group of ornithischian
dinosaurs that, having originated as approximately
kilogram-sized bipeds in the Late Triassic, eventu-
ally achieved multi-ton body sizes by the Late Cre-
taceous. The development of cranial crests among
hadrosaurid ornithopods is one of the most remark-
able aspects of their evolutionary history (Sereno,
1999). The group is particularly interesting from an
evolutionary standpoint because it records a number
of long, gradual morphological transitions via a rela-
tively dense series of closely related forms. Among
the most signi?cant such transitions is the acquisi-
tion of quadrupedalism, associated with many modi-
?cations of the pes (Fig. 1).
The acquisition of a subunguligrade pes presents
a striking example of convergence with mammals
such as rhinocerotids and proboscideans. Studies of
mammals indicate that as body size increases, limb
posture becomes progressively more upright, and
limb motion is restricted to a predominantly para-
sagittal plane (Hildebrand, 1988; Biewener, 1989;
Christiansen, 2002). These changes allow a reduc-
tion in the mass-speci?c amount of force required
to counteract moments about the limb joints (Biew-
ener, 1989), and are based on physical rather than
phylogenetic constraints. Therefore, it is reasonable
to hypothesize that such changes may have accom-
panied body-size increases in dinosaurs as well.
In fact, the transition to a quadrupedal posture
occurs in parallel within numerous dinosaur lineages
[stegosaurs, ceratopsians, and sauropods (Sereno,
1999; Carrano, 2001)], presumably with a consequent
forward shift of the center of mass (Henderson, 1999).
Although some uncertainty still exists about how spe-
cialized (or obligatory) ornithopod quadrupedalism
was, evidence of its use is available fromdifferent-sized
manual/pedal sets of footprints (Lockley and Hunt,
1995; Wright, 1999). In addition, the more primitive
ornithopod Dryosaurus may represent an intermedi-
ate stage in the transition to bipedalism, inwhich juve-
niles engaged in facultative quadrupedalism but
Contract grant sponsors: NMNH Equipment Fund; Overseas
Research Student Award, Universities UK; University of Bristol
Scholarship; Evolution of Terrestrial Ecosystems Group (publication
no. 141).
*Correspondence to: Karen Moreno, University of New South
Wales, School of Biology, Earth and Environmental Sciences, Biol-
ogy Building (D26), Room 558, Sydney, Australia 2052.
E-mail: dinohuella@yahoo.com
Published online 4 December 2006 in
Wiley InterScience (www.interscience.wiley.com)
DOI: 10.1002/jmor.10498
JOURNAL OF MORPHOLOGY 268:50?63 (2007)

 2006 WILEY-LISS, INC.
adults were nearly exclusively bipedal (Heinrich et al.,
1993). A comparative anatomical study of the hadro-
saurid ornithopod Maiasaura (Dilkes, 2001) showed
that although the forelimb was gracile, it was well
suited to carry a portion of body weight, especially in
adults.
The pedal morphology of basal ornithopods is
shared with theropods and is considered plesio-
morphic for Dinosauria. This morphology consists
of three primary weight-bearing digits, a phalan-
geal formula of 2-3-4-5-0, claw-shaped unguals,
phalanges that are proximodistally longer than
mediolaterally wider, well-developed collateral lig-
ament fossae (Fig. 2A), prominent proximal pro-
cesses for the attachment of extensor and ?exor
tendons, and pronounced development of saddle-
shaped (or ginglymoid) joints formed by a sagittal
ridge on the proximal phalangeal articular surface
(and a complementary furrow on the distal sur-
face) (Fig. 2B). These features are evident in most
basal ornithischians, including Lesothosaurus and
??hypsilophodontians?? such as Hypsilophodon, The-
scelosaurus, and Tenontosaurus. Basal ankylopol-
lexians such as Camptosaurus show some forelimb
modi?cations that suggest intermittent use in sup-
port, but the pes remains quite primitive and
retains three claw-like unguals.
In all these forms, the pes is distinctly digitigrade,
and footprints attributed to primitive ornithopods
show discrete digit marks with no indication of a ?e-
shy metatarsal pad. However, more highly derived
ornithopods (iguanodontians) modi?ed this digiti-
grade pes into a more subunguligade structure. At
the same time, the manus became more highly
modi?ed for weight bearing, and quadrupedalism
was presumably more frequently used. These orni-
thopods eliminated the ?rst pedal digit (resulting in
a phalangeal formula of 0-3-4-5-0) and modi?ed the
unguals into hooves. The phalanges are mediolater-
ally wider and anteroposteriorly thinner than proxi-
modistally long, lack collateral ligament fossae, and
exhibit neither a sagittal ridge, a process for tendon
attachment, nor excavation of the joint surfaces; all
articular surfaces are ?attened relative to the ple-
siomorphic state. These marked postural and mor-
phological differences imply associated differences
in pedal kinematics, and therefore in the distribu-
tion of forces across the pes.
In the present work, our goal was to evaluate
the responses of different ornithopod phalangeal
morphologies to external loading. Speci?cally, we
examined differences in pedal digit morphology
and mobility within and among taxa by studying
the external characteristics of the joints. To test
whether these differences may have been corre-
lated with loading conditions during locomotion,
we modeled the distribution of loading in isolated
phalanges of various proportions using ?nite ele-
ment analysis (FEA). Because trabecular architec-
ture is at least partly related to the principal lon-
Fig. 1. Evolution within Ornithopoda. Changes of stance, posture, and size are evident from the skeletal reconstructions;
enlargements highlight changes in digit III pedal morphology. The presence of a soft-tissue pad (black outline beneath pedal pha-
langes) has been inferred from trackway morphologies. Skeletal reconstructions are approximately to scale (Lesothosaurus, 1 m
total length; Camptosaurus, 8 m; Corythosaurus, 10 m; modi?ed from Paul 1987); (phylogeny simpli?ed from Carrano, 1999).
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 51
Journal of Morphology DOI 10.1002/jmor
gitudinal stresses and the magnitude of shear
stresses (Wolff, 1870; Hayes et al., 1982; Bertram
and Swartz, 1991; Gefen and Seliktar, 2004), we
documented the internal trabecular structure
using computed tomography (CT) scanned images,
and made comparisons to the modeled loading pat-
terns. Finally, we interpreted the results in light
of several perceived anatomical ??zones?? within the
phalanx, as a means to understand the consequen-
ces of morphological changes on the external and
internal structures of the distal pedal phalanges.
MATERIALS AND METHODS
For this study, we focused on the non-ungual phalanges from
nearly complete specimens of associated ornithopod feet. We
studied three specimens of the ankylopollexian Camptosaurus
dispar (USNM 5473, USNM 4277, USNM 4697) and two hadro-
saurids, Corythosaurus casuarius (USNM 15578) and Saurolo-
phus sp. (AMNH 5271; mounted in plaster). For comparative
purposes, we also examined the pedes of the non-avian theropod
Allosaurus fragilis (USNM 8324) and the extant ratites Dro-
maius novaehollandiae and Rhea americana (Fig. 3).
External Morphology
We quanti?ed the distal joint curvature (Fig. 4A) and sagittal
ridge height (Fig. 5A) of the pedal phalanges in order to
describe the basic changes that occurred during the evolution of
the ornithopod pes. Joint curvature re?ects the maximal
amount of dorsoventral ?exion and extension; more ?attened
phalangeal surfaces were presumably capable of less rotation in
the dorsoventral plane. The sagittal ridge is a narrow crest that
crosses the proximal joint surface dorsoventrally, dividing it
into two concave facets and thereby creating a ginglymoid mor-
phology (Fig. 2B). This morphology at least partly serves to con-
strain mediolateral and rotational movements, acting to enforce
dorsoventral motion when the joint is under torsional loads.
Measurements of the sagittal ridge and joint curvature on
these specimens were obtained from the digitized distal joint
surfaces using a MicroScribe G2XL (Immersion Corporation
M.R.) in combination with the software Rhinoceros 3D (version
3.0, educational license for the Applied Morphometrics Labora-
tory, National Museum of Natural History, Smithsonian Institu-
tion). For practical reasons, the sagittal ridge data were col-
lected from the distal joint surface (i.e., the sagittal furrow) of
the preceding phalanx (Fig. 2B). Although the sagittal ridge
itself is present on the proximal articulation, the contacting
phalangeal surfaces conform nearly perfectly, permitting accu-
rate measurements to be taken from either surface.
Modeling
We created two-dimensional (2D) models of individual pha-
langes with the software Fempro (Algor V19, Fempro). We con-
structed basic phalangeal models by assembling two basic geo-
metric shapes, a circle and a truncated cone, into a single struc-
ture that represents a phalanx in lateral view. Either shape (or
both) could be modi?ed in order to create variations in the over-
all shape of the phalanx.
Constant left-right symmetry of the structure (circle and
truncated cone assembled) was maintained in our models (Fig.
2A). Although real phalanges often show some degree of asym-
metry, especially in animals with specialized locomotory behav-
iors (e.g., asymmetrical step, fossorial, etc.), the objective of our
model is to show general patterns in phalangeal morphology
that can be easily compared between different animals regard-
less of individual or speci?c variations. The different degrees of
asymmetry can be treated as an additional (untested) variable
that might further modify the stress distributions; certainly
this aspect is worthy of further study.
The scale of the model is assumed to have little effect on the
stress distribution. Other studies have shown that for many
mammals, stresses are maintained at relatively constant levels
over a wide size range without disproportionate changes in the
cross-sectional areas of bones (Alexander et al., 1979). There-
fore, the results of the present model can be generally compared
with pedal bones of different absolute sizes.
To study the in?uence of shaft length (Fig. 2A), we increased
the height of the truncated cone, but not the dimensions of its
top, bottom, sides, or of the circle. We used the same method to
vary the proximal surface width, by changing the length of the
topside of the truncated cone and adjusting the lateral sides for
Fig. 2. Anatomical terms and measurements used in this study. A) Mediolateral view; B)
Anterior view.
52 K. MORENO ET AL.
Journal of Morphology DOI 10.1002/jmor
Fig. 3. Photographs of specimens used in this study in dorsal view. A) Camptosaurus dispar, left pes, USNM 5473; B) Campto-
saurus dispar, right pes, USNM 4277; C) Camptosaurus dispar, left pes, USNM 4697; D) Corythosaurus casuarius, right pes,
USNM 15578; E) Saurolophus sp., right pes, AMNH 5271; F) Allosaurus fragilis, left pes, USNM 8424; G) Dromaius novaehollan-
diae, left pes, P. Kroehler, pers. coll.; and H) Rhea americana, right pes, P. Kroehler, pers. coll. Ornithopods are enclosed in a
frame. Scale bars ? 10 cm.
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 53
Journal of Morphology DOI 10.1002/jmor
the new shape. For the proximal joint concavity, the portion
enclosed by a curve inscribed within the truncated cone was
subtracted from the total surface. An equivalent technique was
used for the distal convexity: we subtracted the distalmost area
formed by a curve inscribed in the circle.
Finite Element Analysis
We performed a FEA in order to examine stress distributions
within the modeled phalanges. The FEAwas performed by the soft-
ware Fempro (Algor V19, Fempro), under the following conditions:
1) Meshing was set to triangular shape at a density of 400?
450 triangles per area unit, with optimum meshing symme-
try. This construction geometry acts as a braced framework
(truss), preventing bending loads in the structure, and is
subjected only to longitudinal loading (tension and compres-
sion) but not shear or bending. These characteristics are
compatible with cancellous bone behavior (Currey, 2002;
Levin, 2002).
2) Material properties were taken from published values (Reilly
and Burstein, 1975) for fast-growing Haversian bovine bone
(isotropic): density ? 1,895 kg/m3; elastic modulus (E) ? 10
GPa; Poisson?s ratio ? 0.4; shear modulus (G) ? 3.66 GPa. Bo-
vine histology seems to resemble that of certain dinosaurs
(Reid, 1996), at least enough to allow the assumption of
broadly similar material properties and minimum strength
capability estimates for the models.
Nonetheless, we also tested two other material properties
in order to assess the effects of changes in this variable.
First, we used general bone material properties taken from
Currey, 2002: density ? 2,000 elastic modulus (E) ? 20 GPa;
Poisson?s ratio ? 0.3; shear modulus (G) ? 5 GPa. Using
these properties did not affect the stress distribution; mini-
mum and maximum stress values varied up to 3% from the
calculated ones using bovine material, but retained their lin-
earity. Second, we used red oak wood (the optimum under
compression) from Algor?s Library (density ? 662.6 elastic
modulus (E) ? 12.411 GPa; Poisson?s ratio ? 0; shear modu-
lus (G) ? 0 GPa). This test also con?rmed stress distribution
and linearity, with output values (stress) deviating up to 8%
in comparison with Bovine material. Both of the alternative
materials tested do not alter the general results of our study.
Therefore, there is no reason to believe that biologically rea-
sonable changes in material properties would modify our
conclusions.
3) With estimates of the body weight and the proximal joint sur-
face area of a given bipedal tridactyl dinosaur, one can
roughly calculate the loading conditions on a single toe in a
standing still posture. Camptosaurus and Allosaurus had a
body weight of 
10 kN (calculated based on femoral circum-
ferences 
300 mm for USNM 6061, USNM 5959, and USNM
8424; Anderson et al., 1985) and a proximal joint surface area
of 
30 to 40 cm2. Corythosaurus and Saurolophus had a body
weight between 70 and 100 kN (Seebacher, 2001), and a proxi-
mal joint surface of 50?60 cm2. Using these estimates, we
derive for a single toe a load of 
0.5 MPa (1 MPa ? 1,000 kN/
m2) for Camptosaurus and Allosaurus, and a load of 2?3 MPa
for Corythosaurus and Saurolophus. These values fall well
within the range of values tested in our models (between
0.0001 and 300 MPa). It is important to mention that the re-
sultant stress is actually a linear function of the applied load.
In other word, the stress distribution is independent of the
load magnitude itself. Therefore, even if the estimates above
for realistic loading conditions (0.5?3 MPa) are inaccurate, our
results remain valid.
Loading was applied normal to the joint surface, under the
assumption that the cartilage and synovial capsule would
transmit most normalized forces. This is based on theoretical
models (Matthewson, 1982; Dar and Aspden, 2003), which es-
tablish that the synovial liquid (uncompressible) as well as
the cartilage elasticity redistributes and homogenizes loads.
Real conditions might differ from theoretical ones, and are
worth further study, but these conditions are used here to
facilitate calculations in the present study.
4) Mobility was constrained by ?xing the distal joint in all direc-
tions (Fig. 2A), in order to simulate limitations on movement
due to the presence of a subsequent phalanx, the ground reac-
tion force (GRF), and the collateral ligaments when the foot
was in contact with the ground. Tendon force was not consid-
ered in the study, because it would introduce a dynamic struc-
ture, thus beyond the scope of the present analysis.
5) Output stress values are expressed as a percentage of the
load applied. This method permits a correct interpretation of
the data, since the numbers presented here have little rela-
tionship with other experimental or in vivo values. Stress
values (Von mises) can be obtained simply by multiplying
the magnitude of the load in N/m2 applied and dividing by
100. Values were tested between 1,000 and 300,000,000 N/
m2 (see above).
6) For all FEA results, color range settings were standardized
based on the highest and lowest percentages found after all
the model calculations were completed (27?338%). This pro-
vides a visual means for comparing communicating stress
distributions between the models.
These loading and constraint conditions correspond to a
static analysis of the stance phase in locomotion. As the pha-
langes were modeled as isolated elements, and loading magni-
tude and direction have no signi?cant effect, our model will
reveal general stress distributions for any phalanx at a given
instant when the foot is in contact with the ground. This means
that our modeled phalanges could correspond to any location in
the foot (different phalanges, digits, or sides), as well as differ-
ent foot postures during weight-bearing walking phases (early
stance, weight bearing, kick off), but always (and only) under
static conditions.
Internal Morphology
We obtained images of the internal structure of the bones by
CT scanning, using a Somatom AR.SP scanner (Siemens Corpo-
ration) at the National Museum of Natural History (Smithsonian
Institution). We scanned the ?rst pedal phalanges of four taxa:
Allosaurus, Camptosaurus, a juvenile Corythosaurus, and Sauro-
lophus. The ?rst three were scanned using a consistent ?eld of
view (FOV) of 116 mm2 (512 3 512 voxels) and 1 mm slice thick-
ness. The single specimen of Saurolophus (AMNH 5271) required
a larger FOV of 350 mm2 (512 3 512 voxels) and 2 mm slice
thickness because it was permanently mounted on a plaster base.
These images revealed the general trabecular orientation
and density of the internal structure of the bones, which are
known to have some relationship with the orientation of princi-
pal compressive or tensile stresses, as well as the magnitude of
shear stresses (Wolff, 1870; Hayes et al., 1982; Bertram and
Swartz, 1991; Gefen and Seliktar, 2004). We tested these obser-
vations against independent results from the FEA of two-
dimensional models (see above).
In the CT images, the gray scale indicates material density,
with white as the highest value and black as the lowest (e.g.,
Fig. 8). However, it is important to note that high density
(white) does not necessarily indicate dense fossilized bone, but
could also correspond to a harder element such as quartz (per-
haps in?lling the medullary cavity), or to a transition between
a surrounding low-density material (air) to the higher-density
fossil (often creating a white outline).
No extant taxa were included in the current analysis. This
deliberate omission re?ects the signi?cant anatomical differen-
ces between most modern animals and non-avian dinosaurs,
which present a speci?c loading problem in each case and are
beyond the scope of the present investigation. For example,
birds display a distinct limb orientation in steady standing: a
horizontal femur and a near-vertical lower limb, which would
54 K. MORENO ET AL.
Journal of Morphology DOI 10.1002/jmor
transmit a large amount of the load from the metatarsal ends
to the ground and a minor part to the pes (Carrano and Biew-
ener, 1999; Farlow et al., 2000), thus minimizing the participa-
tion of the phalanges in supporting body weight. A different but
analogous result would be expected for reptiles due to their
sprawling leg posture. Finally, mammals, which seem to have
closer limb postures and locomotion biomechanics with dino-
saurs (Carrano, 1997, 1998, 2001), exhibit a distinct ankle anat-
omy, with a greater participation of tarsals rather than pha-
langes. All these variables require further study and the devel-
opment of more complex models.
RESULTS
External Morphology
The distal joint curvature is approximately circu-
lar in lateral view, and the collateral ligament fossa
is located close to the center of rotation (Fig. 4A).
However, the penultimate phalanges are an excep-
tion; they achieve a larger ventral joint surface
through a reduction of dorsal width and increase in
ventral width. Here, when the collateral fossa is
Fig. 5. Joint surface topography in pedal phalanges. A) Measurements taken in dorsal view
(curve, chord), distal joint surface (sagittal furrow), showing the curvature calculation. B) Graph
of the average sagittal furrow depth.
Fig. 4. Distal joint curvature in pedal phalanges. A) Measurements taken in lateral view
(curve, chord), showing the curvature calculation. B) Graph of the average curvature for each
digit in the studied specimens.
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 55
Journal of Morphology DOI 10.1002/jmor
present (Camptosaurus, Allosaurus, and ratites)
and displaced dorsally, it generates an angle with
respect to the ligament that attaches to the ungual.
The depth of the collateral ligament fossa can be
greater on either the lateral (Camptosaurus) or
medial side (Allosaurus), or both may be equal
(ratites). On the other hand, Saurolophus and Cor-
ythosaurus lack such fossae, and the distal joint
remains roughly symmetrical, although the outer
sides are better developed in digits II and IV.
The average curvature (Fig. 4B) of Corythosau-
rus phalanges is nearly constant and close to 1.0
for all three digits. In contrast, digits II and III of
Camptosaurus seems to be at least as curved as
those of Allosaurus if not more, but in general cur-
vature remains constant between and within digits
(a low standard deviation). Allosaurus has one of
the largest digit IV curvatures, even more than
the average in birds, whereas birds have the larg-
est distal joint curvatures in digits II and III. Rat-
ites show a large standard deviation in all digits.
This re?ects the high curvature of proximal pha-
langes and relatively lower curvature of distal
phalanges. In Figure 4B, Dromaius and Rhea plot
together within the same standard deviation.
For most taxa we examined, lateral digits have
a wider dispersal of values than the central one
(Fig. 5B), and show a better-developed sagittal
ridge. This is especially the case for digit IV, where
we found the greatest depth values. With the
exception of Camptosaurus, the third digit
presents a low sagittal ridge, and all digit III pha-
langes plot together. Corythosaurus and Saurolo-
phus retain low depth values for all digits, which
is indicative of their derived hadrosaurid condition
(i.e., ?attened joint surfaces).
To summarize, the phalangeal curvature (char-
acteristic associated with movement range) and
the development of the sagittal ridge (related to
phalangeal interlocking) show a general decrease
in the following order: ?rst theropods (Allosaurus
and the birds) together with Camptosaurus, and
?nally hadrosaurids. An exception to the rule is
digit III of Camptosaurus, which has a deep sagit-
tal ridge and contrasts with all the other taxa
examined. Curvature is consistent between the
digits in ornithopods, whereas it shows greater
variability in theropods.
Finite Element Analysis 2D
In general, our 2D FEA models exhibit their
highest stress zones at the contact between the
truncated cone and circle (i.e., the phalanx neck;
Fig. 6), where the extremes of the constraints are
located. The lowest stresses are distributed toward
the distal joint. Logically, these stress patterns are
highly in?uenced by the geometric properties of
the phalanx. The cone acts as a funnel, concentrat-
ing loads toward the outside edges of the narrow
section, and the circle ef?ciently focuses them near
the loading point, which is evident in the model
results (see Fig. 6). Even when these geometric ?g-
ures are fused, with smooth edges, the stress dis-
tribution pattern remains fairly constant (Fig.
7.1B,D).
Shortening the shaft length (Fig. 7.1A?D) in-
creases the maximum stress (compare between
Figs. 7.1A,C and 7.1B,D) but tends to lower the
minimum stress. Therefore, the range of stress
values is wider, and high loads are concentrated in
the small area of the phalanx neck (see Fig. 2);
this region exhibits the highest stress of all the ex-
perimental models (Fig. 7.1C).
Small increases in the concavity of the proximal
joint surface (Fig. 7.2A?D) generate a small decrease
in maximum stress (Fig. 7.2B,C), but a deeper concav-
ity with sharp edges produces higher stress along
this surface (Fig. 7.2D). Hence, the potential bene-
?ts (lower stress range) of increasing the proximal
concavity are limited. Minimum stress remains con-
stant and distally located, which means that
changes to the morphology of the proximal concavity
have no effect on the distal joint surface, in contrast
to the previous example. These models also show
larger stresses distributed along the walls, leaving
Fig. 6. Stress distribution in the basic geometrical shapes
used to construct our 2D phalanx model. A) Truncated cone; B)
Circle. Gray arrows show the application of stress; gray trian-
gles indicate where the structure was ?xed against motion. In-
ternal stress levels are shown from highest (red) to lowest
(blue). Note that the truncated cone concentrates stress toward
the distal part, whereas the circle effectively concentrates it
near the point of application (black arrows).
56 K. MORENO ET AL.
Journal of Morphology DOI 10.1002/jmor
Fig. 7. 2D model of a phalanx in FEA, showing effects of morphological variation. Row 1 varies shaft length and ??neck?? presence: 1A)
original shape, considered a ??long shaft??; 1B) removal of ??neck?? from original shape; 1C) shortened shaft; 1D) shortened shaft without
??neck??. Row 2 (A?D) varies the depth/curvature of the proximal concavity. Row 3 (A?D) demonstrates a decrease in the proximal joint
width. Row 4 (A?D) demonstrates a decrease in the distal joint convexity. Row 5 shows the effect of combining narrow proximal width
(3D) with ?attened distal and proximal joints (4D). Column A represents the same model in each row, for ease comparison.
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 57
Journal of Morphology DOI 10.1002/jmor
an internal region with low stress; this was not
observed in any of the other experiments.
The reduction of proximal joint surface width
causes a general decrease in stress (Fig. 7.3A?D),
which becomes more evenly distributed along the
shaft. This experiment caused the greatest overall
reduction in stress.
Reducing the convexity of the distal joint surface
(Fig. 7.4A?D) raises the minimum stress but
slightly decreases the maximum stress. Therefore,
a ?at structure produces higher but more evenly
distributed stresses.
When the two last characteristics are combined,
decreasing the proximal concavity and the distal
convexity (Fig. 7.5), the resulting stress has a very
low range. This variation exhibited the lowest
maximum stress of all the experiments.
Internal Morphology
From proximal to distal, the sagittal sections of
Allosaurus (Fig. 8.1A) and Camptosaurus (Fig.
8.2A) phalanges show a conical structure with
thick walls of compact bone. This structure is ?lled
internally by a gradient of small (proximal) to
large (distal) trabeculae, which give way to a large
medullary cavity (mc; Fig. 8.1A,B, 8.2A,B). Both
distal joints reveal evenly distributed trabeculae.
Bone layering can be observed within either dorso-
ventral section of the midshafts (Fig. 8.1B, 8.2B).
The only difference is the shape of the dorsoven-
tral cross-section, which is kidney-shaped in
Camptosaurus and circular in Allosaurus.
It is important to note that Allosaurus shows no
major internal structures in CT images (Fig. 8.1).
Unfortunately, the specimen was longitudinally
drilled to insert a metallic support, and hence was
highly fractured. These factors resulted in an
altered CT image, in which the conical gradient of
the proximal trabeculae is only slightly noticeable.
However, it was possible to examine its internal
bone architecture by direct observation of the bro-
ken parts as isolated elements. This direct evi-
dence shows an internal structure that is similar
to Camptosaurus.
Corythosaurus (Fig. 8.3A) has an internal struc-
ture with more evenly distributed trabeculae than
Allosaurus and Camptosaurus. Although the tra-
beculae also form a smooth conical gradient, the
medullary cavity and compact bone are absent.
Large trabeculae lie near the edges of the bone
(Fig. 8.3B), and no layering can be identi?ed.
Saurolophus (Fig. 8.4A,B) reveals much more
evenly distributed trabeculae than the other speci-
mens, with no conical gradient. The sagittal sec-
tion (Fig. 8.4A) shows a small zone in the internal
part of the midshaft that contains slightly larger
trabeculae, but a clear medullary cavity is lacking.
In the dorsoventral section, one ??layer?? passes par-
allel to the shaft edge and disappears near either
joint (Fig. 8.4B). This layer may be a scanning ar-
tifact: the plaster mounting adds another material
interface, which could have produced additional X-
ray re?ection/refraction. However, observations of
broken hadrosaurid phalanges (phalanx III-3,
Edmontosaurus sp., UCM 42353) indicate that this
dense CT ??layer?? could correspond to the boundary
of a zone with smaller (and therefore denser) tra-
beculae located along the medial and lateral pe-
rimeter. The other narrow dense zone, which runs
from the dorsal edge toward the center of the pha-
lanx (Fig. 8.4B), could also be an artifact. Regard-
less, the salient observation here is that CT
images con?rm the absence of the medullary cav-
ity and a more homogeneous trabecular size com-
pared with the other dinosaurs.
DISCUSSION
Pedal Mobility and Flexibility
Interpreting the data in terms of the ?exion-
extension ability of the joints (distal joint curva-
ture; Fig. 4B) and their ability to resist torsional
loads (depth of the sagittal ridge; Fig. 5B), we note
that Camptosaurus retains high digit ?exibility,
the primitive condition and, hence, more similarity
to Allosaurus (see Fig. 9). Accordingly, Camptosau-
rus has a well-developed interlocking phalangeal
morphology that counteracts torsional loads. This
morphology can be observed even in the third
digit, whereas the rest of the animals studied
(including birds) show a very shallow sagittal
ridge. One possible consequence is an asymmetri-
cal step, in which the animal walked with the pes
angled or rotated inward (digits III and IV have
deeper sagittal ridges than digit II).
In Allosaurus, digit ?exibility seems generally
conservative. Here, digits II and III are less ?exi-
ble than in the ratites, but digit IV has a remarka-
ble mobility (Fig. 9C, D), exceeding that seen in
the birds. The interlocking phalangeal morphology
is also well developed in the lateral digits and, in
contrast to Camptosaurus, suggests a more sym-
metrical step in Allosaurus.
Dromaius and Rhea have similar morphologies
to one another (see Fig. 2), and therefore their
pedal function is approximately equivalent, as is
evident from their similar locomotory habits
(Abourachid and Renous, 2000). The fourth digit
has reduced mobility and shortened phalanges,
presumably working as a stiffer element in com-
parison with the other digits.
On the other hand, Corythosaurus (juvenile) and
Saurolophus have little ?exibility in all three dig-
its. This imparts a low resistance to torsion, even
in the lateral digits where all the other animals
studied have some development of a sagittal ridge.
This is typical for a derived ornithopod, and can be
explained as a consequence of the more upright
position of the pes (Fig. 10). This reorientation
58 K. MORENO ET AL.
Journal of Morphology DOI 10.1002/jmor
aligns the pes closer to the main direction of the
GRF, with a resultant loss of digit mobility.
The presence of collateral ligament fossae and
their position relative to the distal joint, together
with the symmetry of the distal curvature in lateral
view, provides additional information about ?exion-
extension ability. The phalanges studied present
symmetrical distal curvature, therefore are built to
contribute equally to extension and ?exion, and the
collateral ligaments constrain and guide their range
Fig. 8. Internal structure in pedal phalanges in sagittal (A) and cross-section (B). 1) Allosau-
rus, second phalanx, digit III; 2) Camptosaurus, ?rst phalanx, digit III; 3) Corythosaurus, ?rst
phalanx, digit III; and 4) Saurolophus, ?rst phalanx, digit III. mc ? medullary cavity. Not to scale.
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 59
Journal of Morphology DOI 10.1002/jmor
of motion. Therefore, movement is restricted dor-
sally and greater ?exion is supported (but extension
is reduced) in asymmetrical phalanges, with a bet-
ter-developed ventral side and more dorsally placed
collateral ligament. This is the case for the penulti-
mate phalanges of Camptosaurus, Allosaurus, and
the ratites. Their unguals are probably slightly
extended neutrally, with the proximal joint resting
high on a footpad, while only a portion of the
ungual contacts the ground. The absence of these
characteristics in Corythosaurus and Saurolophus
indicates that the ungual is more closely aligned
with the preceding phalanx, and therefore less
extended neutrally. This suggests a different func-
tion of the footpad in hadrosaurids, which evenly
supports the entire pes.
Phalangeal Morphology as a Consequence
of Pedal Loading
In most of the animals studied, digit III has a
very low sagittal ridge (and shallow corresponding
furrow) in each of the phalanges (Fig. 5B). The
sagittal ridge works to reinforce the dorsoventral
rotation of the joint. Its weak development (or ab-
sence) indicates that digit III might be subject to
low torsional loads, and therefore must be medio-
laterally aligned with the GRF. This is con?rmed
by experiments carried out in starlings and quail
(Middleton, 2003), which showed that the center of
pressure is in fact located along digit III (which
shows a lower sagittal ridge) and the lateral digits
act later during the walking phase. Variations of
pedal anatomy induced minor changes in the posi-
tion of the center of pressure, but it always main-
tained its place within the middle digit.
Most of the animals studied showed prominent
sagittal ridges in digits II and IV (Fig. 5B). This
indicates that the outer digits offer more resist-
ance to torsional loads, probably re?ecting their
main function as stabilizers during standing and
walking, as well as their secondary weight-bearing
function. Moreover, digit IV appears to have an
even more accentuated sagittal ridge, which sug-
gests that this digit, in particular, is usually under
larger torsional moments than digit II. Thus the
contribution of the digits to locomotion and sup-
port is unequal, and speci?cally is biased toward
the midline of the pes in the animals studied.
The FEA study is consistent with observations
of internal bone structure in these taxa. Compact
bone lines the walls of convexo-concave phalanges
(Fig. 8.1, 8.2), where the zones of highest stresses
are found in the respective FEA models (Fig.
7.2B?D). Cancellous bone with small trabeculae is
present close beneath the proximal joint surface
(Fig. 8.1, 8.2), which is the same relative position
as the elevated stresses (Fig. 7.2B?D). These small
trabecular zones are underlain by a zone of larger
trabeculae and a substantial medullary cavity
(Fig. 7.2B?D), matching the location of a signi?-
cant low-stress zone in the FEA model. In ?at-
tened phalanges, the trabecular architecture is
more homogeneous, and compact bone is largely
absent internally (Figs. 7.3, 7.4, 8.3, 8.4). These
patterns closely match the loading distributions
generated by our models.
Taken together, the alignment of the foot, tra-
becular structure, and loading distribution support
the inference that the ?attened phalanges of
hadrosaurids re?ect a marked modi?cation of foot
function from the primitive ornithopod (and dino-
saur) condition. This transition involved a change
Fig. 9. Reconstructions of pedal mobility using 3D element
scans. The pedal phalanges of Camptosaurus (A, B) and Allo-
saurus (C, D) were placed in maximum ?exion (A, C) and maxi-
mum extension (B, D). Note that in each case, digit II shows
the least mobility, but that the two taxa differ with regard to
whether digit III or IV is the most mobile.
60 K. MORENO ET AL.
Journal of Morphology DOI 10.1002/jmor
in pedal posture toward subunguligrady, restric-
tion of ?exion-extension movements, and homoge-
nization of stress distributions and corresponding
internal bony structures (see Fig. 10).
Function and Evolution
of the Ornithopod Pes
Phalanges with highly convexo-concave joint
surfaces are bene?cial for bipedal animals. As they
have only two supporting limbs, bipedal animals
face greater structural requirements on the con-
tact area of the pes, especially if it is to provide
equilibrium for the entire body. It is possible to
achieve this with long digits that exhibit high, con-
trolled ?exibility, thereby forming a ??stabilizer
platform.?? By contrast, quadrupedal animals are
more stable (Muller and Verhagen, 2002) and
therefore are capable of reducing the contact area
of the foot. It is not a coincidence, perhaps, that no
bipedal animal exhibits an unguligrade stance dur-
ing free standing.
Flattened phalanges with narrow proximal joint
surfaces, in combination with restricted mobility
and upright posture, create a ??columnar support,??
which represents the best structure for longitudi-
nal (axial) loadings. This is also the best arrange-
ment for bone resistance to compressive loading
(Currey, 2002); thus this morphology would be able
to support higher loads and be bene?cial for
larger-bodied animals. It seems logical, then, that
large dinosaurs such as sauropods, ceratopsians,
and stegosaurs, along with large mammals such as
rhinocerotids and proboscideans, share this pha-
langeal morphology.
Another important feature for phalangeal func-
tion is the ??neck?? (see Fig. 5). This structure is a
stress concentrator but also reduces the stress in
other zones, especially the distal joint surface
(compare between models in Fig. 7.1). In light of
these results, small weight-bearing phalanges with
a narrow neck seem improbable, because this
small bone would have to support more loading
per unit volume than a larger one, and the stress
concentration in the phalanx neck could easily
exceed bone resistance. Note that a small phalanx
with a pronounced neck (Fig. 7.1C) exhibits the
highest stress values of all the experiments. This
might explain the reduction of the ??neck?? in
derived pedal phalanges of ornithopods and other
large-bodied animals.
The general shape of a bone is determined ge-
netically. Nevertheless, as a living tissue, a bone
responds to changes in loading by modifying its
size, density, and internal arrangement (Currey,
2002). Thus, the ?nal morphology of a bone
depends signi?cantly on its mechanical situation.
This relationship between loading and bone struc-
ture was ?rst recognized by Wolff (1870), and is
popularly known as ??Wolff ?s law of bone transfor-
mation.?? Although this so-called ??law?? has been
challenged (Bertram and Swartz, 1991; Cowin,
1997), several studies have shown that in many
cases trabecular structure tends to correlate with
the direction of principal strains, while trabecular
density and location of compact bone correlate
with the magnitude of shear stresses (Hayes et al.,
1982; Thomason, 1985; Lanyon, 1990; Biewener
et al., 1996). Moreover, strains slightly higher
than normal stimulate positive remodeling, and by
contrast, lower routine strains lead to bone loss
(Rubin and Lanyon, 1982). It is important to note
that the internal structure of a bone does not pres-
ent an optimal engineering design for loading,
since this tissue has to deal with its vital cellular
functions as well, such as gas, nutrient and waste
exchange, as well as regulation of calcium avail-
ability. Therefore, bone structure re?ects only gen-
eral loading patterns. However, the identi?cation
of these patterns is important because it is usually
Fig. 10. Schematic summary of dinosaur phalanx morpho-
function. A) sagittal section of a typically digitigrade phalanx
(Allosaurus and Camptosaurus), which present a highly concave
proximal joint, conically oriented trabeculae; ??neck?? with inter-
nal medullary cavity and external compact bone; and a highly
convex distal joint with more homogeneous trabeculae. These
features are associated to higher ?exibility, resistance to torsion
and stress. B) sagittal section of a typically subunguligrade
phalanx (Corythosaurus and Saurolophus), which displays a
more ?attened (external) and homogeneous (internal) structure.
These characteristics are related to lower ?exibility, resistance
to torsion and stress.
PEDAL EVOLUTION IN ORNITHOPOD DINOSAURS 61
Journal of Morphology DOI 10.1002/jmor
very dif?cult to determine what forces are acting
on a bone or even less obvious what stresses are
acting inside it.
When looking at the changes that occurred in
ornithopod evolution, it is clear that on the line to
Hadrosauridae, ornithopods drastically altered
posture, changing the pes from a ??stabilizer plat-
form?? to a ??sub-columnar?? structure. The associ-
ated soft tissues also altered their function. For
digitigrade bipeds, pads act as energy-absorbing
cushions and are typically digit-speci?c, but for
subunguligrade quadrupeds, these digit pads
became united beneath the pes and acquired an
additional role in support.
CONCLUSIONS
This study examined the pedal phalanges of sev-
eral dinosaurian taxa, as well as theoretical mod-
els of vertebrate phalanges. The results demon-
strate correlative relationships between several
aspects of external and internal pedal morphology,
pedal posture, and bone loading. These suggest
that the observed changes in pedal structure
within ornithopod dinosaur evolution are indica-
tive of signi?cant alterations in foot posture and
function.
Speci?cally, Camptosaurus and theropods (Allo-
saurus, Rhea, and Dromaius) exhibited many of the
primitive (basal) conditions of the dinosaur foot: con-
cavo-convex joints, marked processes for the attach-
ment of the ?exor and extensor tendons, excavated
collateral fossae, a dorsal position of these fossae in
the penultimate phalanges, a neutral extended claw,
and weak sagittal ridges in the lateral digits.
In Camptosaurus, the presence of well-developed
sagittal ridges in digit III (middle one) suggests
that there was high ?exibility in all digits, and
possibly a mediolaterally asymmetric step. The
weak development of the sagittal ridge in digit III
of Allosaurus may indicate a more symmetrical
step, but digit IV had higher ?exibility, as evi-
denced from its strong joint curvature and marked
sagittal ridge. Both ratites also show high joint
curvature and development of the sagittal ridge in
lateral digits, revealing a particularly elevated
?exibility in digits II and III, and a symmetrical
step, despite the stiffer digit IV. In general, digit
III is the main weight bearer; lateral digits (II and
IV) are under higher torsional moments, with digit
IV being more strongly affected. Taken together,
this suggests that locomotion in the specimens
studied might have been biased toward the mid-
line of the pes.
In contrast, hadrosaurids (Corythosaurus and
Saurolophus) possessed a derived pedal morphol-
ogy, including ?attened phalanges, absence of col-
lateral ligament fossae, and loss of processes for
the attachment of ?exor and extensor tendons.
This morphology suggests that hadrosaurids had a
more upright pedal posture than basal ornitho-
pods, which was closely aligned to the main direc-
tion of the GRF during standing. Furthermore, the
lack of a stress concentrator (phalanx neck) and
the reduction of joint curvature allowed the hadro-
saurid pes to support high loads more effectively
than the primitive ornithopod pes.
FEA models show loading patterns that are con-
sistent with trabecular structure, allowing us to
assume that: primitive pedes (e.g., Allosaurus and
Camptosaurus) are well-suited to work as ??stabi-
lizer platforms,?? which require high, controlled ?ex-
ibility. On the contrary, derived pedes (i.e., hadro-
saurids) are well adapted to ??columnar support??
and resistance to high loads.
Although this research was focused on certain
dinosaurs, the functional morphological issues dis-
cussed here can be applied to other terrestrial tet-
rapods. Non-ungual phalanges are morphologically
simple, but at the same time are directly relevant
to numerous aspects of animal posture and behav-
ior. This makes future comparisons between verte-
brates especially promising with regard to prob-
lems of stabilization versus functionality, increas-
ing body size, and postural changes during
evolution.
ACKNOWLEDGMENTS
The authors thank Bruno Fro?lich and Evan Gar-
ofalo for their invaluable assistance in obtaining
the CT scan data and Peter Kroehler for providing
the ratite pedal bones used in this study. Emily
Ray?eld, John Hutchinson, Erick Snively, Colin
McHenry, Biren Patel, Andrew Lee, Ryan Ridgely,
Brian Richmond, Stephen Gatesy, Corwin Sulli-
van, Jennifer Scott, and two anonymous reviewers
for providing constructive criticism in various
aspects of the manuscript, and Stephen Wroe for
further assistance.
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