Three-Dimensional Geometric Morphometric Analysis of Talar Morphology in Extant Gorilla Taxa from Highland and Lowland Habitats
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THE ANATOMICAL RECORD 298:277–290 (2015)
Three-Dimensional Geometric
Morphometric Analysis of Talar
Morphology in Extant Gorilla Taxa
from Highland and Lowland Habitats
RYAN P. KNIGGE,1* MATTHEW W. TOCHERI,2,3 CALEY M. ORR,4
1
AND KIERAN P. MCNULTY
1
Evolutionary Anthropology Lab, Department of Anthropology, University of Minnesota,
Minneapolis, Minnesota
2
Human Origins Program, Department of Anthropology, National Museum of Natural
History, Smithsonian Institution, Washington, DC
3
Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology,
The George Washington University, Washington, DC
4
Department of Anatomy, Midwestern University, Downers Grove, Illinois
ABSTRACT
Western gorillas (Gorilla gorilla) are known to climb significantly
more often than eastern gorillas (Gorilla beringei), a behavioral distinc-
tion attributable to major differences in their respective habitats (i.e.,
highland vs. lowland). Genetic evidence suggests that the lineages lead-
ing to these taxa began diverging from one another between approxi-
mately 1 and 3 million years ago. Thus, gorillas offer a special
opportunity to examine the degree to which morphology of recently
diverged taxa may be “fine-tuned” to differing ecological requirements.
Using three-dimensional (3D) geometric morphometrics, we compared
talar morphology in a sample of 87 specimens including western (low-
land), mountain (highland), and grauer gorillas (lowland and highland
populations). Talar shape was captured with a series of landmarks and
semilandmarks superimposed by generalized Procrustes analysis. A
between-group principal components analysis of overall talar shape sepa-
rates gorillas by ecological habitat and by taxon. An analysis of only the
trochlea and lateral malleolar facet identifies subtle variations in troch-
lear shape between western lowland and lowland grauer gorillas, poten-
tially indicative of convergent evolution of arboreal adaptations in the
talus. Lastly, talar shape scales differently with centroid size for highland
and lowland gorillas, suggesting that ankle morphology may track body-
size mediated variation in arboreal behaviors differently depending on
ecological setting. Several of the observed shape differences are linked
biomechanically to the facilitation of climbing in lowland gorillas and to
stability and load-bearing on terrestrial substrates in the highland taxa,
providing an important comparative model for studying morphological
variation in groups known only from fossils (e.g., early hominins). Anat
Rec, 298:277–290, 2015. V C 2014 Wiley Periodicals, Inc.
Key words: foot; arboreality; terrestriality; talus; tarsals
Grant sponsor: Wenner-Gren Foundation; Grant number: Received 3 October 2014; Accepted 11 October 2014.
7822. DOI 10.1002/ar.23069
*Correspondence to: Ryan P. Knigge, Department of Anthro- Published online in Wiley Online Library (wileyonlinelibrary.
pology, University of Minnesota, Minneapolis, MN 55454, USA. com).
E-mail: knigg008@umn.edu
C 2014 WILEY PERIODICALS, INC.
V
278 KNIGGE ET AL.
The talus serves as the connection between the bones areas, and curvatures), focused solely on variation
of the lower limb and those of the rest of the foot. Proxi- among gorillas (Dunn et al., 2014). This study employed
mally, the talus articulates with the tibia and fibula to two specific measurements to compare gorilla taxa: the
form the talocrural joint complex, and distally it articu- mediolateral curvature of the trochlear surface (meas-
lates with the calcaneus to form the subtalar joint and ured using quadric surface fitting; see Marzke et al.,
the navicular as a part of the midtarsal complex. Among 2010 for methodological details) and the surface area of
primates, the talus is centrally involved in plantarflexion- the lateral malleolar facet relative to the entire talar
dorsiflexion and abduction-adduction of the foot at the area (see Tocheri et al., 2005 for methodological details).
talocrural joint, supination-pronation at the subtalar These articular surfaces are of interest based on the
joint, and plantarflexion-dorsiflexion at the midtarsal expectation that strong mediolateral curvature of the
joint (Levangie and Norkin, 2011). Thus, primate talar trochlea and a larger relative lateral malleolar facet
morphology is a reasonably strong indicator of foot func- area (resulting in a higher lateral trochlear rim) result
tion in living taxa, and is useful for interpreting locomo- in a more inverted foot posture, which is biomechani-
tor adaptations in fossil hominins (Latimer et al., 1987; cally advantageous for movement on arboreal substrates
Latimer, 1991; Gebo and Schwartz, 2006; DeSilva, 2008, (Latimer et al., 1987). Conversely, a flatter trochlear sur-
face and smaller relative lateral malleolar facet area
2009; DeSilva and Devlin, 2012; Su et al., 2013). Multiple
result in a more neutral foot position favorable for ter-
studies have included analyses of primate talar shape
restrial locomotion and limiting mediolateral excursion
and functional morphology using a wide variety of meth-
of the foot (Latimer et al., 1987; Harcourt-Smith and
odological approaches (Lisowski et al., 1974; Wood,
Aiello, 2004; DeSilva, 2008). The results showed that
1974a,b; Langdon, 1986; Latimer et al., 1987; Lewis, talar shape falls along a morphocline that tracks func-
1989; Harcourt-Smith, 2002; Berillon, 2004; Gebo and tion in terms of differing frequencies of arboreal behav-
Schwartz, 2006; Jungers et al., 2009; Marivaux et al., iors, which vary according to ecological habitat (Dunn
2010, 2011; Turley and Frost, 2013). Regardless of et al., 2014). Lowland gorillas have tali characterized by
whether these studies used a more traditional morpho- relatively higher lateral trochlear rims and more medio-
metric approach or three-dimensional (3D) geometric laterally curved trochleae, similar to other arboreally-
morphometrics, the overall results have been similar: adapted primates (Gebo and Schwartz, 2006; Turley and
there is substantial talar shape variation among primate Frost, 2013), whereas highland gorillas have relatively
taxa, and this variation is partitioned according to differ- even trochlear rims and mediolaterally flatter troch-
ences in ankle function, substrate use/preference, body leae—more broadly similar to modern human tali (Dunn
mass, and phylogeny. Here, we specifically evaluate the et al., 2014).
relationship between morphological variation in the talus
and the ecology and locomotor substrate use within the
genus Gorilla.
Ecological Differences Among Gorillas
Three-dimensional talar shape has recently been stud- Gorillas living in lowland areas, which comprise equa-
ied by Turley and Frost (2013), who used geometric mor- torial rainforest habitats typically below 900 m above
phometrics to study variation in a sample of extant sea level (ASL) (Mayaux et al., 2004), climb and eat fruit
catarrhines. In their study, a set of 30 landmarks (modi- more often than those living in highland areas (Casimir,
fied from Harcourt-Smith, 2002) was used to quantify 1975; Tuttle, 1970; Goodall and Groves, 1977; Tuttle and
the morphology and size of each talus, and subsets of Watts, 1985; Tutin et al., 1991; Yamagiwa et al., 1992;
these were analyzed to quantify and compare the proxi- Tutin and Fernandez, 1993; Remis, 1994; Yamagiwa and
mal (trochlea, lateral and medial malleolar facets) and Mwanza, 1994; Doran, 1996; Goldsmith, 1996; Yamagiwa
distal (talar head and posterior calcaneal facet) articular et al., 1996; Doran and McNeilage, 1998; Remis, 1998;
surfaces separately. They found that overall talar mor- Goldsmith, 1999; Goldsmith, 2003; Robbins and McNei-
phology was greatly influenced by size and by substrate lage, 2003; Ferriss, 2005). These lowland habitats often
preference (Turley and Frost, 2013). Looking separately include high-canopied, continuously-distributed forests
at the proximal and distal articular surfaces, however, that provide ample opportunities for gorillas to exploit
they demonstrated that proximal facet shapes covary seasonal fruits and build nests atop large supports (Tut-
with the frequency of arboreal and terrestrial behaviors tle, 1970; Tuttle and Watts, 1985; Tutin et al., 1991;
while distal facet shapes reflect phylogeny as well as Tutin and Fernandez, 1993; Remis, 1994, 1998; Gold-
substrate preference (Turley and Frost, 2013). They smith, 1996, 1999; Doran and McNeilage, 1998; Ferriss,
show that components of talar shape associated with ter- 2005). In contrast, highland gorilla habitats are com-
restrial substrates have proximal articulations that posed of montane rainforest that are typically above
reflect stability for dorsiflexion (e.g., smaller, flatter 1,500 m ASL (Mayaux et al., 2004) and provide fewer
medial and lateral malleolar facets and a higher, flatter arboreal opportunities or incentives for gorillas. For
trochlea) in addition to distal articulations that exhibit instance, trees are smaller and less continuously distrib-
medial axis stability (e.g., a flatter, laterally placed pos- uted, and seasonal fruits are scarce (Schaller, 1963;
terior calcaneal facet and a flat talar head). Conversely, Groves, 1970, 1971; Tuttle, 1970; Fossey and Harcourt,
shape components coinciding with arboreality demon- 1977; Tuttle and Watts, 1985; Doran, 1996; Doran and
strate flexibility in movement while remaining stable on McNeilage, 1998, 2001; Stewart et al., 2001; Robbins
unsteady substrates (e.g., asymmetric trochlear rims, a and McNeilage, 2003).
deep trochlear groove, a concave and posteriorly placed Although direct quantitative comparisons of climbing
posterior calcaneal facet) (Turley and Frost, 2013). frequency among gorilla taxa are lacking, a reasonable
Another recent study analyzed talar shape using non- proxy derives from examinations of the number of fruit
geometric morphometric methods (joint angles, surface species in the diet of different gorilla taxa, which reflects
3D GEOMETRIC MORPHOMETRIC ANALYSIS OF GORILLA TALAR SHAPE 279 the relative climbing effort needed to incorporate fruit tain gorillas derive from highland localities. Museum and other arboreal resources into the diet (Remis, 1994, records were used to determine collection localities and 1998). Robbins and McNeilage (2003) compared the altitude (Fig. 1; Table 1). Nearly all specimens (N 5 84) number of fruit species they observed in Bwindi moun- were scanned using a NextEngine 3D Scanner HD laser tain gorillas with those of multiple studies of other goril- scanner (macro setting, 16 scans per orientation, mini- las. Their comparisons show a clear relationship mum two orientations per bone). ScanStudio HD PRO between the number of fruit species in gorilla diet and software was used to align and merge each set of scans, altitude: Virunga (Karisoke) mountain gorillas (2,700– and the resulting surface was subsequently exported as 3,400 m ASL) had 1 fruit species in their diet (Watts, a triangular mesh. The triangular meshes of each bone 1984; Vedder, 1984); Bwindi mountain gorillas (1,300– were then aligned, merged, and digitally cleaned using 2,400 m ASL) had 16 different species (Robbins and Geomagic Studio software, and then exported as a final McNeilage, 2003); highland populations of grauer goril- 3D model. The remaining three specimens were digitized las (1,800–3,300 m ASL) had 20 fruit species whereas using a SIEMENS Somatom Emotion CT scanner (110 lowland grauer gorillas (600–1,300 m ASL) had 48 kV, 70 mA, 1 mm slice thickness, 0.1 mm reconstruction (Yamagiwa et al., 1992, 1994, 1996); western lowland increment, H50 moderately sharp kernel). Final 3D mod- gorillas (
280 KNIGGE ET AL.
Fig. 1. Map of central Africa showing the current distribution of gorillas sampled are from the southern range shown (i.e., Virunga
extant gorilla taxa as described by the IUCN (International Union for localities only). The insert provides a closer view of the eastern gorilla
Conservation of Nature) red list of threatened species. Only western distribution (G. beringei) which also specifies the ranges of mountain
lowland (G. g. gorilla), mountain (G. b. beringei), and grauer (G. b. gorillas and highland versus lowland grauer populations.
graueri) gorilla subspecies were used in this study. All of the mountain
TABLE 1. Sample sizes by taxon, habitat, sex, and museum collectiona
Western (G. g. gorilla) Grauer (G. b. graueri) Mountain (G. b. beringei)
Lowland Lowland Highland Highland
Collection Male Female Unknown Male Female Unknown Male Female Male Female Unknown
AMNH 3 5 1
USNM 5 3 1 2 2
RMCA 1 2 1 8 6 2 4
ANSP 4 2
MCZ 2 2
ASU 1
RBINS 1 1 11
MSGP 5 9 1
KNM 1 1
Total by sex 16 13 2 3 1 11 8 6 11 15 1
Total by taxon 31 15 14 27
a
Museum abbreviations: AMNH: American Museum of Natural History, New York; USNM: United States National
Museum; RMCA: Royal Museum for Central Africa; ANSP: Academy of Natural Sciences, Philadelphia; MCZ: Museum of
Comparative Zoology; ASU: Arizona State University; RBINS: Royal Belgian Institute of Natural Sciences; MSGP: Moun-
tain Gorilla Skeletal Project; KNM: National Museums of Kenya.
warp the shape space as do approaches based on order to preserve the articular shapes and their anatomic
canonical variates. positions/orientations within the talus. This approach pro-
An initial BGPCA was performed on the full set of 189 vides a further test of previously published results, which
landmarks and semilandmarks to assess variation in highlighted the shape variation of the trochlea and lateral
overall talar morphology. A separate analysis was also malleolar articular surfaces related to ecological con-
carried out using only the 66 semilandmarks of the troch- straints and substrate preferences both within gorillas
lear and lateral malleolar surfaces. Data for the latter and among various catarrhine taxa (Dunn et al., 2014;
analysis were extracted following specimen superimposi- Turley and Frost, 2013). Both BGPCAs were performed
tion of the full set of landmarks and semilandmarks in using SAS 9.3 software (SAS Institute, Cary NC).
3D GEOMETRIC MORPHOMETRIC ANALYSIS OF GORILLA TALAR SHAPE 281
Fig. 2. Landmarks visualized on a western lowland gorilla right talus in (a) dorsal, (b) plantar, (c) poste-
rior, and (d) anterior views. Semilandmarks patches were placed on the 6 articular surfaces (outlined in
blue) using a set of 30 landmarks (white circles) as anchors, and 5 landmarks (red circles) were selected
from nonarticular areas.
Lastly, to explore the effects of overall talar size on grauer) from lowland (western and lowland grauer)
morphology, we computed a multivariate regression of gorilla populations rather than distinguishing the gorilla
the shape variables on log centroid size and display the species, G. gorilla and G. beringei. The shape compo-
size/shape relationship by plotting multivariate regres- nents that coincide with separating highland from low-
sion scores against log centroid size for each group. land gorillas are visualized in Figure 4a. For example,
Lacking a direct measure of body mass for these speci- low values for BGPC 1 represent a higher lateral troch-
mens, log centroid size of the talus was used as a good lear rim that extends more dorsally than the medial
proxy for overall body size (cf., Parr et al., 2011). The rim, an anteriorly extended and mediolaterally
multivariate regression scores were computed and restricted trochlear head, and flatter lateral malleolar
exported using MorphoJ (Klingenberg, 2011). and posterior calcaneal facets. Conversely, higher values
for BGPC 1 depict a flatter trochlear surface and talar
RESULTS head, and more concave lateral malleolar and posterior
calcaneal facets (Fig. 4a).
Overall Talar Morphology
Taxonomic differences become apparent on BGPC 2
Results of the BGPCA on overall talar morphology are (34.3%), where grauer gorillas separate from the other
illustrated in Figures 3 and 4. The first between-group two populations, in particular highland grauer gorillas
PC axis explains 47.4% of among-group variance and separate from western gorillas (Fig. 3a). The shape com-
roughly separates highland (mountain and highland ponents driving the variation along this axis depict a
282 KNIGGE ET AL.
Fig. 3. Plots of the between-group PCA using the full set of 189 components that separate highland grauer gorillas from western goril-
landmarks and semilandmarks with 95% concentration ellipses: (a) las at opposite ends of BGPC 2 include the depth of the trochlear
BGPC 1 vs. 2 and (b) BGPC 1 vs. 3. BGPC 1, 2, and 3 account for groove, the anteroposterior length of the posterior calcaneal facet,
47.4, 34.3, and 18.3% of the total among-group variance, respectively. and width of the flexor hallucis longus groove. Variation driving BGPC
BGPC 1 roughly separates highland from lowland gorillas and thus 3 highlights the curvature of the anterior trochlear region and medial
highlights shape components associated with ecological variation malleolar facet. The four gorilla groups are represented as: western-
(e.g., height of the lateral trochlear rim, shape of the talar head, and 5 green triangles; lowland grauer 5 orange squares; highland
curvature of the lateral and posterior calcaneal facets). The shape grauer 5 purple squares; and mountain 5 red diamonds.
flatter or slightly convex trochlear surface, an anteropos- shape of the lateral trochlear rim. Positive values dem-
teriorly shorter posterior calcaneal facet, and mediolater- onstrate a more dorsally expanded central aspect of the
ally narrower flexor hallucis longus groove as higher lateral trochlear rim (Fig. 6c).
values are attained along this vector (Fig. 4b). The final Interestingly, the shape changes associated with sepa-
component (BGPC 3) accounts for the residual variance rating highland and lowland gorillas in the full dataset
(18.3%) and reflects the variation of lowland grauer and are distributed across the first and third axes of the
mountain gorillas from highland grauer and western trochlea and lateral malleolar facet analysis, but in a
gorillas (Fig. 3b). The morphology described along this more subtle manner. For example, the positive ends of
vector includes variation in the curvature of the anterior BGPC 1 and 3 of the reduced dataset (occupied by low-
trochlear region and medial malleolar facet and the land grauer and western gorillas, respectively in Figs.
anteroposterior length of the anterior calcaneal facet 5a,b) are both associated with increased height (i.e., dor-
(Fig. 4c). sally extended) of the lateral trochlear rim, which is also
visualized along BGPC 1 of the full dataset (Figs. 3a,
4a). However, this configuration is achieved differently
Trochlea and Lateral Malleolar Facet
as each vector primarily influences a different aspect of
Analysis of the trochlea and lateral malleolar facet the trochlear rim. Lowland grauer gorillas have an
highlighted more subtle variations in surface morphol- expanded posterior trochlear rim (Fig. 6a) while western
ogy that are partitioned across the three between-group gorillas have a higher central trochlear rim (Fig. 6c),
PC shape vectors. Figure 5a shows a continuum along and these shape characteristics are evident in examples
BGPC 1 with mountain gorillas and lowland grauer of actual lowland grauer and western gorilla tali rather
gorillas occupying opposite ends of the distribution. In a than only these components of shape variation (Fig. 7).
visualization of this vector (Fig. 6a), higher values repre-
sent an expansion of the posterior, lateral trochlear rim
Size and Shape
in the dorsal/posterior direction and conversely a reduc-
tion of this aspect for lower values. The variation along Results comparing talar shape with talar size show a
BGPC 2 highlights the distinct nearly convex trochlea significant correlation between the regression scores and
for low values (coinciding with the range for highland log centroid size for all four gorilla groups (Table 2).
grauer gorillas) resulting from a dorsal expansion of the This is not surprising given the substantial difference
central aspect of the trochlear surface (Fig. 6b). Along between males and females in body size. However, there
this axis, western, mountain, and lowland grauer goril- is a clear difference between highland and lowland popu-
las retain slightly positive values while highland grauer lations in the way talar shape scales with size (Fig. 8).
gorillas are markedly negative. The shape differences As tali from both highland and lowland populations
reflected along BGPC 3 are again associated with the increase in size, their size-correlated components of
3D GEOMETRIC MORPHOMETRIC ANALYSIS OF GORILLA TALAR SHAPE 283
Fig. 4. Visualization of shape change along (a) BGPC 1, (b) BGPC 2, vature of the talar head and posterior calcaneal facet; BGPC 2—cur-
and (c) BGPC 3 for the full talar landmark set. The models represent vature of the trochlear groove, width of the flexor hallucis longus
idealized shapes at the ends of the corresponding BGPC axes. The groove, and anteroposterior length of the posterior calcaneal facet;
following aspects of morphology contain the major shape components BGPC 3—anterior extension of the anterior calcaneal facet and curva-
for the specified BGPC axes: BGPC 1—lateral trochlear rim and cur- ture of the medial malleolar facet and anterior trochlear surface.
shape converge on a morphology that is similar among differences plausibly related to variation in locomotor
adult males of all groups. behavior, such as differences in hand and foot segmental
proportions (Sarmiento, 1994; Jabbour, 2008), hallucal
abduction (Tocheri et al., 2011), cross-sectional geometry
DISCUSSION
through ontogeny (Ruff et al., 2013), and vertebral for-
Previous studies of primate tali that included gorillas mula (Williams, 2012).
have primarily sampled western lowland gorillas Our results also suggest that ecology plays a signifi-
(Gorilla gorilla gorilla) (Harcourt-Smith, 2002; Berillon, cant role in shaping gorilla talar morphology, corroborat-
2004; Gebo and Schwartz, 2006; Jungers et al., 2009; ing and extending the results of previous work. When
Parr et al., 2011). However, an analysis focused solely on considering morphological differences among group
gorilla talar morphology demonstrated dramatic varia- means, the largest component of variation distinguishes
tion related to ecological differences among populations those populations that live in low-elevation equatorial
(Dunn et al., 2014). Figure 7 provides a comparison of rainforests from those who inhabit high-elevation mon-
actual gorilla tali from each group demonstrating the tane rainforests. This distinction runs counter to estab-
diversity of talar shape among extant gorillas. Other stud- lished genetic relationships that have identified
ies of gorilla anatomy have documented morphological mountain and grauer gorillas as sister taxa to the
284 KNIGGE ET AL. Fig. 5. Results from the between-group PCA of only the trochlea rior and central portions of the lateral trochlear rim, respectively. and lateral malleolar facet with 95% concentration ellipses: (a) BGPC BGPC 2 reflects variation in the curvature of the trochlear groove. The 1 vs. 2 and (b) BGPC 1 vs. 3. BGPC 1, 2, and 3 account for 49.8, four gorilla groups are represented as: western 5 green triangles; low- 36.4, and 13.8% of the total among-group variance, respectively. land grauer 5 orange squares; highland grauer 5 purple squares; and BGPC 1 and 3 are associated with changes in the height of the poste- mountain 5 red diamonds. exclusion of western taxa (Ruvolo, 1997; Saltonstall to the long axis of the tibia) during habitual foot pos- et al., 1998; Jensen-Seaman and Kidd, 2001; Jensen- tures used on arboreal versus terrestrial supports. In Seaman et al., 2003; Jensen-Seaman et al., 2004; Thal- particular, the asymmetry in height (i.e., dorsal exten- mann et al., 2005; Anthony et al., 2007a,b; Thalmann sion) of the medial and lateral trochlear rims exhibited et al., 2007; Scally et al., 2012). Rather than reflecting by lowland gorillas results in a cone-shaped articular phylogenetic relationships, as one might expect in a surface with a supratalar joint space that is oblique to landmark-based study (see Bookstein, this volume), the plantarflexion-dorsiflexion axis of the ankle. This major aspects of talar morphology of lowland grauer arrangement is thought to impart concomitant adduction gorillas resemble that of the more distantly related west- of the foot with plantarflexion and abduction with dorsi- ern gorillas, suggesting that these shape data provide a flexion, which in turn results in an abducted knee and functional rather than phylogenetic signal. lateral travel of the shank over the ankle when the foot Western gorillas are known to engage in substantially is planted on a substrate (Latimer et al., 1987). Such a more arboreal activities than mountain gorillas as a configuration probably allows for habitually abducted result of residing in more densely forested lowland lower limb postures and inverted foot positioning (sole of regions (Tutin et al., 1991; Remis, 1994; Doran, 1996; the foot turned medially toward the substrate) as used Goldsmith, 1996; Remis, 1998; Goldsmith, 1999). Corre- in vertical climbing and above-branch quadrupedal spondingly, field studies have shown that mountain behaviors (Meldrum, 1991; Isler, 2005). gorillas are primarily terrestrial and have a less varied In contrast to the more asymmetrical medial and lat- locomotor repertoire than western lowland gorillas eral talar trochlear rims and more curved trochlear sur- (Schaller, 1963; Groves, 1970, 1971; Tuttle, 1970; Fossey face seen in lowland gorillas, the more equal rim heights and Harcourt, 1977; Tuttle and Watts, 1985; Doran, and flatter trochlea in highland gorillas are broadly sim- 1996; Doran and McNeilage, 1998, 2001; Stewart et al., ilar to the condition exhibited by humans (Dunn et al., 2001; Robbins and McNeilage, 2003). Grauer gorillas are 2014). This likely facilitates the use of plantigrade foot interesting in this regard because, though more closely postures in which the sole of the foot is oriented approxi- related to mountain gorillas, they inhabit both highland mately perpendicular to the long axis of the tibia when and lowland habitats (Mehlman, 2008). Comparing the the sole is placed downward (e.g., Latimer et al., 1987; shapes delineated along BGPC 1 of the full talar dataset Harcourt-Smith and Aiello, 2004; DeSilva, 2008). In (Fig. 4a), one can see that differences between highland humans, the tibial platform is also slightly cone-shaped, and lowland gorillas bear out the functional predictions and this results in plantar flexion being coupled with made by Dunn et al. (2014). abduction of the foot and dorsiflexion being coupled with Understanding the exact functional significance of the adduction (Inman, 1976). However, because the suprata- differences among gorilla taxa warrants further detailed lar joint space is more approximately parallel to the biomechanical study. However, the most likely possibility inferred plantarflexion-dorsiflexion axis of the ankle, is that differences in ankle morphology impact “foot set” concomitant mediolateral deviations of the foot may (the orientation of the plantar surface of the foot relative occur to a lesser degree than in highland gorillas.
3D GEOMETRIC MORPHOMETRIC ANALYSIS OF GORILLA TALAR SHAPE 285 Fig. 6. Visualization of shape change along BGPC 1 (a), BGPC 2 (b), tain the major shape components for the specified BGPC axes: BGPC and BGPC 3 (c) for the trochlea and lateral malleolar facet only. Simi- 1—height of the posterior aspect of the lateral trochlear rim; BGPC lar to Fig. 4, the models represent idealized shapes at the ends of the 2—curvature of the trochlear groove; BGPC 3—height of the central corresponding BGPC axes. The following aspects of morphology con- aspect of the lateral trochlear rim. Consequently, the knee should travel over the planted restricted range of joint positions (c.f. Hamrick, 1996). foot in a path that more closely approximates a parasag- Specifically, DeSilva (2008) suggests that the highly ittal plane. This anatomical arrangement combines a keeled talar trochlea (of lowland gorillas and most non- foot position that should be more stable on relatively human anthropoids according to DeSilva’s data) may flat, terrestrial substrates with efficient lower leg kine- help to maintain joint congruence during forceful inver- matics while walking on the ground (Latimer et al., sion of the foot because the lateral trochlear lip abuts 1987). the fibula closely in such positions. With a less pro- Whether or not Latimer et al.’s (1987) model for nounced lateral lip, the talus can “tilt” away from the lower limb kinematics applies to gorillas requires fur- distal tibia and fibula, decreasing overall joint congru- ther experimental validation as well as complementary ence, possibly damaging ligaments and cartilage during morphometric work on the rest of the lower limb. Alter- high impact loading. As with the current study, DeSilva natively (or as a complement to the kinematic model), (2008) found that humans and mountain gorillas have the more mediolaterally curved talocrural surface of much flatter (non-keeled) talocrural articular surfaces. lowland gorillas (associated with the asymmetrical Regardless of the exact mechanism involved, the appa- trochlear rims) may better accommodate a varied load- rent convergence of talocrural joint shape between ing regime as might be expected on irregular arboreal bipedal humans and highland gorillas suggests that supports, while the overall flatter joint of highland this shared condition is the result of adaptation to ter- gorillas may maximize load transmission efficacy in a restrial substrates.
286 KNIGGE ET AL.
Fig. 7. Examples of actual tali from each gorilla group in posterior, dorsal, lateral, and plantar views.
Each talus is a 3D model of an actual specimen and falls near the mean values for each particular group
in the analysis so as to approximate the mean morphology for that group.
TABLE 2. Multivariate regression of shape variables gorillas may constrain their abilities to frequently climb
on log centroid size (CS) and engage in other arboreal positional behaviors. Such
sex differences in arboreal behavior may be driven by
Regression scores vs. log(CS) the seasonal variation in fruit availability with female
R2 P value western lowland gorillas maintaining a consistent level
of arboreality regardless of fruit distribution, while
Western (lowland) 0.49 0.00001 males become more terrestrial and less frugivorous
Grauer (lowland) 0.77 0.00002 when fruit is scarce or only accessible on smaller, termi-
Grauer (highland) 0.53 0.00300 nal branches (Remis, 1999). The scaling relationship
Mountain (highland) 0.26 0.00610
between log centroid size and talar shape in western
and lowland grauer gorillas (Fig. 8) suggests that larger-
Differences in the scaling relationship of talar size bodied individuals (inferred by talar centroid size) attain
and shape among gorillas also support the hypothesis a talar morphology more closely resembling that of the
that certain aspects of the morphology may be associated larger-bodied terrestrial highland gorillas. This is con-
with substrate use. Behavioral data indicate that male sistent with a model by which morphological variation
and female mountain gorillas are similar in their degree tracks body-size mediated differences in substrate use in
of terrestriality (Tuttle and Watts, 1985; Doran, 1996, lowland taxa (which largely manifest as male/female dif-
1997; Remis, 1998). In contrast, western lowland gorillas ferences due to the pronounced size dimorphism in
exhibit sex differences in the proportion of time spent on gorillas).
arboreal substrates (Remis, 1995, 1999). Remis (1995) Although a significant relationship between talar size
has suggested that the large body size of male western and shape also exists for both mountain and highland3D GEOMETRIC MORPHOMETRIC ANALYSIS OF GORILLA TALAR SHAPE 287
In both our study and that of Turley and Frost (2013),
the variations in trochlear and lateral malleolar facet
shape reflect the degree to which catarrhine primates
(including gorillas) engage in arboreal versus terrestrial
behaviors. Furthermore, Turley and Frost (2013) suggest
that the shapes of the distal facets are greatly influenced
by phylogeny and, to a lesser degree, substrate prefer-
ence. In our study, we did give specific attention to only
the shapes of the distal facets, but the results yielded
plots and shape vectors similar to the analysis using the
whole talus (Figs. 3, 4). In this regard, the main aspects
of distal facet shape variation are related to ecological
differences (highland versus lowland) rather than phy-
logeny (eastern versus western). The distal facet shapes
found to be related to substrate preference in catar-
rhines demonstrate that arboreal forms have a more
concave posterior calcaneal facet and a rounder, more
convex talar head relative to terrestrial forms (Turley
and Frost, 2013). In our analysis, the more arboreal low-
land gorillas share a similarly rounded and convex talar
head, but conversely have a flatter posterior calcaneal
facet (Figs. 4a, 7) in comparison to the more terrestrial
highland gorillas. This may suggest that the gorilla talus
is uniquely modified in relation to terrestrial and arbo-
real behaviors in at least some ways that deviate from
Fig. 8. Plot of the multivariate regression scores of the full landmark
dataset against log(centroid size) to illustrate the relationship between
the general catarrhine pattern.
talar shape variation and talar size across the four gorilla groups (see One of the benefits of 3D geometric morphometrics is
Table 2 for regression statistics). All gorilla groups exhibit a significant the ability to detect more subtle variations in shape that
relationship between the size and shape of the talus, although the may be overlooked or difficult to quantify using other
lowland groups appear to scale differently in comparison with the methods; this is particularly evident in the shape of the
highland gorillas which may reflect the variation in substrate use. lateral trochlear rim. Dunn et al. (2014) used the rela-
Western 5 green; lowland grauer 5 orange; highland grauer 5 purple; tive area of the lateral malleolar facet to indirectly
mountain 5 red; males 5 plus signs; females 5 squares; unknown 5 - approximate the degree to which the lateral trochlear
triangles. Blue boxes indicate specimens belonging to captive
rim extends dorsally. They found that western gorillas
individuals.
have the largest relative lateral malleolar area; however,
among eastern gorillas, relative lateral malleolar area
did not differ significantly (Dunn et al., 2014). In this
grauer gorillas (Fig. 8), it may be a consequence of sex analysis, we found higher lateral trochlear rims in both
differences or allometric scaling that is unrelated to dif- western and lowland grauer gorillas, but, importantly,
ferences in substrate use, as behavioral observations each group achieves this configuration in a different
suggest that mountain gorilla males and females are way, expanding different aspects of the lateral trochlear
more similar in substrate use than are lowland gorillas rim. The central portion of the lateral trochlear rim is
(Remis, 1994; Doran-Sheehy et al., 2009). This relation- dorsally expanded in western gorillas (Fig. 6c) while the
ship between body size (inferred by talar size) and sub- posterior portion is expanded posteriorly and dorsally in
strate use could be further tested with ontogenetic lowland grauer gorillas (Fig. 6a). These specific charac-
samples. For example, Ruff et al. (2013) found signifi- teristics of the lateral trochlear rim are also evident in
cant changes in inter-limb strength proportions occurred actual western and lowland grauer gorilla tali displayed
abruptly in infant mountain gorillas at around 2 years in Figure 7. Although these minor variations are detect-
of age. Their result corresponds with ontogenetic behav- able through analysis of 3D shape, they likely achieve
ioral data that show mountain gorillas become signifi- similar functional results, and may be evidence for inde-
cantly less arboreal/more terrestrial at this age (Doran, pendently evolved adaptations to arboreality in each lin-
1997; Ruff et al., 2013). Unfortunately, the gorilla talus eage, rather than representing the possible primitive
is not completely ossified until well after this age so it condition for all living gorillas.
would be difficult to study in terms of external shape. The results from this study have implications for
However, one might predict that trabecular structure or interpreting the paleobiology and evolution of extinct
orientation within the gorilla talus may vary according taxa including fossil hominins. Indeed, although all
to ontogenetic locomotor behavioral patterns, although known fossil hominin feet show clear primary adapta-
such an approach has thus far produced mixed results tions to bipedality, there is a surprising amount of diver-
for adult hominoid tali (DeSilva and Devlin, 2012; Su sity in early hominin talocrural morphology that does
et al., 2013). not necessarily follow a temporal trend or to be consist-
The research presented here focuses specifically on ent within lineages (Harcourt-Smith and Aiello, 2004;
gorilla tali, but certain aspects of the results substanti- Gebo and Schwartz, 2006). For example, tali attributed
ate the conclusions of Turley and Frost (2013) regarding to Australopithecus afarensis (Hadar specimens AL288-
overall catarrhine talar morphology, and in particular 1as and AL333-147) have platform-like talocrural joint
those related to proximal facet shape and substrate use. surfaces with medial and lateral rims of more equal288 KNIGGE ET AL.
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