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Compliant walking in primates Elbow and knee yield in primates compared to other mammals.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 125:42–50 (2004)
Compliant Walking in Primates:
Elbow and Knee Yield in Primates
Compared to Other Mammals
Eileen Larney1 and Susan G. Larson2*
1
Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University,
Stony Brook, New York 11794-4364
2
Department of Anatomical Sciences, Stony Brook University School of Medicine, Stony Brook, New York 11794-8081
KEY WORDS
arborealism
limb compliance; limb yield; early primate evolution; marsupials;
ABSTRACT
It has been suggested that primates utilize a compliant gait to help reduce peak locomotor
stresses on their limbs (Schmitt [1994] J. Hum. Evol.
26:441– 458; Schmitt [1998] Primate Locomotion, p. 175–
200; Schmitt [1999] J. Zool. Lond. 248:149 –160). However,
the components of such a gait, i.e., increased step length,
prolonged contact time, and substantial limb yield, have
only been documented on a handful of primate species. In
order to explore the generality of this claim, elbow and
knee angles during walking were documented at touchdown, midstance, and liftoff in a sample of primates, carnivores, marsupials, rodents, and artiodactyls, all under
25 kg. Limb yield was calculated as the change in angle
from touchdown to midstance, and re-extension as the
change in angle from midstance to liftoff for both forelimbs
and hind limbs. Use of a compliant gait (as reflected in
significant limb yield) in primates was confirmed for both
forelimbs and hind limbs. However, there was variability
within primates in the degree of either elbow or knee
yield. Surprisingly, marsupials were found to exhibit almost as much elbow yield and even greater knee yield
than primates. Carnivores and rodents display a modest
amount of limb yield during walking, while artiodactyls
appear to display a relatively stiff gait. These data are
consistent with the suggestion that the use of a compliant
gait to attenuate peak substrate reaction forces may have
facilitated the primate invasion of a small-branch niche.
However, limb compliance (as reflected by elbow or knee
yield) does not appear to be exclusive to the primate order.
Am J Phys Anthropol 125:42–50, 2004.
Use of clawless, grasping extremities has long
been recognized as a distinctive characteristic of
primates (e.g., LeGros Clark, 1959). According to
current views on primate origins, this as well as
other early primate specializations can be related to
adaptations for foraging and feeding on small terminal branches (Cartmill, 1972, 1974, 1992; Rasmussan, 1990; Sussman, 1991; Hamrick, 1998; Fleagle,
1999). The use of clawless, grasping hands and feet
to forage and feed on small terminal branches has,
in turn, been either directly or indirectly related to a
variety of other morphological or behavioral specializations in primates. As Schmitt (1999) argued, traveling on small branches presents conflicting demands for long and mobile limbs to reach and grasp
discontinuous supports, and the necessity for keeping a low center of mass for balance. A crouching
posture is a means of resolving this conflict, but
raises a new problem of potentially high locomotor
stresses on the limbs due to large joint moments
created by a substrate reaction force vector that is
far removed from joint centers (Biewener, 1982,
1983, 1989; Schmitt, 1999). Primates, therefore,
need ways to improve stability on branches and to
attenuate high locomotor stresses on mobile, unstable limbs, especially the forelimbs.
In order to achieve one or both of these goals,
primates have evolved a suite of unusual locomotor
characteristics, including greater reliance on hind
limbs for both support and propulsion (Kimura et
al., 1979; Reynolds, 1985; Kimura, 1985, 1992;
Demes et al., 1994), use of a diagonal sequence/
diagonal couplets walking gait (Howell, 1944; Prost,
1965, 1969; Hildebrand, 1967; Rollinson and Martin, 1981; Vilensky, 1989; Vilensky and Larson,
1989), changes in muscle recruitment patterns (Lar-
©
2004 WILEY-LISS, INC.
©
2004 Wiley-Liss, Inc.
Grant sponsor: NSF; Grant number: BCS-0109331.
*Correspondence to: Susan G. Larson, Department of Anatomical
Sciences, Stony Brook University School of Medicine, Stony Brook,
NY 11794-8081.
E-mail: susan.larson@stonybrook.edu
Received 26 March 2003; accepted 18 June 2003.
DOI 10.1002/ajpa.10366
Published online 19 November 2003 in Wiley InterScience (www.
interscience.wiley.com).
43
LIMB YIELD IN PRIMATES
Fig. 1. Compliant gait model from Schmitt (1999). Schematic
primate forelimb is shown undergoing a step using a stiff gait
(solid line and open segments), and a compliant gait (dashed line
and hatched segments). Compliant shoulder follows a flatter path
during contact, maintains contact for a longer time, covers a
greater excursion angle, and displays significant yield at elbow. A
vertical force curve (solid line) for stiff limb has a short duration
and high peak, while that for compliant limb (dashed line) has a
longer time over which to develop force and thus yields lower
peak vertical force.
son and Stern, 1989; Larson, 1998), and use of relatively long stride lengths (Vilensky, 1980; Alexander and Maloiy, 1984; Reynolds, 1987) at
relatively low stride frequencies (Alexander and
Maloiy, 1984; Demes et al., 1990), brought about by
relatively long limb bones (Alexander et al., 1979)
and large limb angular excursions (Reynolds, 1987;
Larson et al., 2000, 2001). Demes et al. (1990) proposed that increased step length and stride length
allow a primate to achieve higher walking speeds
while avoiding the potential for branch sway caused
by a high-frequency gait. Increased step length can
also lead to prolonged contact time on a substrate,
which improves security and stability when traveling in a terminal branch habitat (Cartmill, 1985;
Larson et al., 2001). In addition, increased step
length and prolonged contact time, coupled with
substantial limb yield, are components of a compliant gait (McMahon, 1985; McMahon et al., 1987),
which Schmitt (1994, 1998, 1999) showed can reduce
peak locomotor forces on limbs in primates (Fig. 1).
He suggested that the use of a compliant gait to
attenuate peak forces may have facilitated the invasion of the small-branch niche by the earliest members of the primate order by allowing them to use a
crouched posture while having relatively long, mobile limbs.
Schmitt (1999), however, examined only the forelimb, and although he suggested that the use of a
compliant walking gait is rare among nonprimate
mammals, relatively few comparative data exist. Indeed, some partially arboreal nonprimate mamma-
lian species were found to display large limb angular
excursions (Larson et al., 2001), which could contribute to longer step lengths, a component of a compliant gait. Unfortunately, it has yet to be demonstrated whether any of these partially arboreal
species display the limb yield that is essential for a
gait to be truly compliant (Larson et al., 2001). The
goal of the present study is to test the assertion by
Schmitt (1999) of the general use of a compliant gait
in primates in contrast to a more stiff gait in nonprimate mammals, through documentation of elbow
and knee yield in a variety of mammalian species. In
the course of this study, the following questions will
be addressed: 1) Is forelimb compliance (as reflected
in elbow yield) universal in primates? 2) Is the primate hind limb also compliant? 3) Are primates the
only order to exhibit significant limb yield indicative
of a compliant walking gait? 4) Within primates (and
other mammalian groups that may be found to exhibit limb compliance), is there variability in limb
yield, and if so, is greater limb yield associated with
arboreality, supporting the proposal that limb compliance evolved as an accommodation to terminal
branch use?
METHODS
Limb positional data were derived from videotapes of captive animals taken at the following zoos
and research centers: Bronx Zoo, New York, NY;
Cleveland Zoo, Cleveland, OH; Pittsburgh Zoo,
Pittsburgh, PA; San Diego Zoo, San Diego, CA; Duke
Primate Center, Durham, NC; Primate Locomotion
Laboratory, Stony Brook, NY; and Laboratoire
d’Ecologie Générale, CNRS/Unité de Recherche
1183, Brunoy, France. Most of the videotapes were
recorded by one of the authors (S.G.L.) with a Panasonic AG 195 camcorder equipped with an electronic
shutter (1/500 sec) at 60 fields/sec. Additional video
was recorded by Pierre Lemelin using a Sony
HandyCam Super 8-mm camcorder, and by Mark
Hamrick using a Panasonic PV 900 camcorder. In
most cases, subjects were 5 or more meters from the
camera, minimizing parallax problems (Plagenhoef,
1979; Winter, 1990). Video analysis was performed
on a Panasonic AG-7500 VCR, using frame-by-frame
playback (60 frames/sec) to identify steps in which
the subject was traveling in a relatively straight
path, approximately perpendicular to the line of
sight of the camera. Only walking gaits were analyzed of steps on substrates inclined no more than
20° to the horizontal. As described in Larson et al.
(2000, 2001), the nature of the data source makes it
impossible to control for speed or substrate type, or
to correct for any out-of-plane motion. The latter was
especially problematic in regard to documenting
knee angles in lorisids, which display considerable
hind limb rotation during a step. We were therefore
unable to collect knee angle data for Perodicticus
potto or Nycticebus pygmaeus, but were able to substitute three-dimensional (3D) elbow and knee angles for Loris tardigradus and N. coucang, gener-
44
E. LARNEY AND S.G. LARSON
Fig. 2. Drawing of brown lemur Eulemur fulvus walking on a
pole, taken from video records to illustrate limb angles reported
here. Upper row shows elbow angles taken at forelimb touchdown
(TD), midsupport (Mid), and liftoff (LO). Lower row shows knee
angles taken at corresponding points for hind limb. Limb yield is
defined as change in angle from TD to Mid; limb re-extension is
change from Mid to LO.
ously given to us by Nancy Stevens who collected
biplanar kinematic data on these species (for a description of her methodology, see Stevens, 2003).
Video images were imported into a Pentium microcomputer with a MiroVIDO DC30 Plus (Pinnacle
Systems) frame grabber board, and digitized for
quantitative analysis using Peak Motus 2000 Software (Peak Performance Technologies, Inc.). Elbow
angle was defined as the anterior angle between a
midline axis of the arm (approximation of line between shoulder joint center and lateral epicondyle of
humerus) and forearm (approximation of line between lateral epicondyle of humerus to center of
wrist) of the forelimb, and knee angle was the posterior angle between a midline axis of the thigh
(approximation of line between hip joint center and
lateral epicondyle of femur) and leg (approximation
of line between lateral epicondyle of femur to center
of ankle) of the hind limb (Fig. 2). Elbow and knee
angles were documented at touchdown (TD), the
first frame in which the limb is in contact with a
support; midsupport (Mid), the point when wrist or
ankle was immediately below the shoulder or hip;1
and liftoff (LO), the termination of elbow or knee
extension near the end of stance phase, prior to the
limb flexion associated with lifting the hand or foot
off the ground for swing phase (Fig. 2). We elected to
document elbow and knee angles at the latter point
rather than when the hand or foot actually lost
contact with the substrate, since our goal was to
document the magnitude of change in limb flexion
through stance phase, and often hand or foot release
involves renewed flexion of the limb in preparation
for swing phase. Only quadrupedal mammalian species with an average body weight under 25 kg were
included in the study, since this encompasses the
1
According to data published by Schmitt (1994, 1998), midsupport
as defined here is the point of maximum elbow or knee flexion in
primates. We are making the assumption that this is also true for
nonprimates.
range of most primate species (Table 1). Efforts were
made to quantify at least 10 steps of both the forelimb and hind limb for each animal subject. However, this was not always possible (Table 1).
Limb yield was calculated as the change in angle
from TD to Mid, and re-extension from Mid to LO for
both forelimbs and hind limbs. Data were analyzed
in SPSS (version 11 for Windows). To avoid bias due
to unequal numbers of steps for different species,
species means were first derived, and group means
for each mammalian order were computed from species means. The nonparametric Kruskal-Wallis Test
for independence of samples was used to compare
group means (Conover, 1999). We chose to run this
nonparametric statistical test because our small
sample size did not meet certain criteria of parametric statistics. Correlation analysis using the nonparametric Spearman’s rho statistic on ranked data
was used to explore for relations to overall body size
and between different variables.
RESULTS
Mean elbow and knee angles at TD, Mid, and LO
for each group are reported in Table 2, and are
displayed along with error bars (mean ⫾ 2 SE) in
Figure 3a,b. Interestingly, primate forelimbs and
hind limbs are more extended at nearly every stage
of the step cycle than in other mammalian groups.
In regard to limb yield, all groups display some
decrease in elbow or knee angle at midphase; however, this decrease is most marked in primates and
marsupials.
To better illustrate these changes in limb angles,
mean yield (TD[3:Directions MT/86]Mid) and reextension (Mid[3:Directions MT/86]LO) angles for
the five groups are displayed in Figure 3c,d. The
Kruskal-Wallis tests for independence of samples
for forelimb and hind limb yield were significant at
P ⬍ 0.01. Primates display the greatest degree of
elbow yield, but are followed closely by marsupials.
Carnivores and rodents and others exhibit a modest
amount of elbow yield, while artiodactyls show the
least elbow flexion. Post hoc tests indicate that primates are significantly different from all groups except marsupials. For the hind limb, marsupials actually exceed primates in knee yield, although the
value for primates is also quite high. As with the
forelimb, carnivores, rodents, and others display a
modest amount of knee yield, and artiodactyls again
exhibit the smallest amount of knee flexion. Post hoc
tests again indicate that primates are significantly
different from all groups except marsupials.
Comparing forelimbs to hind limbs, carnivores,
marsupials, and artiodactyls all display slightly
greater knee yield than elbow yield. For primates
and rodents and others, the reverse situation obtains, but in all cases, the differences are fairly
small.
Several individual species outside the primate
and marsupial groups exhibit substantial limb yield
that is masked in the ordinal averages. The fossa
45
LIMB YIELD IN PRIMATES
TABLE 1. List of species studied
Taxon
Carnivores (n ⫽ 10)
Ailurus fulgens
Arctictis binturong
Cryptoprocta ferox
Eira barbara
Felis caracal
Leopardus wiedi
Nasua nasua
Neofelis nebulosa
Suricata suricatta
Vulpes corsac
Marsupials (n ⫽ 5)
Caluromys philander
Dasyurus maculatus
Dendrolagus matschiei
Phascolarctos cinereus
Primates
Anthropoids
Cercopithecoids (n ⫽ 15)
Cercocebus galeritus
Cercopithecus ascanius
Cercopithecus diana
Cercopithecus lhoesti
Cercopithecus neglectus
Chlorocebus aethiops
Colobus angolens
Erythrocebus patas
Nasalis lavartus
Macaca mulatta
Mandrillus sphinx
Papio anubis
Trachypithecus auratus
Trachypithecus cristata
Trachypithecus francoisi
Ceboids (n ⫽ 7)
Alouatta seniculus
Aotus trivirgatus
Cebuella pygmaea
Lagothrix lagothricha
Pithecia pithecia
Saguinus geoffroyi
Saimiri sciureus
Prosimians
Lemuroids (n ⫽ 5)
Daubentonia madagascariensis
Eulemur fulvus
Hapalemur griseus
Lemur catta
Lorisoids (n ⫽ 4)
Loris tardigradus
Nycticebus coucang
Nycticebus pygmaeus
Perodicticus potto
Rodents and others (n ⫽ 6)
Dasyprocta aguti
Dinomys branickii
Dolichotis patagonum
Myoprocta acouchy
Tupaia glis
Artiodactyls (n ⫽ 5)
Gazella dorcas
Madoqua guentheri
Muntiacus muntjac
Neotragus moschatus
Sylvicapra grimmia
1
Body size (kg)
No. of
steps FL
No. of
steps HL
4.00
11.50
9.50
4.50
16.00
2.501
4.00
15.201
0.79
5.50
3
6
5
8
9
2
3
6
7
13
0
0
3
4
6
0
3
0
7
10
0.30
2.50
7.20
9.30
6
8
6
16
6
4
0
12
7.40
3.31
4.55
5.901
5.501
3.62
8.62
9.45
20.40
9.90
22.25
19.20
7.102
6.18
7.52
13
3
15
1
2
11
4
11
7
12
18
14
9
6
4
2
2
9
0
0
11
3
12
4
14
13
14
7
5
3
Red howler monkey
Owl monkey
Pygmy marmoset
Woolly monkey
White-faced saki
Geoffroy’s tamarin
Squirrel monkey
5.95
0.77
0.12
7.15
1.76
0.49
0.72
17
11
2
10
5
6
8
10
10
2
11
9
5
8
Aye aye
Brown lemur
Gentle lemur
Ring-tailed lemur
3.00
2.21
0.94
2.21
13
14
13
14
0
9
10
9
Slender loris
Slow loris
Pygmy slow loris
Potto
0.19
0.65
0.42
1.10
304
304
9
9
304
304
0
0
Orange-rumped agouti
Pacarana
Patagonian cavy
Acouchy
Tree shrew
2.65
12.50
12.50
0.95
0.17
16
3
12
3
2
13
2
10
4
2
Dorcas gazelle
Guenther’s dik dik
Muntjac
Suni
Gray duiker
17.50
4.60
16.00
6.50
18.50
11
2
2
6
2
9
0
2
7
3
Common name
Red panda
Binturong
Fossa
Grey headed tayra
Caracal
Margay
Coati
Clouded leopard
Meerkat
Corsac fox
Woolly opossum
Quoll
Tree kangaroo
Koala
Tana River mangabey
Red-tailed monkey
Diana monkey
L’Hoest’s guenon
DeBrazza’s monkey
Vervet monkey
Angolian colobus monkey
Patas monkey
Proboscis monkey
Rhesus macaque
Mandrill
Olive baboon
Ebony langur
Silvered langur
Francois langur
Body size estimate from Nowak (1999).
Body size estimate from Rowe (1996); otherwise from Larson et al. (2001).
3
Data from Krakauer et al. (2002).
4
Data from Stevens (2003).
2
46
128.90 ⫾ 2.20
126.63 ⫾ 4.27
122.74 ⫾ 2.71
117.51 ⫾ 4.72
113.60 ⫾ 4.14
10.86 ⫾ 1.82
7.32 ⫾ 4.55
17.97 ⫾ 7.86
6.91 ⫾ 3.89
1.87 ⫾ 4.83
The goal of this project was to document change in
elbow and knee angles through a walking step in a
variety of primates and nonprimate mammals. This
was done by documenting angles at three discrete
points in the step cycle, and calculating the changes
Standard error.
121.93 ⫾ 3.36
117.61 ⫾ 3.07
101.61 ⫾ 1.55
107.57 ⫾ 3.84
103.01 ⫾ 2.80
22.60 ⫾ 1.98
9.66 ⫾ 2.89
19.94 ⫾ 6.98
11.64 ⫾ 2.96
2.54 ⫾ 3.93
144.53 ⫾ 1.991
127.27 ⫾ 3.59
121.55 ⫾ 8.26
119.20 ⫾ 3.66
105.54 ⫾ 4.75
Primates
Carnivores
Marsupials
Rodents and others
Artiodactyls
DISCUSSION
1
Re-extension
Mid
118.03 ⫾ 3.19
119.31 ⫾ 1.95
104.77 ⫾ 5.15
110.60 ⫾ 5.33
111.74 ⫾ 6.24
22.02 ⫾ 1.98
12.03 ⫾ 3.36
22.56 ⫾ 3.67
8.77 ⫾ 2.68
6.16 ⫾ 2.37
140.05 ⫾ 3.17
131.35 ⫾ 4.57
127.33 ⫾ 3.79
117.90 ⫾ 6.65
117.90 ⫾ 6.65
142.22 ⫾ 2.27
127.89 ⫾ 2.57
109.27 ⫾ 3.80
123.38 ⫾ 5.22
118.73 ⫾ 7.43
Hind limb
Yield
TD
LO
Re-extension
Mid
Forelimb
Yield
TD
Group
TABLE 2. Group mean elbow and knee angles (in degrees) at touchdown, midstance, and liftoff
(Cryptoprocta ferox) and tree shrew (Tupaia glis)
both display elbow yield around 20°, comparable to
that of most primates. The margay (Felis wiedi) also
displays substantial elbow yield. For the hind limb,
only the tayra (Eira barbara) displays an unusual
level of knee yield.
Mean touchdown, midsupport, and liftoff angles
for primates grouped into superfamilies are reported
in Table 3 and displayed in Figure 4a,b; Figure 4c,d
shows the mean changes in elbow and knee angles
for each of these groups. Elbow yield is most extreme
in lorisoids, followed by ceboids and lemuroids, and
is least in cercopithecoids (test for independence of
samples was significant at P ⫽ 0.01). Conversely,
the amount of knee yield is highest in ceboids and
cercopithecoids, and least in lorisoids (including
data only for L. tardigradus and N. coucang; see
Methods). However, the test for independence of
samples among primate superfamilies was not significant for knee yield. All primates but cercopithecoids flex their elbows more than marsupials on
average, but knee yield in marsupials is comparable
to that of the anthropoid species. Correlation analysis across the primate sample reveals a tendency
for larger species to have more extended elbows and
knees throughout a step, as predicted by Biewener
(1982, 1983, 1989; see also Polk, 2002), and to display smaller changes in elbow or knee angles (with
the exception of knee yield).2 There are also significant correlations between the degree of elbow yield
and re-extension, although not between knee yield
and re-extension.
Since many of the variables display some correlation to body size, partial correlation analysis (on
ranked data) was used to explore for intervariable
relationships, controlling for body size. Most of the
intervariable correlations do in fact appear to be due
to their mutual correlations to overall size. As might
be expected, there are significant negative partial
correlations between midsupport elbow angle and
forelimb yield (r ⫽ ⫺0.59, P ⬍ 0.01), indicating that
at any body size, the less extended the elbow is at
midsupport, the greater the degree of yield. Midsupport knee angle and hind limb yield did not display
a significant partial correlation, although hind limb
yield and forelimb yield are correlated to each other
(r ⫽ 0.49, P ⫽ 0.02).
20.29 ⫾ 1.67
10.28 ⫾ 2.44
7.66 ⫾ 3.44
15.81 ⫾ 3.89
15.73 ⫾ 6.02
LO
E. LARNEY AND S.G. LARSON
2
Spearman’s rank correlation coefficients to body weight: FL TD,
r ⫽ 0.48; FL Mid, r ⫽ 0.75; FL LO, r ⫽ 0.63; FL Yield, r ⫽ ⫺0.77; FL
Re-Ext, r ⫽ ⫺0.72; HL TD, r ⫽ 0.75; HL Mid, r ⫽ 0.75; HL LO, r ⫽
0.51; HL Yield, r ⫽ 0.05; HL Re-Ext, r ⫽ ⫺0.65; all except HL Yield
are significant at P ⬍ 0.01.
LIMB YIELD IN PRIMATES
47
Fig. 3. Error bars represent group means ⫾ 2 standard errors of mean for each
order. a: Error bars and
means for elbow angles at TD
(light gray), Mid (black), and
LO (dark gray). b: Error bars
and means for knee angles at
TD (light gray), Mid (black),
and LO (dark gray). On average, primates display more
extended limbs at nearly every stage of a step cycle than
other mammals. c: Error
bars and means for elbow
yield (black) and re-extension
(gray). d: Error bars and
means for knee yield (black)
and re-extension (gray). Average limb yield is high in
primates and marsupials,
modest in carnivores and rodents and others, and low in
artiodactyls.
in angle from touchdown to midsupport, and from
midsupport to liftoff. Our results demonstrate that
substantial yield at the elbow is universal among
primates, and that most primates, except lorisoids,
also display marked knee yield. To the degree that
limb yield is indicative of the use of a compliant gait,
these results support the assertion of Schmitt (1994,
1998, 1999) that primates as a group are characterized by use of a compliant gait. However, primates
are not unique in displaying limb yield: marsupials
also exhibit significant yield at both the elbow and
knee, and carnivores and rodents display modest
limb yield.
Only artiodactyls appear to use a genuinely stiff
(absence of yield) walking gait. They begin a step
with both their elbows and knees in flexed postures,
and while the elbow undergoes re-extension in the
second half of support phase, the knee angle remains largely unchanged through a step. It is possible, however, that artiodactyls may exhibit more
yield and/or re-extension at their ankle joint (hock)
rather than knee.
Within the primate order, there was variation in
limb yield and re-extension, especially for the hind
limb. Although larger species tend to display more
extended limbs and less elbow yield and limb reextension, most larger species are cercopithecoids
and smaller species are prosimians, making it difficult to separate size from phylogenetic influences. In
addition, some of the largest species in the sample
are terrestrial quadrupeds, adding the confounding
effect of substrate differences.
The fact that all primate groups except cercopithecoids typically display more forelimb yield than hind
limb yield supports suggestions that the dual role of
the forelimb for both locomotion and foraging/manipulation makes it especially vulnerable to high
locomotor stresses, and therefore, it is especially
advantageous if peak substrate reaction forces can
be attenuated to some degree, such as through the
use of a compliant gait (Schmitt, 1994, 1998, 1999).
However, this raises the question as to why cercopithecoids do not follow the same pattern. Of the
taxa examined here, cercopithecoids are unusual in
that they comprise the only group that includes terrestrial and semiterrestrial species. In their display
of greater hind limb than forelimb yield, cercopithecoids are more like terrestrial nonprimate quadrupeds. Current views on cercopithecoid origins suggest that Victoriapithecus, a potential common
ancestor of colobines and cercopithecines, may have
indeed been semiterrestrial (von Konenigswald,
1969; Simons, 1972; McCrossin and Benefit, 1992,
1994; McCrossin et al., 1998; Benefit and McCrossin, 2002). Therefore, modifications for some measure of terrestriality, including emphasis on stability at the shoulder and rapid flexion/extension at the
elbow (McCrossin et al., 1998), may have been maintained to varying degrees among extant cercopithecoids, despite the fact that many are now largely or
exclusively arboreal. A modest degree of elbow yield
during walking may be a similar retention.
Finally, marsupials exhibit comparable levels of
limb yield to primates, and they were shown to be
second only to primates in limb excursion angles
48
6.96 ⫾ 2.19
13.44 ⫾ 4.08
16.31 ⫾ 2.60
19.07 ⫾ 3.92
Standard Error.
1
LO
Re-extension
Mid
127.09 ⫾ 3.71
109.29 ⫾ 6.16
110.31 ⫾ 1.63
101.36 ⫾ 2.47
23.43 ⫾ 2.99
25.34 ⫾ 2.63
18.08 ⫾ 3.34
7.09 ⫾ 2.20
150.52 ⫾ 1.98
134.63 ⫾ 5.68
128.40 ⫾ 1.87
108.45 ⫾ 0.28
151.12 ⫾ 2.20
133.36 ⫾ 3.72
132.86 ⫾ 4.74
133.76 ⫾ 4.56
15.82 ⫾ 1.56
21.91 ⫾ 2.10
22.54 ⫾ 3.72
31.99 ⫾ 7.54
16.21 ⫾ 2.11
27.53 ⫾ 4.04
26.90 ⫾ 3.88
33.62 ⫾ 4.64
151.51 ⫾ 1.371
138.98 ⫾ 2.64
137.22 ⫾ 5.79
135.38 ⫾ 8.44
Cercopithecoids
Ceboids
Lemuroids
Lorisoids
135.30 ⫾ 2.57
111.45 ⫾ 5.17
110.31 ⫾ 7.92
101.77 ⫾ 8.71
Hind limb
Yield
TD
LO
Re-extension
Forelimb
Mid
Yield
TD
Superfamily
TABLE 3. Primate mean elbow and knee angles (in degrees) at touchdown, midstance, and liftoff
134.05 ⫾ 2.60
122.73 ⫾ 5.01
126.62 ⫾ 1.05
120.44 ⫾ 1.45
E. LARNEY AND S.G. LARSON
(Larson et al., 2000, 2001), which could indicate
increased step length, both important aspects of a
compliant gait. However, conclusions about marsupial gait based on the data presented here should be
tempered by the fact that our sample size is small
and includes two highly arboreal species, the woolly
opossum (Caluromys philander), which was already
shown to display morphological and behavioral convergences with primates (Lemelin, 1996, 1999; Lemelin and Schmitt, 2001; Lemelin et al., 2002;
Schmitt and Lemelin, 2002), and the koala (Phascolarctos cinereus). With this said, the dramatic yield
seen in these marsupial species and primates does
tend to support a link between the use of a compliant
gait and arboreal habits (Schmitt, 1994, 1998, 1999).
This link is further supported by the individual species outside of primates and marsupials that display
unusual changes in limb angles, such as the fossa
(Cryptoprocta ferox), which was described as extremely agile in arboreal environments (Garbutt,
1999), as well as the margay (Felis wiedi) (Konecny,
1989), tayra (Eira barbara) (Nowak, 1999), and tree
shrew (Tupaia glis) (LeGros Clark, 1959), which are
all regular tree dwellers.
Schmitt (1994, 1998, 1999) suggested that the use
of a compliant gait is a derived character for primates related to their arboreal origins. If this is
correct, then the high limb yield reported here for
marsupials would be a case of convergence. Alternatively, limb yield and use of a compliant gait could be
primitive retentions in primates as well as marsupials. Whether the origins of mammalian posture
and locomotion are related to terrestriality or arboreality has long been a topic of debate (for an overview, see Jenkins, 1974), and which view is adopted
impacts upon whether the arboreal habits of primates are viewed as a departure from the primitive
mammalian condition or an elaboration of it. Theories on primitive mammalian locomotor adaptation
have suffered from a lack of sufficiently old fossils
representing common ancestral forms (Jenkins,
1974). However, a recently discovered fossil Eomaia
scansoria from the early Cretaceous period in China
is believed to be the oldest known Eutherian mammal (Ji et al., 2002). Its elongated fingers and toes
have been interpreted to reflect climbing abilities
and arboreal habits (Ji et al., 2002), supporting an
arboreal origin for mammalian postural and locomotor characteristics. In addition, primitive members
of the marsupial lineage are also believed to have
been climbers (Kielan-Jaworowska et al., 1979).
Therefore, if the use of a compliant gait is indeed an
adaptation to arboreal habits, it may have arisen
early in mammalian evolution, and limb yield could
be a primitive retention in primates as well as marsupials. However, this would not alter the fact that
as a mechanism for reducing peak forces on the
limbs, a compliant gait would have facilitated the
invasion and subsequent radiation of basal primates
into a terminal branch niche.
LIMB YIELD IN PRIMATES
49
Fig. 4. Error bars represent group means ⫾ 2 standard errors of mean for different primate superfamilies
(marsupials included for
comparison). a: Error bars
and means for elbow angles
at TD (light gray), Mid
(black), and LO (dark gray).
b: Error bars and means for
knee angles at TD (light
gray), Mid (black), and LO
(dark gray). On average, cercopithecoids display more extended limbs at every stage
of a step cycle than other primate groups. c: Error bars
and means for elbow yield
(black) and re-extension
(gray). d: Error bars and
means for knee yield (black)
and re-extension (gray). Average elbow yield is higher
than knee yield in all primate
groups except cercopithecoids.
ACKNOWLEDGMENTS
This study is based on videotapes of animals at
the following institutions: Bronx Zoo, New York, NY;
Cleveland Zoo, Cleveland, OH; Pittsburgh Zoo,
Pittsburgh, PA; San Diego Zoo, San Diego, CA; Duke
Primate Center, Durham, NC; Primate Locomotion
Laboratory, Stony Brook, NY; and Laboratoire
d’Ecologie Générale, CNRS/Unité de Recherche
1183, Brunoy, France. Thanks go to Pierre Lemelin
and Mark Hamrick, who collected some of the video,
to Luci Betti-Nash for the preparation of Figure 2,
and to Anthony Olejniczak for the development of a
post hoc statistical test for Kruskal-Wallis results.
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