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Brief communication Forelimb compliance in arboreal and terrestrial opossums.

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Brief Communication: Forelimb Compliance in Arboreal
and Terrestrial Opossums
Daniel Schmitt,1* Laura T. Gruss,2 and Pierre Lemelin3
Department of Evolutionary Anthropology, Duke University, Durham, NC 27708
Department of Biology, Benedictine University, Lisle, IL 60532
Division of Anatomy, 5-05A Medical Sciences Building, Faculty of Medicine and Dentistry,
University of Alberta, Edmonton, Alberta, Canada T6G 2H7
primate origins; locomotion; arboreality; marsupial; biomechanics
Primates display high forelimb compliance (increased elbow joint yield) compared to most
other mammals. Forelimb compliance, which is especially marked among arboreal primates, moderates vertical oscillations of the body and peak vertical forces
and may represent a basal adaptation of primates for
locomotion on thin, flexible branches. However, Larney
and Larson (Am J Phys Anthropol 125 [2004] 42–50)
reported that marsupials have forelimb compliance comparable to or greater than that of most primates, but
did not distinguish between arboreal and terrestrial
marsupials. If forelimb compliance is functionally linked
to locomotion on thin branches, then elbow yield should
be highest in marsupials relying on arboreal substrates
more often. To test this hypothesis, we compared forelimb compliance between two didelphid marsupials,
Caluromys philander (an arboreal opossum relying
heavily on thin branches) and Monodelphis domestica
(an opossum that spends most of its time on the
ground). Animals were videorecorded while walking on
a runway or a horizontal 7-mm pole. Caluromys showed
higher elbow yield (greater changes in degrees of elbow
flexion) on both substrates, similar to that reported for
arboreal primates. Monodelphis was characterized by
lower elbow yield that was intermediate between the
values reported by Larney and Larson (Am J Phys
Anthropol 125 [2004] 42–50) for more terrestrial primates and rodents. This finding adds evidence to a model
suggesting a functional link between arboreality—particularly locomotion on thin, flexible branches—and
forelimb compliance. These data add another convergent trait between arboreal primates, Caluromys, and
other arboreal marsupials and support the argument
that all primates evolved from a common ancestor that
was a fine-branch arborealist. Am J Phys Anthropol
141:142–146, 2010. V 2009 Wiley-Liss, Inc.
The exact nature of the locomotor behavior and substrate
environment of the earliest primates has been the subject of
continuous debate for almost 100 years (e.g. Jones, 1916;
Cartmill, 1972, 1992; Szalay et al., 1987; Szalay and
Dagosto, 1988; Sussman, 1991; Larson, 1998; Schmitt and
Lemelin, 2002; Shapiro and Raichlen, 2005, 2007; Stevens
2006, 2008; Cartmill et al., 2007b; Lemelin and Schmitt,
2007; Raichlen et al., 2007; Wallace and Demes, 2008). As
early as 1916, Jones promoted the idea that the origin of
primates was associated with a fundamental change in the
functional role of the forelimb. He argued that the earliest
primates reduced the weight-bearing role of the forelimb in
order to use it as a more mobile, manipulative organ. This
idea has persisted ever since as a theme of most discussions
of primate locomotor evolution, but has only been tested
experimentally over the past 15 years.
As an extension of Jones’ original ideas, the role of
forelimb stiffness has recently gained prominence in anthropological studies of forelimb function. Schmitt (1995,
1998, 1999, 2003) observed that Old World monkeys,
especially more arboreal species walking on instrumented poles simulating arboreal substrates, are characterized by considerable elbow yield (which may reflect
relatively low forelimb vertical stiffness) compared to
other mammals. Larney and Larson (2004) independently confirmed Schmitt’s finding for a wider range of
primates, although Franz et al. (2005) did not observe
evidence of increased forelimb compliance in ring-tailed
lemurs moving on different substrates. Schmitt (1999)
and Larney and Larson (2004) suggested that elbow
yield may be a part of a set of biomechanical features
that evolved early in primate evolution in association
with locomotion and foraging on thin branches where
the forelimbs are used for reaching, grasping and manipulation. Thus, much has been made of elbow yield as an
important diagnostic feature of primate locomotion, and
specifically for movement in a fine-branch environment,
yet few tests of this assumption have been applied outside of primates.
In this light, one especially intriguing finding by Larney and Larson (2004) is that marsupials have forelimb
compliance as great, if not greater, than that of most primates. These data clearly conflict with claims made by
Schmitt (1998, 1999) that primates are unique among
mammals in having high degrees of elbow yield. Yet
these data also suggest a pattern that has implications
for understanding the origins of primate locomotion.
C 2009
Grant sponsor: National Science Foundation; Grant numbers:
SBR-9318750 and BCS-9904401; Grant sponsor: Duke University.
*Correspondence to: Daniel Schmitt, Department of Evolutionary
Anthropology, Duke University, Box 90383, Durham, NC 27708.
Received 17 June 2008; accepted 29 May 2009
DOI 10.1002/ajpa.21145
Published online 9 November 2009 in Wiley InterScience
Schmitt (1999, 2003) and Schmitt et al. (2007, 2008)
argued that forelimb compliance moderates vertical oscillations of the body and peak vertical forces on the limbs.
It was proposed that these features are basal adaptations of primates for moving and foraging on thin, terminal branches. But if all marsupials, including terrestrial
species, show high-forelimb compliance, these claims
would require re-evaluation. Larney and Larson (2004)
presented average data only for primarily, but not exclusively, arboreal marsupials. Thus, their data might
indicate convergence between arboreal marsupials and
This would hardly represent the first or only convergent trait between arboreal marsupials and primates. A
wide array of recently documented morphological, behavioral, and ecological convergences between primates and
some arboreal marsupials, especially the woolly opossum
(Caluromys), have allowed researchers to test specific
hypotheses about the origins of primates [see Lemelin
and Schmitt (2007) for a review]. These convergent traits
between many primates and arboreal marsupials like
Caluromys include foraging behavior and life-history
traits (Cartmill, 1974; Eisenberg and Wilson, 1981;
Charles-Dominique, 1983; Rasmussen, 1990), grasping
abilities of the extremities (Lemelin, 1999; Lemelin and
Schmitt, 2007), shoulder anatomy (Argot, 2001; Larson,
2007), limb protraction (Larson et al., 2000, 2001 Fischer
et al., 2007; Nayakatura et al., 2007), weight distribution
on the limbs during locomotion (Schmitt and Lemelin,
2002), and footfall patterns (Pridmore, 1994; Cartmill et
al., 2002, 2007a,b, 2008; Lemelin et al., 2003; Fischer et
al., 2007; Nayakatura et al., 2007).
Not only are arboreal marsupials convergent on primates in many ways, they also differ from terrestrial
marsupials. Lemelin and colleagues have drawn specific
contrasts between the woolly opossum and its close, but
more terrestrial, relative the short-tailed opossum
(Monodelphis) (Schmitt and Lemelin, 2002; Lemelin et
al., 2003; Lemelin and Schmitt, 2007). Monodelphis has
very different morphological characteristics than Caluromys, including shorter, less prehensile digits (Lemelin,
1999). In spite of these differences, Monodelphis retains
some climbing abilities like most opossums (Lemelin and
Schmitt, 2007), supporting the notion that all opossums
evolved from a common ancestor that was arboreal
(Szalay, 1994).
In addition to behavioral and morphological divergences between arboreal and terrestrial marsupials, Lemelin
and his colleagues have found several informative biomechanical divergences as well. For example, they found
that Caluromys has significantly lower peak vertical
forces on its forelimbs relative to its hindlimbs, a pattern
shared with most primates (Schmitt and Lemelin, 2002;
Lemelin and Schmitt, 2007) whereas Monodelphis, like
most other nonprimate mammals and several primates,
has relatively higher peak forelimb forces (Schmitt and
Lemelin, 2002; Lammers and Biknevicius, 2004; Lemelin
and Schmitt, 2007). Lemelin and Schmitt (2007) also
showed that Caluromys showed values of arm protraction (1208) like that of most primates (Larson et al.,
1999, 2001), whereas Monodelphis had values only
slightly beyond 908 relative to its body axis at forelimb
touchdown during quadrupedal walking more similar to
that of nonprimates (Larson et al., 1999, 2001). Fischer
et al. (2002) found even lower values for Monodelphis
walking on a treadmill. Finally, like many other nonpri-
mate mammals, Monodelphis relies lateral-sequence
walking gaits (Pridmore, 1994; Cartmill et al., 2002;
Lemelin et al., 2003; Parchman et al., 2003; Lammers
and Biknevicius, 2004; Cartmill et al., 2007a; Lemelin
and Schmitt, 2007). Woolly opossums, in contrast, use
primarily diagonal-sequence gaits, especially when walking on relatively thin poles compared to a runway (Cartmill et al., 2002, 2007a,b; Lemelin et al., 2003; Lemelin
and Schmitt, 2007).
From these studies, Lemelin and Schmitt argued that
convergent evolution of woolly opossums toward a primatelike biomechanical condition was functionally linked
to moving and foraging on thin branches (Schmitt and
Lemelin, 2002; Lemelin et al., 2003; Lemelin and
Schmitt, 2007). They further assumed that Caluromys
had reduced forelimb stiffness (increased forelimb joint
compliance) like primates and that Monodelphis did not.
Yet to date, they have not provided any actual measure
of joint yield. The study presented here fills that gap
and tests the hypothesis that an arboreal marsupial
(Caluromys philander) will have more elbow joint yield
than a more terrestrial, closely related species (Monodelphis domestica). In many ways, the expected differences
in opossums should parallel those previously reported
for primates (Schmitt, 1999; Larney and Larson, 2004).
A detailed description of the experimental set-up,
methods, and equipment used in this study can be found
in Schmitt and Lemelin (2002) and Lemelin and Schmitt
(2007) and are briefly summarized below. Three adult
woolly opossums (Caluromys philander) weighing on average 377 g and four adult short-tailed opossums (Monodelphis domestica) weighing on average 135 g were used
in this study. All data were collected in the Animal Locomotion Laboratory in the Department of Biological
Anthropology and Anatomy at Duke University, Durham, NC, USA. Animals were allowed to move freely
within a 3.6-m long, 1-m tall, and 1-m wide Lexan enclosure. Both opossum species walked on a flat wood surface covered with a layer of paint and sand. Additionally,
woolly opossums walked on a 2.5-m long, 7-mm diameter
stiff pole made of graphite, and covered with a layer of
sand and paint. The short-tailed opossums used in this
study were unable to walk on the 7-mm pole. When they
attempted to do so, they were slow, used asymmetrical
gaits, and fell frequently. We did use a larger pole (28mm in diameter) [see Lemelin et al. (2003)], but only
obtained two symmetrical gait cycles that were not analyzed in this study. For this study, we only examined
walking (no aerial phase) gaits.
Subjects were filmed by a single, lateral view JVC GYX3 videocamera (JVC Professional Products, Wayne, NJ)
recording at 60 Hz with an electronic shutter set at
1/1,000 s and a MotionScope high-speed camera (Redlake
MASD, Tucson, AZ) recording at 250 images/s. The cameras were placed five meters from the center of the runway, perpendicular to the animal’s line of travel. Video
sequences were transferred to a personal computer running Motus, 2000 movement analysis software (Vicon,
Lake Forest, CA). Because of the high flexibility in skin,
external markers were not relied on here. Instead, areas
over the skin of the relevant joints (glenohumeral, elbow,
wrist, and hip) of the experimental animals were shaved
for clear visual assessment on the videotapes. Moreover,
we manipulated the relevant joints of the animals when
American Journal of Physical Anthropology
Fig. 1. Still frame pictures of Monodelphis domestica (A, B) and Caluromys philander (C, D) at touchdown (A, C) and midsupport (B, D) during walking. The digitized points and lines used to calculate angles are indicated. Opossums on top and bottom panels are not pictured on the same scale.
sedated, identified their centers, and obtained segment
length that we could use to confirm the relative accuracy
of measurements by comparing digitized to actual segment length. In addition, the line of segments could be
used also as a guide for confirming joint centers. The
methods match those of Schmitt (1999), Larney and
Larson (2004), and Lemelin and Schmitt (2007), to which
these data are being compared. Scaled x, y coordinates
for the eye, and shoulder, elbow, wrist, and hip joints
were collected. Figure 1 shows representative video
images and digitization method used in this study.
Forward velocity was calculated from the x-coordinates
of the eye. Only video sequences with speed variation
not exceeding 25% were used. From the digitized values
for joint position, the acute angles of the elbow joint for
the limbs facing the camera were calculated following a
similar convention as that used by Larney and Larson
(2004). The degrees of elbow yield (i.e., change in elbow
angle from limb touchdown to point of maximum elbow
flexion) were then calculated for each trial. The differences between taxa and between substrates (in woolly
opossums only) were compared using a Mann–Whitney
U-test using SAS statistical software (SAS Institute,
Cary, NC).
Thirty-one steps on a 7-mm pole and 23 steps on a
runway respectively for the woolly opossum, and 30
steps on the runway for the short-tailed opossum were
collected. The mean values and one standard deviation
for forelimb compliance, as measured by elbow yield, are
displayed in Figure 2. As predicted, woolly opossums
exhibited significantly greater elbow yield compared to
American Journal of Physical Anthropology
short-tailed opossums (P \ 0.01; Fig. 2). Similar average
degrees of elbow yield were found between the small
pole (318) and runway (308) in woolly opossums. Differences in elbow yield between the two opossum species
are significant (P \ 0.01), regardless of whether Monodelphis was compared to Caluromys on the ground or on
a pole. Mean elbow yield in woolly opossums is greater
than the average reported by Larney and Larson (2004)
for primates as a group (22.68). The same average value
in short-tailed opossums (15.28) lies between the marsupial (19.98) and rodent (11.68) averages reported by
Larney and Larson (2004).
We tested the hypothesis that an arboreal opossum
will experience higher degrees of forelimb compliance
compared to a more terrestrial one. This hypothesis was
supported by a comparison showing that a highly arboreal, fine-branch specialist, Caluromys philander, had
significantly greater elbow yield than the more terrestrial Monodelphis domestica. It is interesting to note
that limb compliance in the woolly opossum did not
increase on the pole compared to the ground. This is contrary to findings for Old World monkeys (Schmitt, 1999;
Schmitt and Hanna, 2004), but consistent with previous
findings that woolly opossums do not show differences in
peak vertical force when walking on poles versus the
ground (Schmitt and Lemelin, 2002; Lemelin and
Schmitt, 2007). A similar pattern was reported by Franz
et al. (2005) for Lemur catta. Although their comparison
of peak vertical force on the limbs between terrestrial
galloping and arboreal walking was invalid, because galloping is a more compliant gait than walking (McMahon,
Fig. 2. Mean and one standard-deviation for elbow yield in
Caluromys philander and Monodelphis domestica. [Color figure
can be viewed in the online issue, which is available at www.]
2002; Hamrick, 1999, 2001) convergences between primates and opossums that specialize on locomotion and
foraging on slender supports. These convegences
between arboreal opossums and primates are important,
because they represent a robust test of Cartmill’s model.
The link is further supported by the recent description
of locomotor convergences between primates, arboreal
marsupials, and chameleons (Cartmill et al., 2004, 2008;
Fischer et al., 2007; Nyakatura et al., 2007) as well as
some highly arboreal carnivorans (Lemelin et al., 2008).
This study represents an additional piece of evidence
supporting the model that primate locomotor features
may have evolved in association with the exploitation of
a fine-branch niche by early primates.
1985), their data on estimated body oscillations did
include walking gaits on the ground and does suggest
that whatever yield might occur in these animals does
not vary across substrates. It is possible that some
groups (opossums and lemurs) maintain similar levels of
compliance during locomotion, independently of substrate size.
The data presented here advance our understanding of
the evolution of arboreal locomotion in primates in two
important ways. First, they add to the growing list of
distinctions between arboreal and terrestrial opossums
already established (Hunsaker and Shupe, 1977;
Charles-Dominique, 1983; Rasmussen, 1990; Lemelin,
1999; Argot, 2001, 2002; Cartmill et al., 2002, 2007a,b;
Schmitt and Lemelin, 2002, Lemelin et al., 2003; Lemelin and Schmitt, 2007). Second, these data indicate
another convergence between a marsupial fine-branch
arborealist and most primates. Schmitt (1999) was
clearly incorrect in claiming that primates were unique
among mammals in showing high degrees of forelimb
compliance. The data presented here combined with that
of Larney and Larson (2004) show that arboreal marsupials have limb compliance like that of many primates.
The fact that woolly opossums display relatively compliant forelimbs during walking is consistent with the
hypothesis of a functional link between locomotion on
relatively thin branches and forelimb compliance
(Schmitt, 1999, 2003; Schmitt and Lemelin, 2002;
Lemelin and Schmitt, 2007).
These results are also striking because of the size differences between the two opossums we studied. Biewener (1989, 1990) observed that larger animals stand
and move with more extended limb joints. Polk (2002)
found the same pattern within closely related primates
of different body mass. The pattern is reversed here,
with the larger marsupial walking with more yielding
forelimbs. This suggests that substrate use may have an
important influence in determining limb posture in
smaller mammals.
The idea that primates evolved unique morphological
and behavioral specializations in association with cautious, well-controlled locomotion on thin and flexible supports was first proposed by Cartmill (1970, 1972, 1974),
although Szalay (2007) provides a recent summary of a
contrary view that involves significant grasp-leaping
behavior in the earliest primates. Cartmill’s model of primate origins has received considerable support from
studies showing ecological (Hunsaker, 1977; Hunsaker
and Shupe, 1977; Charles-Dominique, 1983; Rasmussen,
1990) and morphological (Lemelin, 1999; Argot, 2001,
We thank Martine Atramentowicz (URA 8571 CNRS/
MNHN) and Kathleen Smith (Duke University) for
giving access to the opossums. We are grateful to Susan
Larson for helpful and insightful discussions. We are
grateful for all the efforts of the Editor of this
journal, the Associate Editor, and two reviewers. Their
comments vastly improved the manuscript. Laboratory
procedures were approved by Duke University Institutional Animal Care and Use Committee (IACUC Registry
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