AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 141:142–146 (2010) Brief Communication: Forelimb Compliance in Arboreal and Terrestrial Opossums Daniel Schmitt,1* Laura T. Gruss,2 and Pierre Lemelin3 1 Department of Evolutionary Anthropology, Duke University, Durham, NC 27708 Department of Biology, Benedictine University, Lisle, IL 60532 3 Division of Anatomy, 5-05A Medical Sciences Building, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada T6G 2H7 2 KEY WORDS primate origins; locomotion; arboreality; marsupial; biomechanics ABSTRACT 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  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  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 V WILEY-LISS, INC. C 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. E-mail: Daniel_Schmitt@baa.mc.duke.edu Received 17 June 2008; accepted 29 May 2009 DOI 10.1002/ajpa.21145 Published online 9 November 2009 in Wiley InterScience (www.interscience.wiley.com). COMPLIANT GAIT IN OPOSSUMS 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 primates. 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- 143 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). MATERIALS AND METHODS 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 144 D. SCHMITT ET AL. 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). RESULTS 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). DISCUSSION 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, 145 COMPLIANT GAIT IN OPOSSUMS 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. interscience.wiley.com.] 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. ACKNOWLEDGMENTS 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. 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