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Keywords:

  • cross-sectional geometry;
  • Imax/Imin, suspensory;
  • arboreal;
  • functional convergence;
  • limb loading;
  • forelimb

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

Studies on the cross-sectional geometry of long bones in African apes have documented that shape ratios derived from second moments of area about principle axes (e.g., Imax/Imin) are often correlated with habitual locomotor behaviors. For example, humeral cross-sections tend to appear more circular in more arboreal and forelimb suspensory chimpanzees compared with terrestrial quadrupedal gorillas. These data support the hypothesis that cross-sections that are more circular in shape are adapted for multidirectional loading regimes and bending moments encountered when using acrobatic locomotor behaviors. Whether a more circular humerus reflects greater use of forelimb suspension in other primates and nonprimate mammals is unknown. In this study, cross-sections at or near midshaft of the humerus were obtained from anthropoid primates that differ in their use of forelimb suspension, as well as from two genera of suspensory sloths. Imax/Imin ratios were compared within and between groups, and correlations were made with behavioral data. In broad comparisons, observed differences in morphology follow predicted patterns. Humeri of suspensory sloths are circular. Humeri of the more suspensory hominoids tend to be more circular than those of quadrupedal taxa. Humeri of the suspensory atelines are similar to hominoids, while those of Cebus are more like nonsuspensory cercopithecoids. There is, however, considerable overlap between taxa and within finer comparisons variation between species are not in the predicted direction. Thus, although Imax/Imin ratios of the humerus are informative for characterizing generalized locomotor modes (i.e., forelimb suspensory vs. quadrupedal), additional structural information is needed for more fine-grained assessments of locomotion. Anat Rec, 296:545–556, 2013. © 2013 Wiley Periodicals, Inc.

Morphological variation in bone shape and structure likely results from complex interactions between development, evolution, and function (e.g., Ruff and Runestad, 1992; Lieberman et al., 2004; Pearson and Lieberman, 2004; Ruff et al., 2006; Hansen et al., 2009; Wallace et al., 2010). Yet even with such complexity, the analysis of cross-sectional properties of long bone diaphyses to infer habitual locomotor behaviors of living and extinct animals remains an important and frequently used approach by many functional morphologists and paleontologists. Such investigations are based on the premise that cross-sectional geometry reflects bone functional adaptation to its mechanical loading environment (e.g., Wainwright et al., 1976; Ruff and Hayes, 1983; Ruff et al., 1984, 2006; Schaffler et al., 1985; Burr et al., 1989; Trinkaus et al., 1991; Ruff and Runestad, 1992; Martin et al., 1998; Polk et al., 2000; Currey, 2002; Ruff, 2002; Habib and Ruff, 2008; Shaw and Ryan, 2012). When modeled as a beam, a long bone's cross-sectional geometry can provide measures of its compressive strength (e.g., cross-sectional area [CSA] and cortical area [CA]), as well as its resistance to bending and torsion about a particular axis (i.e., second moments of area [I] and polar moments of area [J], respectively; e.g., Huiskes, 1982). Together, such parameters can provide researchers enough information to develop hypotheses and biomechanically supported generalizations about habitual positional and locomotor behaviors of animals from which in vivo data (e.g., kinematics, kinetics, and bone strain) cannot be obtained, including past human populations, endangered species and fossils. One potential downside, however, of using variables such as CSA and J in comparative analyses of fossils and/or isolated long bone specimens is that both require some information about an individual's body mass or size to make these measures biomechanically informative (e.g., Polk et al., 2000).

Several studies have also evaluated whether cross-sectional shape, another variable of a long bone's cross-sectional geometry, can serve as a correlate of a long bone's mechanical loading history (Carlson, 2005; Carlson et al., 2006, 2008, 2011; Carlson and Judex, 2007; Simons, 2009, Simons et al., 2011; see also Demes, 2007 for alternative arguments). Specifically, these studies have tried to test the general hypothesis that cross-sectional shape reflects whether an animal's long bones have experienced relatively uniform or variable (i.e., multidirectional) loading regimes and bending moments. For example, a long bone with a more elliptical cross-section is thought to be adapted for bending loads in one particular plane or direction, likely from using stereotypical or uniform locomotor behaviors (e.g., strict sagittal plane movements). In contrast, a more circular cross-section is thought to be adapted for more variable loading regimes including bending and torsion in multiple planes that could likely come from using diverse locomotor behaviors (e.g., Lovejoy et al., 1976; Jungers and Minns, 1979; Burr et al., 1989; Ruff and Runestad, 1992; Carlson, 2005; Carlson and Judex, 2007; but see Ruff et al., 1984; Trinkaus et al., 1991).

The most common method for estimating a long bone's cross-sectional shape is to use second moments of area (I) either about anatomical axes (anteroposterior [Iy]; mediolateral [Ix]) or about principle axes (maximum [Imax]; minimum [Imin]) derived from either physical sections of bones or cross-sections obtained with noninvasive imaging techniques such as computed tomography (CT) (Schaffler et al., 1985; Carlson, 2005). Specifically, ratios created from these second moments, either Ix/Iy or Imax/Imin, can be used to assess how much cross-sectional shape deviates from circularity; ratios that deviate from 1.0 are more elliptical. Second moment ratios about anatomical axes can further illustrate if deviations from circularity occur either in the anteroposterior (A–P) or mediolateral (M–L) axes, whereas ratios about principal axes do not convey this information (without more information on the specific orientation of principal axes). The upside of using shape ratios is that they do not require information about an individual's body mass or size. This makes the use of shape ratios particularly appealing for isolated long bone specimens and fossils. In addition, the Imax/Imin ratio does not require information about anatomical orientation, facilitating the analysis of even fragmentary bone shafts.

Force plate and bone strain studies have shown that suspensory and arboreal quadrupedal locomotion tends to produce more variable bending regimes compared with terrestrial quadrupedal locomotion (Swartz et al., 1989; Chang et al., 2000; Demes et al., 2001; Carlson et al., 2005; Demes et al., 2006; Demes and Carlson, 2009; Schmidt and Fischer, 2010). Therefore, the limb bones of animals using these types of locomotor behaviors may be adapted to resist multidirectional bending regimes (i.e., more circular cross-sections with more even distribution of bone around its central axis). For example, analyses of cross-sectional shape using Imax/Imin ratios suggest that a suspensory (and more arboreal) signal (i.e., ratios closer to 1.0) may be present in humeri of chimpanzees (Pan) compared with a more quadrupedal (and more terrestrial) signal (i.e., ratios deviating from 1.0) observed in closely related gorillas (Gorilla) (see Table 3 in Carlson, 2005). Subsequent studies of humeral cross-sectional shape, however, have demonstrated fewer significant differences within and between individuals, sexes, and populations of wild chimpanzees with specific documented positional behavioral data (Carlson et al., 2006, 2008, 2011) or between wild and captive chimpanzees that most likely differed in positional behaviors, as well as substrate use, diet, and so forth (Morimoto et al., 2011). Thus, while long bone cross-sectional shape as measured from the ratio of Imax and Imin could be used to aid in distinguishing more general locomotor behaviors and substrate preferences (e.g., arboreal or terrestrial; quadrupedal or suspensory), it may be more difficult to distinguish between specific locomotor categories (e.g., scrambling, bridging, and climbing; Carlson, 2005; Carlson et al., 2006).

Whether the humeral cross-sectional shape patterns previously observed in African apes are representative of other primates is unknown. This is primarily because Carlson's (2005, and subsequent references) research focused on trying to determine form–function relationships in closely related animals (gorillas and/or chimpanzees). Additional evidence that Imax/Imin ratios reflect locomotor behaviors, in particular forelimb suspension, in additional extant taxa would prove very useful to functional morphologists and paleontologists for evaluating previous reconstructions of suspensory behaviors of extinct primates including early hominins (e.g., Ardipithecus, Australopithecus, and early Homo), Miocene hominoids and pliopithecoids (e.g., Oreopithecus, Dryopithecus, Hispanopithecus, and Epipliopithecus) and subfossil lemurs (i.e., palaeopropithecids). In fact, many of these fossil taxa have isolated humeri or humeral fragments assigned to them. If a more circular humeral cross-section reflects a bone adapted for more variable limb loading experienced during forelimb suspensory behaviors, other primate species that incorporate a large amount of forelimb suspension (i.e., Asian apes and some atelines) should also have more circular humeri when compared with closely related species that adopt little to no forelimb suspension (e.g., habitual quadrupeds). In contrast, less- or nonsuspensory primate species should have more elliptical humeral cross-sections.

To investigate this possibility and to expand on previous research investigating the general usage of Imax/Imin ratios to interpret fossil positional behaviors, this study examines humeral cross-sectional shape in several Asian apes (Hylobates, Symphalangus, and Pongo), African apes (Pan and Gorilla), papionin cercopithecoids (Macaca and Papio), and platyrrhines (Ateles, Lagothrix, Alouatta, and Cebus) that are known to differ in their use of forelimb suspension. This comparative sample serves as both functional and phylogenetic “outgroups” (cf., Patel, 2005) to further assess the form–function relationship between long bone cross-sectional shape (i.e., Imax/Imin ratio) and habitual loading regimes (i.e., generalized locomotor behavior). We predicted that primates engaged in more forelimb suspension will have more circular humeri compared with closely related primates that are predominately quadrupedal and do not hang from superstrates.

In addition to examining the morphology of primates with great diversity in positional behaviors, examining nonprimate animals with similar locomotor behaviors as primates (i.e., those that are functionally convergent) can provide an even more robust test of functional hypotheses (cf., Coddington, 1994). Such an approach is not uncommon in studies of primate functional morphology (e.g., Orr, 2005; Lemelin and Schmitt, 2007; Kirk et al., 2008; Patel and Carlson, 2008; Organ et al., 2009). For example, to identify specific suspensory morphological adaptations in primates, several researchers have used living sloths (Bradypus and Choloepus) as comparative models or functional analogues (e.g., Mendel, 1979; White, 1993; Jungers et al., 1997; Patel and Carlson, 2008). This is because sloths are phylogenetically distant from primates (Springer et al., 2004) and display both fore- and hindlimb suspensory positional behaviors and morphology (Goffart, 1971; Mendel, 1985; Adam, 1999; Nowak, 1999; Nyakatura et al., 2010; Nyakatura, 2012; Toledo et al., 2012). Furthermore, because the two genera of extant sloths likely evolved their suspensory behaviors independently (Gaudin, 2004; Gaudin and McDonald, 2008; Nyakatura, 2012), using them to investigate issues of functional convergence effectively adds two outgroups with which primates can be compared. While neither sloth genus engages in high-speed or richochetal brachiation like ateline or hylobatid primates, they do engage in slower, more careful anti-pronigrade quadrupedal and climbing movements in the wild. Moreover, recent reports on the kinematics of sloth suspension have shown similarities to living lorises (Nyakatura et al., 2010), and possibly Pongo. Thus, if the relationship between humeral cross-sectional shape and habitual locomotor modes can extend beyond primates (i.e., to sloths), it may further indicate that metrics such as Imax/Imin ratios are indeed informative and would bolster the hypothesis that long bone cross-sectional geometric shape is influenced in part by function (see also Simons [2009] and Simons et al. [2011] for a similar approach using birds). We predicted that humeri of suspensory sloths will also exhibit Imax/Imin ratios close to 1.0 because they habitually suspend their bodies below superstrates, and thus they should have similar long bone cross-sectional shapes to suspensory primates.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

The primate sample combines males and females of only wild-shot adult individuals (Table 1). Although there may be an effect of sex on some cross-sectional shape variables in primates such as African apes and baboons (Carlson, 2005; Hansen et al., 2009), pooling data from both sexes was justified in this study because we are interested only in examining general locomotor trends across different primate groups. Furthermore, because the ultimate goal is to evaluate the applicability of cross-sectional shape to fossil and other rare specimens, and because it is often difficult to determine sex of isolated humeri in the fossil record, male and female samples were combined. The combining of samples was further justified because preliminary analyses revealed no major differences in humeral Imax/Imin ratios between males and females of Pongo, Pan, and Gorilla (i.e., the most sexually dimorphic hominoids in terms of both body size and behavior; see Appendix for relevant statistics; see also Carlson [2005] for similar findings). Although we acknowledge that all the primate taxa discussed below do in fact use a variety of locomotor behaviors and that there may be sex-specific differences in suspensory locomotion with females usually being more suspensory than males (e.g., Sugardjito and van Hooff, 1986; Hunt et al., 1996; Carlson, 2005; Thorpe et al., 2005, Thorpe and Crompton, 2006), we decided to focus on more generalized locomotor categories as a more conservative comparative approach to make these data more applicable for potential future studies (Ruff, 2002). That is to say, we believe it is necessary to first be able to discern behaviors such as forelimb suspension from generalized quadrupedalism in our sample before trying to identify more specific behaviors such as arboreal scrambling or climbing, or to discern intraspecific differences across sexes (e.g., Carlson, 2005; Carlson et al., 2006).

Table 1. Descriptive statistics of humeral cross-sectional shape (Imax/Imin ratios)
Taxon% SuspensporyaSlice locationNMeanSDMinMax
  1. a

    Average reported forelimb suspensory behavior during arboreal locomotion (%) used by each primate genus. Suspensory behaviors may include arm-swinging, brachiation and/or tail-assisted suspension in either an orthrograde or pronograde orientation. Comparable data not available for sloths. See text for references.

  2. b

    Includes the following species: Bradypus tridactylus and B. variegates.

  3. c

    Includes the following species: Choloepus didactylus and C. hoffmanni.

Bradypus sp.b>50?H40111.1880.0911.0801.390
H50111.1660.1011.0301.320
Choloepus sp.c>50?H400
H50121.2220.1571.0201.570
Hylobates lar56.0H40101.2000.0931.0901.370
H500
Symphalangus syndactylus51.0H40101.1800.0991.0401.370
H5051.2160.1181.0901.390
Pongo pygmaeus52.0H40201.1850.0881.0001.320
H50201.2440.0951.1001.490
Pan paniscus16.76H4041.1860.0821.0701.260
H5041.2520.1951.0301.440
Pan troglodytes7.11H40201.1680.1081.0401.380
H50201.2860.1321.0701.540
Gorilla g. gorilla7.39H40101.3050.1501.1301.600
H50101.3610.1231.2101.630
Gorilla g. beringei1.25H40101.2240.1011.0501.390
H50101.3180.1381.0601.490
Macaca fascicularis0.0H40201.4160.2051.1201.920
H50201.4740.1921.1001.940
Papio cynocephalus0.0H40201.3870.2021.1301.810
H50201.5980.2131.2502.190
Ateles fusciceps28.97H4061.2240.0871.1001.340
H500
Lagothrix lagotricha11.7H4071.1650.1561.0301.480
H500
Alouatta palliata0.0H4081.1500.0891.0401.310
H500
Cebus apella0.0H4081.4460.2021.1081.767
H500

The hominoids consist of taxa that vary substantially in the degree to which they engage in forelimb suspension during arboreal locomotion. The apes that engage the most in forelimb suspension are Hylobates lar (N = 10), Symphalangus syndactylus (N = 11), and Pongo pygmaeus (N = 20). Fleagle (1976) documented that more than 50% of all locomotor behaviors in both Hylobates and Symphalangus is comprised of either slow or ricochetal brachiation. Similarly, Thorpe and Crompton (2006) and Cant (1987) have shown that more than half of the locomotor behaviors Pongo uses involves orthrograde or pronograde suspension. Pan troglodytes (N = 20) and Pan paniscus (N = 4) also use forelimb suspensory locomotor behaviors, but they are primarily quadrupedal on both arboreal and terrestrial substrates; Pan paniscus is the more arboreal species (Doran, 1993, 1996; Carlson, 2005). Although as much as 18% of total arboreal locomotion involves forelimb suspension in Pan paniscus, and an average of 7% of total arboreal locomotion in Pan troglodytes, these behaviors only contribute less than 2% of total locomotor behavior (see references by Doran [1989, 1993, 1996], Doran and Hunt [1994], and Hunt [1989, 1992] cited in Carlson [2005]). Gorilla g. beringei (N = 10) and Gorilla g. gorilla (N = 10) are primarily quadrupedal when adults, with G. g. beringei being more terrestrial than the other subspecies (Remis, 1998). Both subspecies, however, do engage in some degree of forelimb suspension and females are typically more suspensory than males. Also, it has been documented that female Gorilla g. gorilla individuals can in engage in as much suspension as some Pan troglodytes individuals (Doran and Hunt, 1994; Doran, 1996; Remis, 1994, 1995, 1998; Carlson, 2005). In this study, cross-sectional morphological data from all hominoids except one specimen of Pan paniscus and three specimens of Symphalangus syndactylus are originally from Ruff (2002) and details of that sample can be found therein.

The cercopithecoid sample used in this study is also from Ruff (2002) and consists of arboreal quadrupedal Macaca fascicularis (N = 20) and (semi-) terrestrial quadrupedal Papio cynocephalus (N = 20). Although these monkeys are morphologically different from hominoids (e.g., have tails; have intermembral proportions that are similar; have different muscle organizations in their stylopodia), neither of these monkey species uses forelimb suspensory behaviors (e.g., Rose, 1977; Fleagle, 1999). Thus, they can serve as comparators in functional studies, and in fact, it is not uncommon to combine hominoid and cercopithecoid samples when testing functional hypotheses about bone form (e.g., Schaffler et al., 1985; Ruff, 2002; Carlson and Patel, 2006; Patel and Carlson, 2007, 2008; Shaw and Ryan, 2012).

The platyrrhine sample includes three species of closely related ateline monkeys that engage in different amounts of forelimb suspensory behaviors: Ateles fusciceps (N = 6), Lagothrix lagotricha (N = 7), and Alouatta palliatta (N = 8). Studies of wild Ateles have shown that forelimb suspension (with and without the assistance of a prehensile tail) can range between ∼23% and 39% of total locomotor behavior (Fleagle and Mittermeier, 1980; Cant, 1986; Cant et al., 2001, 2003). Similarly, Lagothrix species have also been documented to use high levels of these same locomotor behaviors (∼12%; Cant et al., 2001, 2003). Alouatta, however, does not engage in forelimb suspension during locomotion, but does frequently adopt tail-assisted suspensory postures that are similar in frequency to Ateles (∼15%–17%: Cant, 1986; see also Fleagle and Mittermeier, 1980; Schön Ybarra, 1984). Also included within the platyrrhine sample is Cebus apella (N = 8), a non-ateline platyrrhine primate that does not engage in forelimb suspension. Cebus apella engages in tail suspension during feeding and postural behaviors, although not usually during locomotor behaviors, which contrasts directly with ateline platyrrhines (Fleagle and Mittermeier, 1980; Organ, 2007, 2010; Wright, 2007). The Ateles and Cebus samples were obtained from the Smithsonian National Museum of Natural History (USNM). The Lagothrix sample comprises skeletons from both the USNM and the American Museum of Natural History (AMNH). The Alouatta individuals come from deceased animals recovered from the grounds of Hacienda La Pacifica, Guanacaste, Costa Rica, and are under the care of Dr. Ken Glander, Duke University. Additional details of the ateline sample are provided elsewhere (Organ, 2007, 2010).

The three-toed sloths (Bradypus; N = 10) and the two-toed sloths (Choloepus; N = 9) were sampled from the AMNH and USNM. Different species for each genus were combined because of small sample sizes available from museum collections (Table 1). Furthermore, unlike the primate sample described above, sloth specimens included individuals that were wild-shot and captive. No individual exhibited any obvious sign of disease or injury to any of their long bones. Statistical tests between wild and captive individuals for each sloth genus were not significant for all cross-sectional shape variables. As noted above, sloths primarily use suspensory positional and locomotor behaviors, although we are unaware of any studies quantifying their positional behaviors in the wild (Mendel, 1985; Adam, 1999; Nowak, 1999; Nyakatura et al., 2010; Nyakatura, 2012).

The methods describing how the cross-sectional images of our primate sample 1 were obtained have been previously described in great detail by Ruff (2002) and Organ (2007, 2010), and therefore the details are not repeated here. Briefly, a single humerus for each individual was scanned with either a medical CT scanner or a peripheral quantitative CT (pQCT) scanner (Stratec XCT SA+, Norland Medical Systems) with customized internal pQCT software (Norland/Stratec XCT 5.40). Before scanning, each bone was positioned in a standardized orientation such that cross-sections were obtained orthogonal to the long axis of the diaphysis (see Appendix B in Ruff, 2002, for orientation protocols; see also Ruff and Hayes, 1983). Cross-sectional locations were determined based on percentages of bone length from its distal end (Fig. 1). Humerus length was measured from the lateral lip of the trochlea to the superior surface of the humeral head. For all individuals, we analyzed cross-sections at 40% of biomechanical humerus length from the distal end (H40). For most individuals excluding Hylobates and the platyrrhines, we also analyzed cross-sections at 50% of biomechanical humerus length (H50). Cross-sections at H50 were not analyzed for these taxa because they sometimes have large deltoid tuberosities at this level.

image

Figure 1. Representative primate (Hylobates, Papio) and sloth (Bradypus, Choloepus) humeri in ventral view (scaled to the same length) illustrating two cross-sectional locations (solid black lines) analyzed in this study: H40: 40% of humerus length relative to the distal end; H50: midshaft.

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Cross-sectional images of the sloth material were also obtained using medical CT scanning, but with a slightly different protocol compared with how the primate data were collected. Three different CT scanners were used: (1) GE Lightspeed 16 scanner (120 kV, 70 ma, 0.625 mm slice thickness) housed in the Department of Radiology, Stony Brook University Medical Center (Stony Brook, NY); (2) Philips Brilliance 64 scanner (120 kV, 50 mA, 1 mm slice thickness) located at the Holzer Clinic (Athens, OH); and (3) Siemens Somotom Emotion Single Spiral scanner (110 kV, 80 mA, 1 mm slice thickness) housed in the Department of Anthropology, Smithsonian Institution (Washington, DC). For all three scanners, either a “bone,” “orthopedic,” or “osteo” reconstruction algorithm was used to obtain sharper bone/air boundaries in our cross-sectional images. Due to time limitations at the scanning locations, serial scans of the entire bone were obtained, rather than single scans at our desired locations. To accommodate differences in lengths of the bones, as well as to minimize the collection of unnecessary digital data, scans were collected in an incremental value that resulted in ∼150 to 250 slices per specimen. Time restrictions on the scanners used for this portion of the study also prevented us from systematically orienting each specimen before scanning (as done for the primate sample). Therefore, after the acquisition of the CT slices, rendered virtual reconstructions of each humerus were digitally reoriented following the orientation protocol described by Ruff (2002) and then re-sliced (with the same voxel dimensions) using GE MicroView software. The images in the re-sliced stack were then used for all analyses. As with the primate sample, cross-sections at H50 in each sloth specimen were analyzed based on similar length measuring criteria. Cross-sectional properties were analyzed at H40 in Bradypus, but not Choloepus, because the latter has a well-developed and tall lateral supracondylar ridge (supinator crest) that can artificially create a more elliptical cross-sectional shape.

Imax and Imin were determined from each image using the software program SLICE (Nagurka and Hayes, 1980), ImageJ software with MomentMacroJ v. 1.3 (www.hopkinsmedicine.org/fae/mmacro.htm), or with standard engineering formulae (Riley et al., 2002) from pQCT-derived axis-specific second moments of area. Imax/Imin ratios were then calculated to assess how much cross-sectional shape deviates from circularity; as noted above ratios that approximate 1.0 are said to be more circular.

Statistical analyses included calculating descriptive statistics of each cross-sectional shape variable for each taxon. Box-and-whiskers plots were created to visually assess the data within and across taxa and a series of Mann-Whitney U-tests was performed to determine if there were any significant differences between taxa for each of our cross-sectional shape variables. Finally, nonparametric Spearman's rho correlation coefficients (in the primates sample only) were calculated between mean humeral cross-sectional shape and reported suspensory behavior measured as percent suspension relative to total arboreal locomotor behavior (Table 1). Correlations were performed separately: (1) within only hominoids, (2) within the entire catarrhine sample of hominoids and cercopithecoids, and (3) within only the platyrrhine sample. The catarrhines and platyrrhines were not combined because of their fundamentally different morphologies (i.e., the platyrrhines have prehensile tails that aid in suspension). The use of tail-assisted suspension could reduce or even alter the loads (both in magnitude and orientation) that a tail-less hominoid would experience when hanging below superstrates with its forelimbs (e.g., Schmitt et al., 2005). For all analyses, nonparametric tests were used because the assumptions for parametric ANOVAs were not met. All tests were deemed significant at the P < 0.05 level (with Bonferroni corrections for sample size differences), but we also report comparisons that approximate significance (P = 0.1–0.05).

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

Descriptive statistics and results of statistical comparisons of humeral cross-sectional shape are provided in Tables 13. In general, there is support for the hypothesis that circular humeri are associated with suspensory locomotion. However, as illustrated in Fig. 2, there is a great deal of variation in Imax/Imin ratios for each taxon, and their shape ratios overlap extensively. The highly forelimb suspensory Hylobates, Symphalangus, and Pongo do have relatively circular humeral cross-sections (Fig. 3). All three of these apes, however, are not significantly different from each other, and their humeral cross-sections are not more circular than those of Pan. Moreover, although the mean values of humeral Imax/Imin at both H40 and H50 are closer to 1.0 in all four of these hominoids when compared with both Gorilla subspecies, these differences are only significant between (1) Symphalangus/Pongo/Pan and G. g. gorilla at H40, and (2) Symphalangus/Pongo and G. g. gorilla at H50 (Table 2). Furthermore, the two subspecies of Gorilla are not statistically different from each other. Ranked ordered correlations between reported suspensory behavior (i.e., percent suspension relative to total arboreal locomotor behavior; see Table 1) and mean Imax/Imin at H40 are not significant within hominoids (rho = −0.143, P = 0.713), but they do approach significance at the H50 level (rho = −0.771, P = 0.103). In both cases, the correlations are negative, that is, greater suspension is correlated with a lower Imax/Imin ratio.

image

Figure 2. Box-and-whiskers plots of Imax/Imin ratios at: (A) 40% of humerus length [H40] and (B) midshaft [H50]. Horizontal lines within each box illustrate the median of the distribution. Boxes envelop the interquartile range (50% of values) of the sample distribution, and whiskers encompass the range excluding outliers. Filled circles beyond whiskers indicate outliers. Values closer to 1.0 represent more circular cross-sections.

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image

Figure 3. Representative images of humeral cross-sections in some suspensory and quadrupedal primates and suspensory sloths examined in this study.

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Table 2. Mann-Whitney U-test results
H40Hylobates larSymphalangus syndactylusPongo pygmaeusPan paniscusPan troglodytesGorilla g. beringeiGorilla g. gorillaMacaca fascicularisPapio cynocephalusAteles fuscicepsLagothrix lagotrichaAlouatta palliataCebus apella
Bradypusnsnsnsnsnsnsabbnsnsnsb
Hylobates nsnsnsnsnsnsbbnsnsnsb
Symphalangus  nsnsnsnsbbbnsnsnsb
Pongo   nsnsnsbbbnsnsnsb
P. paniscus    nsnsnsbbnsnsnsb
P. troglodytes     nsbbbnsnsnsb
G. g. beringei      nsbbnsnsnsb
G. g. gorilla       nsnsnsaans
Macaca        nsbbans
Papio         abbns
Ateles          nsnsb
Lagothrix           nsb
Alouatta            b
H50Choloepus sp.Symphalangus syndactylusPongo pygmaeusP. paniscusP. troglodytesGorilla g. beringeiGorilla g. gorillaMacaca fascicularisPapio cynocephalus
  1. a

    P = 0.1–0.05

  2. b

    P < 0.05.

Bradypusnsnsansbbbbb
Choloepus nsnsnsnsnsbbb
Symphalangus  nsnsnsnsbbb
Pongo   nsnsabbb
P. paniscus    nsnsnsnsb
P. troglodytes     nsnsbb
G. g. beringei      nsbb
G. g. gorilla       ab
Macaca        a
Table 3. Ranked ordered correlations between reported suspensory behavior and mean Imax/Imin ratio
Slice location and groupSpearman's rhoP value
H40
Hominoids only−0.1430.713
All catarrhines−0.5940.099
Platyrrhines0.1051.000
H50
Hominoids only−0.7710.103
All catarrhines−0.8980.005

Compared with all hominoids that engage in some level of forelimb suspension, the quadrupedal cercopithecoids (Macaca and Papio) have significantly more elliptical humeral cross-sections at both levels (except when compared with G. g. gorilla at H40; Figs. 2, 3). Papio has an Imax/Imin ratio that deviates the most from 1.0 at midshaft (H50) and is significantly different from all other taxa sampled except Macaca. Ranked ordered correlations between reported forelimb suspensory behavior and mean Imax/Imin at H40 approach significance within the cattarhine sample (rho = −0.594, P = 0.099), and are significant at the H50 level (rho = −0.898, P = 0.005). Again, both correlations are negative as predicted.

Among platyrrine primates, atelines (Ateles, Lagothrix, and Alouatta) that engage in suspensory locomotor behaviors (with and without their tails) have significantly more circular cross-sections at H40 when compared with the less suspensory Cebus (Fig. 2A; Table 2). Although not statistically significant, the most forelimb suspensory ateline, Ateles, is observed to have a more elliptical humeral cross-section compared with Alouatta, the least suspensory ateline. Ranked ordered correlations between reported suspensory behavior and mean Imax/Imin at H40 are not significant within the platyrrhine sample (rho = 0.105, P = 1.0).

Both sloth genera have Imax/Imin ratios close to 1.0, thus making their humeral cross-sections near-circular in shape. When compared with primates, their humeral cross-sections at H50 are as circular as those seen in hominoids at H50 (Figs. 2B, 3). Bradypus also has a relatively circular cross-section at H40, and its Imax/Imin ratios overlap with both suspensory apes and the atelines at this humeral level (Figs. 2A, 3).

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

Functional interpretations from the few previous studies of long bone cross-sectional shape using Imax/Imin ratios have provided mixed results (Carlson, 2005; Carlson et al., 2006, 2008, 2011; Morimoto et al., 2011). Possible reasons for these results include the fact that the data have come primarily from a relatively narrow phylogenetic and functional sampling or that the functional signals of the behaviors examined are too fine to tease apart (Carlson, 2005; Carlson et al., 2006). In this study, we attempted to address the first limitation by increasing the taxonomic and behavioral range of species sampled, by including (1) Asian hominoids and ateline primates, because of their habitual use of forelimb suspension, (2) less suspensory Old and New World monkeys (Papio, Macaca, and Cebus), and (3) sloths, because they can serve as functional and phylogenetic “outgroups” for primates when investigating issues of functional morphology associated with suspension (Patel and Carlson, 2008).

As predicted, the most forelimb suspensory hominoid taxa (Hylobates, Symphalangus, and Pongo) tend to have more circular cross-sections at both humeral levels (H40 and H50). Their mean Imax/Imin ratios are close to 1.0. Moreover, their humeral cross-sections are not significantly different from each other, which is not surprising considering that they all engage in similar levels of forelimb suspensory behaviors (∼50% of total arboreal locomotion). These Asian hominoids, however, do not have more circular humeri when compared with either species of Pan, which use forelimb suspensory locomotor behaviors to a lesser degree (<20% of total arboreal locomotor behavior). Furthermore, these hominoids do not have significantly more circular humeral cross-sections than the highly terrestrial and least suspensory G. g. berengei. Rather, the biggest and statistically significant differences are only between G. g. gorilla and the other ape species. But as noted by Remis (1995, 1998) and Doran and Hunt (1994), some individuals of G. g. gorilla engage in similar levels of forelimb suspension as Pan troglodytes (Table 1; see references above).

When compared with apes, quadrupedal cercopithecoids that do not engage in any forelimb suspension have more elliptical humeral cross-sections at both levels. This suggests that their forelimbs may not be subjected to the same degree of variability in bending and torsion as those of apes. In fact, Papio has an Imax/Imin ratio that deviates the most from 1.0 at midshaft (H50) and is significantly different from all other taxa sampled except Macaca. It should be recognized that because most of our differences are between hominoids and cercopithecoids, these cross-sectional shape patterns we observe here might be related to phylogeny and not necessarily function alone. O'Neill and Dobson (2008) have shown that a phylogenetic signal is present in cross-sectional properties of primate long bones. Further study incorporating additional catarrhine primates could be used to test this possibility. In particular, future studies should attempt to compare habitually quadrupedal Macaca and Papio species with other cercopithecoids that have more diverse locomotor behaviors, especially those that have been observed to use varying degrees of forelimb suspension (e.g., Pygathrix cinerea, P. nemaeus, and Trachypithecus delacouri; Wright et al., 2008; Workman and Schmitt, 2012).

Analysis of humeral Imax/Imin ratios in atelines show that they have more circular cross-sections at H40 compared with Cebus. Although it is possible that this may be simply related to phylogeny rather than function (i.e., atelines are more closely related to each other than to Cebus), Ateles and Lagothrix engage in significant amounts of forelimb suspension (with and without the assistance of a tail) and both have relatively circular humeral cross-sections. In fact, active suspensory atelines like Ateles and richochetal brachiating hylobatid apes have similar cross-sectional shapes that are not significantly different from each other. The same is true for non- (or less) suspensory Cebus, Macaca, and Papio (Figs. 2, 3). Therefore, in general these patterns of humeral cross-sectional shape in a more taxonomically diverse primate sample are in line with predictions and do provide some evidence for the hypothesis that forelimb suspensory taxa should have more circular humeri than non- (or less) suspensory taxa (Carlson, 2005).

The two genera of suspensory sloths studied here have similar Imax/Imin ratios as those seen in the most suspensory primates at H50, and as predicted, they are relatively circular in cross-sectional shape like suspensory apes. The three-toed Bradypus also has a relatively circular cross-section at H40, and its Imax/Imin ratios overlap with both suspensory primates and the arboreal atelines at this humeral level. We are unaware of any detailed kinematic data for Bradypus except for Mendel's (1985) study of climbing and terrestrial locomotion, but data from Choloepus under laboratory conditions show that it uses gaits and forelimb kinematics that are similar to those of some arboreal primates, especially lorsies (Nyakatura et al., 2010). Although no kinetic data have been reported for either sloth genus, the converging gait, kinematics and cross-sectional humeral morphology between sloths and primates supports the hypothesis that humeral cross-sectional shape reflects the external forces experienced by the forelimb.

Despite these general primate and sloth patterns supporting our hypothesis, there are several patterns in the sample that are less encouraging. For example, the highly suspensory Asian apes do not have significantly more circular humeral cross-sections than Pan, which is less suspensory and uses more quadrupedal locomotor behaviors. Similarly, although adult Gorilla do not typically engage in the same level of forelimb suspension and other forelimb assisted acrobatic activities in the trees as other apes do, their humeral Imax/Imin ratios are within the observed range of these other apes. Also, the more terrestrial Gorilla g. beringei seems to have a more circular humeral cross-section compared with the more arboreal Gorilla g. gorilla, again contrary to expectations; these results, however, are not statistically significant (Table 2). Also counter to our predictions, the most suspensory New World monkey Ateles is observed to have a more elliptical humeral cross-section compared with both Lagothrix and Alouatta. When compared with Lagothrix, the prehensile tail of Ateles helps reduce side-to-side movements when used during suspension (Schmitt et al., 2005). This could (presumably) reduce levels of multidirectional loading of its forelimb resulting in the more elliptical humeri seen in the Ateles sample.

CONCLUSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

A long bone's cross-sectional geometry can provide researchers information to assist in developing inferences about habitual positional and locomotor behaviors of animals from which kinematics, kinetics, and bone strain data cannot be obtained (e.g., fossils). This study took a rather conservative approach in trying to discern if two general habitual locomotor behaviors, forelimb suspension versus quadrupedalism, can be inferred from humeral cross-sectional shape, and as such builds on the detailed comparative research by Carlson (2005) who investigated the link between long bone cross-sectional shape and specific locomotor behaviors used by African apes. In general, data from more diverse hominoid and nonhominoid taxa lend some support to these previous studies that had found differences between the humeri of suspensory Pan and the more quadrupedal Gorilla (Carlson, 2005). For example, suspensory Asian apes have more circular humeral cross-sections than Gorilla (but not Pan) and arboreal and semiterrestrial quadrupedal cercopithecoids. Suspensory atelines have more circular humeri than the less suspensory Cebus, and each of these groups is more similar to catarrhines with broadly similar behavioral patterns, that is, more and less suspensory, respectively. Additional support for this hypothesis is demonstrated by the morphological convergence seen between suspensory sloths and suspensory primates.

Based on these results, we suggest that Imax/Imin ratios for the humeral diaphysis may be useful for inferring generalized locomotors modes (e.g., forelimb suspension vs. quadrupedalism) in isolated fossil specimens. However, considering the great deal of overlap in the shape ratios documented here, and the sometimes contradictory patterns found within finer taxonomic (and functional) groupings, it is important to also consider other biomechanically relevant cross-sectional properties (e.g., CSAs, second moments of area in specific planes) when reconstructing locomotor behaviors from preserved skeletal remains (e.g., Trinkaus et al., 1991; Lieberman et al., 2004). Continued experimental studies (e.g., see Carlson and Judex, 2007) are also important in testing the relationships between overall circularity as well as more specific cross-sectional geometric properties of long bone diaphyses in response to mechanical loadings. A number of factors, both extrinsic (e.g., differences in substrate reaction and muscle forces) and intrinsic (e.g., genetics, developmental patterning), likely contribute to variation in cross-sectional shape in primates and other animals (e.g., Ruff and Runestad, 1992; Lieberman et al., 2004; Pearson and Lieberman, 2004; Ruff et al., 2006; Hansen et al., 2009; Wallace et al., 2010). Our results support the continued use and study of long bone cross-sectional shape ratios in reconstructing past locomotor behavior but also indicate that these should not be used alone in studies of functional morphology.

Appendix

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED
Table 4. Mann-Whitney U-test results of humeral cross-sectional shape (Imax/Imin ratios) comparing hominoid males to femalesa
TaxonN males/N femalesH40 P valueH50 P value
  1. a

    All comparisons were not statistically significant at the P < 0.05 level.

Pongo pygmaeus10/100.4270.571
Pan troglodytes10/100.7340.076
Gorilla g. beringei5/50.6760.835
Gorilla g. gorilla5/50.8350.403

ACKNOWLEDGEMENTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED

The authors thank Ken Glander, and the curators and staff of the American Museum of Natural History and the Smithsonian National Museum of Natural History for access to specimens in their care. They also appreciate the generosity of the Radiology Department at Stony Brook University Medical Center, the Anthropology Department at Smithsonian National Museum of Natural History, and Holzer Clinic (Athens, OH), and their respective staff for facilitating access to their medical CT scanners. This research benefited from insightful discussions with Kris Carlson.

  • 1

    The four primate specimens not part of the original Ruff (20022002) study were CT scanned following the same protocols used for scanning the sloth material.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. Appendix
  8. ACKNOWLEDGEMENTS
  9. LITERATURE CITED