Unitat de Biofísica, Departament de Bioquímica i Biologia Molecular, and Centre d'Estudis en Biofísica, Facultat de Medicina, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Catalonia, Spain
Biomechanical models are considered to be a very useful tool in biological anthropology and evolutionary anatomy for the exploration of the functional implications of some structural and skeletal design characteristics, and the reconstruction of the behavioral pattern of different extant and fossil primate species (Ruff, 2000; Bertram and Chang, 2001; Schmitt, 2003; Wang et al., 2004; Nagano et al., 2005; Webb and Sparrow, 2007; Curtis et al., 2008). In this regard, research into forearm rotation or pronosupination may be very useful for obtaining further knowledge about adaptation to certain locomotor, positional, and manipulative behaviors of hominoids. Pronosupination is an essential component of the hominoid orthograde corporal plane that, together with some other anatomical and functional characteristics of the upper-limb, enables these primates to execute efficient and sure locomotion in their habitat (Myatt et al., 2012). The rotatory ability of the hominoids' forearm is not only a consequence of its relatively massive rotatory muscles but also of several features of the design of their upper-limb bones (Rose, 1988, 1993). In humans, the entire upper-limb skeletal system underwent coaptation in order to develop a manipulative function, but it maintains the basic structures and capacities that are common to all hominoid species (O'Connor and Rarey, 1979; Stern and Larson, 2001).
Galtés et al. (2008) developed a biomechanical model to calculate the rotational efficiency of the pronator teres muscle of the forearm. Even though this biomechanical model was initially developed using computerized tomography, its application to skeletal remains was later performed using photographs of the distal epiphysis of the humerus (Galtés et al., 2009a). Although this methodology is simple and practical, the technique is limited since spatial representation of the humeral planes is not possible. Therefore, some assumptions about the arm and forearm mechanics and the representation of the geometrical points used to calculate rotational efficiency had to be made.
3D technology is a new tool with many potential applications in physical anthropology (Zumwalt, 2005; Curtis et al., 2008; Harcourt-Smith et al., 2008; Sylvester et al., 2008; De Groote et al., 2010; Marzke et al., 2010; Oka et al., 2010) basically because its extreme accuracy and precision make it particularly appropriate for biomechanical models. The application of the biomechanical model to the calculation of the rotational efficiency of the forearm by means of 3D technology could eliminate the abovementioned limitations, enabling accurate representation of every single geometrical measure needed.
The current study aims to investigate the variability of forearm rotational efficiency using a large sample of humans and 3D technology. Specifically, we test the hypothesis that there is a human pattern of rotational efficiency that reflects the functional specialization of the human upper-limb, which differs from that of nonhuman hominoids. In addition, we determine which structural features of the upper-limb bones have the greatest influence on rotational efficiency variation. This study will contribute to further knowledge of the functional and evolutionary meaning of the skeletal design of the upper-limb, since its results will be essential for a future comparative morphofunctional study with nonhuman extant and fossil hominoids.
MATERIALS AND METHODS
Two different samples, housed at the Unitat d'Antropologia Biològica, Universitat Autònoma de Barcelona (UAB), both from small rural communities from eastern Spain, were included in the study: 7 skeletons from a contemporary osteological collection of known age and sex (UAB Collection), and 22 well-preserved skeletons recovered from a number of archaeological sites (Table 1). The main criterion for inclusion was good skeletal preservation, in order to accurately estimate age and sex. In this regard, these diagnoses were estimated using a multifactorial approach in accordance with the criteria proposed by Buikstra and Ubelaker (1994). Sub-adults were excluded in order to guarantee that all the epiphyses were completely fused. Furthermore, individuals exhibiting pathological conditions that might affect the musculoskeletal system of the forearm were eliminated. The entire sample consisted of 29 complete adult upper-limb specimens (humerus, ulna, and radius), including 21 males and 8 females, with similar percentages of both sides.
Table 1. Specimens included in the sample
UAB, Unitat d'Antropologia Biològica (Univeristat Autònoma de Barcelona); IMAZ, Antropologisches Institut und Museum der Universität Zürich-Irchel; EBD, Estación Biológica de Doñana (Consejo Superior de Investigaciones Científicas).
Mediterranean archaeological populations
Right or left humerus, ulna, and radius, depending on the individual
Documented collection from UAB
Right or left humerus, ulna, and radius, depending on the individual
Right humerus, ulna, and radius
Right humerus, ulna, and radius
Left humerus and radius. Right ulna
To properly study human variability, an out-group composed of three nonhuman hominoid specimens (chimpanzee, gorilla, and orangutan) was also included in the sample (Table 1). This out-group is expected to be out of human variation range, so it will enable us to better assess the extent of human variability itself. All of the specimens were nonpathological and wild-shot.
Biomechanically, the rotational efficiency of the forearm is defined from the geometric relationship between both attachment sites of the pronator teres muscle during pronosupination (Galtés et al., 2008, 2009a). In the current study, the rotational efficiency of the forearm in a full elbow extension (180°) and an intermediate position of the elbow (90°) were analyzed. Rotational efficiency was calculated from both osteometrical and geometrical parameters of the elbow and forearm (Galtés et al., 2008). Osteometrical parameters (lf, lpr, dr, dc, λ and AO, Fig. 1) were measured directly on dry bones (Galtés et al., 2009a), whereas geometrical parameters were assessed using 3D images of the humeri, which were obtained using NextEngine's 3D Scanner and processed using ScanStudio HD (2006) and Rhinoceros 4.0 SR1 (2007). This processing consisted of several steps. First, the longitudinal axis of each humerus, defined as the intersection between humeral coronal and sagittal planes (Ruff, 2002), was represented. We defined the coronal plane as a plane that passes through the center of a sphere adjusted to the humerus head and through the elbow flexion axis, defined by Bottlang et al. (2000) as a straight line adjusted to the centers of the condyle and the medial and lateral shifts of the trochlea. The sagittal plane was defined as a plane perpendicular to the coronal plane that passes through the center of the lateral lip of the trochlea and the center of the sphere adjusted to the head of the humerus (Fig. 2).
The proximal attachment site of the pronator teres muscle was also represented (point B, Figs. 1 and 3) (Galtés et al., 2009a) in the 3D image of the humerus. This point was defined as the furthest point of the medial epicondyle from the sagittal plane, since it was described by Rouvière and Delmas (1988) as the point at the apex of the medial epicondyle. The use of tridimensional images of the humeri, rather than photographs of their distal epiphyses (Galtés et al., 2009a), enabled us to improve the accuracy and precision when placing the humeral axis and point B.
To reduce the complexity of the analysis, we assumed that humeral and forearm axes coincide at the center of the lateral lip of the humeral trochlea (Galtés et al., 2009a), both axes being aligned and perpendicular in elbow position at 180° and 90° of flexion, respectively.
The distance between planes P1 and P3 (l1) decreases when the elbow is flexed (see Fig. 1). Galtés et al. (2009a) defined this distance as the sum of lpr (Fig. 1) and distance d (Fig. 3). The former is an osteometrical measure taken directly on the radius, whereas the latter is the distance between point B and a plane tangential to the humeral condyle, whose position depends on both the carrying angle and the elbow position. Using 3D images of the humeri, distance d was assessed at full extension and semiflexion elbow positions (Fig. 3).
The remaining geometrical parameters needed to calculate rotational efficiency are measured from the resulting projection of plane P1 on P3 (Galtés et al., 2008). These parameters are represented on plane P1 for better visualization (Figs. 1 and 4) (Galtés et al., 2009a). This plane passes through point B. At 180°, plane P1 was represented as a plane perpendicular to the humeral axis. At 90°, it was represented as a plane parallel to the coronal plane of the humerus (Fig. 4).
The 95% confidence intervals for the mean of rotational efficiency values and of the positions of maximum efficiencies in the pronosupination range were calculated in the human sample to establish statistical comparisons with the nonhuman specimens. Nonparametric tests were performed to test differences between males and females in humans, as well as differences in maximum efficiencies and in the position of these maximums between both elbow positions. A principal components analysis (PCA) was performed to determine which structural parameters contribute the most to variation in rotational efficiency. Moreover, a stepwise regression analysis including the same parameters was performed in order to determine which are the most important for the determination of maximum efficiency and the position of this maximum in the pronosupination range. All analyses were performed using SPSS 15.0 software (2006).
Table 2 shows the descriptive statistics for the osteometrical and geometrical parameters calculated to analyze the rotational efficiency of the human forearm, as well as their values for the nonhuman hominoids. All the parameters are significantly higher in human males than in females, except for carrying angle of the elbow (λ) and φ (90 and 180°) (Table 2).
Table 2. Descriptive statistics of osteometrical and geometrical parameters
Pan troglodytes (N = 1)
Gorilla gorilla (N = 1)
Pongo pygmaeus (N = 1)
Males (N = 21)
Females (N = 8)
l1 is the sum of lpr (Fig. 1) and d (Fig. 3). AO′ (rotational radius of the pronosupination movement) is calculated as a function of AO (radial curvature, Fig. 1) (Galtés et al., 2009a). Distance values are in centimeters. Bold values indicate statistically significant differences between males and females (Mann-Whitney: P < 0.05).
In humans, for a given elbow position, rotational efficiency varies throughout the entire rotational range (Fig. 5). With the elbow fully extended, rotational efficiency is minimal when the forearm is completely supinated. From this position, efficiency increases and reaches a maximum (x = 0.67; 95%CI = 0.64/0.71) as the neutral-semipronation position is approached (x = −14°; 95%CI = −15.2°/−12.7°); then efficiency decreases as the radius moves into a full-pronation position. Moreover, when the human elbow is semiflexed (90°), maximum efficiency undergoes an increase (x = 0.71; 95%CI = 0.67/0.74) and displaces towards a neutral-semisupination position (x = 7°; 95%CI = 5.7°/7.8°) relative to the full extension position.
Differences in maximum efficiency values and in the position of these maximums between both elbow positions (full extension and semiflexion) are statistically significant (Wilcoxon: Z = −4.314; P < 0.01; Wilcoxon: Z = −4.708; P < 0.01, respectively).
Maximum efficiency values are significantly higher in human males than females both in extension and flexion of the elbow. Nevertheless, no differences in the positions of the maximums between sexes are observed (Table 3).
Table 3. Values for maximum efficiencies and positions of the maximums in human males (N = 21) and females (N = 8)
Bold values indicate statistically significant differences between males and females (Mann-Whitney: P < 0.001).
Maximum efficiency (180°)
Maximum efficiency (90°)
Position of maximum efficiency (180°)
Position of maximum efficiency (90°)
To evaluate the variation range for the rotational efficiency of the forearm, we compared the values obtained in humans with those of three nonhuman hominoids (chimpanzee, gorilla, and orangutan). Comparisons were performed using the 95% confidence interval of the mean for the human sample. Results show (Fig. 6) that efficiency values as a function of the forearm rotational stage for humans are mainly lower than those for nonhuman hominoids in both extension and flexion positions. Additionally, the maximum efficiency positions in nonhuman hominoids are out of the range for humans (Table 4), except for the chimpanzee's elbow extension, whose value is within human range, although close to the lower limit. The most remarkable differences are those for extension in the gorilla and flexion in the orangutan. In the former, the maximum displaces several degrees towards a more pronated position, whereas in the latter, it displaces towards a more supinated position.
Table 4. Positions of maximum rotational efficiencies of the analyzed individuals in the pronosupination range
The PCA of the structural parameters from which rotational efficiency is calculated is represented in Fig. 7. The first component of the PCA is mainly correlated with all parameters (Fig. 7A), except for φ (180°), which is principally correlated with the second component (Fig. 7B). The first component separates humans from nonhuman hominoids (Fig. 7C), indicating higher values of AO′, l1 (90° and 180°), O′B′ and φ (90°) in nonhuman hominoids. Nevertheless, this separation is not observed for the second component, indicating major intra and interspecific variation of φ (180°). Human females are grouped in the negative extreme of the first component, because of their lower values of AO′, l1 (90° and 180°) and O′B′, although both sexes are overlapped (Fig. 7C).
The regression analysis between efficiency features and structural parameters essentially shows that maximum efficiency values are mainly correlated to O′B′, whereas the positions of these maximums in the pronosupination range are principally correlated to φ (Table 5).
Table 5. Summary of the stepwise multiple regression analysis between geometrical and osteometrical parameters and different efficiency features
Maximum efficiency (180°)
O′B′, AO′, l1 (180°)
Maximum efficiency (90°)
O′B′, AO′, l1 (90°), φ (90°)
Position of maximum efficiency (180°)
φ (180°), O′B′, l1 (180°), AO′
Position of maximum efficiency (90°)
φ (90°), O′B′, l1 (90°), AO′
Pattern of Human Rotational Efficiency
The application of the biomechanical model (Gatlés et al., 2008, 2009a) to a human sample enabled us to define a pattern of forearm rotational efficiency for humans. When flexing the elbow from a fully extended to a semiflexed position, maximum rotational efficiency displaces from a neutral-semipronation towards a neutral-semisupination position of the forearm. The human pattern also shows an increase in efficiency during flexion, resulting in greater efficiency over the entire supination range. These results confirm previous observations from in vivo rotational efficiency analysis (Galtés et al., 2008). Differences in maximum rotational efficiency values between sexes are triggered by size-dependent parameters (O′B′, AO′ and l1). The forearm position of these maximums, however, does not differ between males and females because it is basically determined by size-independent parameters (φ).
The nature of the human pattern may be related to the main manipulative function of the human upper-limb (Marzke, 1997; Dunsworth et al., 2003; Drapeau et al., 2005). In this regard, the fact that rotational efficiency is maximal when the forearm is close to the neutral position supports the relationship between this position and the functional position of the forearm, which implies a state of natural equilibrium between the antagonistic muscle groups in order to minimize expenditure of muscular energy (Kapandji, 2002). This forearm position also implies an optimum position of the hand for grasping. In neutral position, the axis of the grip is in line with the axis of pronation-supination (Kapandji, 2002), in order to enhance the precision of the grip (Marzke, 1997). Moreover, the pattern of human rotational efficiency displays a coupling between pronation and elbow extension and between supination and elbow flexion, which was also observed in an experimental kinematic study during the human reach-and-grasp task (Lan and Baker, 2004).
The pattern of rotational efficiency in humans differs from the efficiency curve observed in the analyzed nonhuman hominoid specimens. This finding can be interpreted in the light of morphofunctional adaptations. The mainly lower rotational efficiency in humans is in agreement with the higher functional requirements of the upper-limb in nonhuman hominoids (Crompton et al., 2008). In the studied gorilla specimen, the displacement of the maximum efficiency towards a more pronated position during elbow extension implies a remarkably greater efficiency over the entire pronation range. As regards the analyzed orangutan specimen, we observe a remarkably higher maximum efficiency and major displacement to supination of its maximum efficiency, both in flexion of the elbow. The fact that we studied one specimen of each nonhuman taxon imposes limitations on the interspecific functional interpretations of our results. Certainly, this area clearly warrants further research and a broader comparative sample of nonhuman hominoids should be considered. Nevertheless, our results indicate a tendency, displaying nonhuman hominoids as an out-group with respect to humans in terms of rotational efficiency.
Anatomical Parameters on Which Rotational Efficiency Depends
In the current study, the application of 3D technology to the biomechanical model enables optimization of the technique, bringing the study of efficiency in skeletal remains closer to its analysis in vivo through computed tomography (Galtés et al., 2008). It enables us to obtain, for instance, more accurate variables in relation to the size and shape of the medial epicondyle of the humerus.
Our results show that medial epicondylar form is the determining factor of the features of the rotational efficiency of the forearm. Higher rotational efficiency is mainly due to a more pronounced medial epicondyle projection (O′B′). This explains why rotational efficiency tends to be higher in nonhuman hominoids compared to humans. Orientation of the medial epicondyle (φ) mainly determines the maximum efficiency position. In extension of the elbow, φ is a measure of the anteroposterior orientation of the medial epicondyle, a trait that is highly correlated (Pearson: r = 0.915; P < 0.01) with the retroflexion of the medial epicondyle as defined by MacPhee and Meldrum (2006). In elbow flexion, φ is a proxy for proximodistal orientation of the medial epicondyle. It is, therefore, possible to state that the shape of the medial epicondyle mainly determines the differences between humans and nonhuman hominoids in terms of the maximum efficiency position. The results indicate that, in elbow extension, a more retroflexed epicondyle leads to the displacement of the maximum efficiency towards a more pronated position, e.g., gorilla. Moreover, in elbow flexion, a more proximal projected epicondyle leads to the displacement of the maximum efficiency towards a more supinated position, e.g., orangutan. These displacements may be related to functional aspects.
In evolutionary anthropology, humeral medial epicondyle retroflexion is a widely used morphological feature of the primate elbow in the reconstruction of the locomotor habits of extant and fossil primate taxa (Fleagle, 1988; Lague and Jungers, 1996; Bacon, 2000). In contrast, proximodistal medial epicondyle orientation is not a commonly used parameter in such studies. The results of the current study provide further insight into the functional significance of the humeral medial epicondyle, specifically concerning the relationship between its shape and the rotational efficiency of the forearm. In this regard, our results highlight the importance of proximodistal orientation, rather than anteroposterior orientation (retroflexion), of the medial epicondyle in the analyses aiming to differentiate humans from other hominoid species. We found that whereas proximodistal orientation of the medial epicondyle — φ (90°) — is a skeletal feature that presents differences between humans and nonhuman hominoids, anteroposterior orientation of the medial epicondyle — φ (180°) — does not. The latter parameter shows major variability in the human sample, which encompasses the values observed in the orangutan and chimpanzee. We, therefore, suggest that proximodistal orientation of the medial epicondyle may be suitable for use as a parameter to infer behavioral aspects from skeletal remains and fossils.
The results of the present study emphasize the role of the form of the humeral medial epicondyle in the rotational efficiency of the forearm. Even though their asseveration requires an application of this methodology to a broader comparative sample, some of the characteristics of the curves obtained for each nonhuman hominoid species show the potential application of the forearm efficiency model to evolutionary studies.
In summary, we have applied, using 3D methodology, the biomechanical model to calculate the rotational efficiency of the forearm using a large human sample in order to obtain a pattern of human rotational efficiency, which clusters humans and eliminates the studied nonhuman hominoid specimens. This is a useful tool for studies of plasticity in upper-limb design, since morphological issues and their relationship with a functional feature, such as rotational efficiency, will enable us to understand how functional and structural changes influence each other. In this regard, we will be able to obtain further knowledge about the functional interpretations of the functional position of the forearm and the selective pressures that have related it to the neutral position, in which the efficiency tends to be maximal. Furthermore, in the field of evolutionary anthropology, the human pattern should be compared with patterns of extant and fossil primate taxa. The application of the biomechanical model of the rotational efficiency of the forearm could contribute to a more accurate interpretation of the skeletal adaptation of the hominoid upper-limb.
The authors thank Josep Fortuny, Institut Català de Paleontologia, for helping them with the 3D images treatment. They are also grateful to José Cabot, Estación Biológica de Doñana, and Gemma Noés, Unitat d'Antropologia Biològica (Universitat Autònoma de Barcelona), for part of the analyzed sample.