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Dossier spécial - BipédieS chez les Primates : de la philosophie au comportement

Habitual locomotor types and the shape of lower leg bones in primates, especially in hominoids

Types locomoteurs habituels et forme des os de la jambe chez les primates, en particulier chez les hominoïdes
Tasuku Kimura

Résumés

La dominance mécanique des membres postérieurs par rapport aux membres antérieurs dans le comportement positionnel des primates a été établie. Parmi les os des membres postérieurs des primates, c'est le fémur qui a été le plus étudié. Les os de la jambe des primates n'ont pas été étudiés précisément en relation avec le comportement locomoteur. Dans cette étude, les os de la jambe des primates ont été examinés chez 316 individus de 80 espèces et 47 genres. Les longueurs et largeurs relatives du tibia et de la fibula ont été comparées suivant les types de locomotion habituels, en se concentrant sur les hominoïdes. Différents types de locomotion ont été caractérisés chez les hominoïdes, tels que la brachiation chez les grands singes de petite taille (hylobatidés), la quadrupédie sur l’articulation des phalanges des mains ou sur les poings et le balancement par les bras, y compris les comportements locomoteurs des membres antérieurs avec une posture orthograde du torse, chez les grands singes, et la bipédie chez les humains. Les os de la jambe des grands singes présentent des diamètres relativement importants, en particulier de grandes largeurs distales par rapport à leur longueur. Les humains présentent également des diamètres relativement grands en de nombreux points de mesure, comme les grands singes, mais leurs extrémités distales sont de forme différente. Les os de la jambe sont relativement robustes chez ces espèces, où une plus grande proportion du poids du corps est habituellement supportée par les membres postérieurs. Parmi les singes quadrupèdes, y compris les prosimiens, les animaux ayant adopté un mode de vie plus terrestre présentent des diamètres plus grands par rapport à la longueur que les animaux arboricoles pour de nombreuses mesures. Les grands singes et les singes qui ont adopté la brachiation ou le balancement par les bras dans leur répertoire locomoteur dans les environnements arboricoles présentent une extrémité distale et une largeur de malléole tibiale relativement grandes par rapport aux singes quadrupèdes. Une grande largeur de la cheville par rapport à la profondeur et une grande largeur de la malléole faciliteraient les mouvements d'inversion et d'éversion. La cheville humaine est relativement étroite par rapport à celles des grands singes et est adaptée principalement aux mouvements de flexion/extension dans un plan parasagittal. La forme des os de la jambe est donc liée aux différences de type locomoteur et d'utilisation du substrat chez les espèces de primates.

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Notes de la rédaction

Received 15/05/2021, accepted after revisions 17/01/2022, published online 24/02/2022 in the context of the special issue "BipedalismS in primates" (Varia 2021).

A translated version, in french, is available online.

Une version traduite, en français, est disponible en ligne.

Texte intégral

1 Introduction

1Compared with non-primate terrestrial quadrupedal mammals, primates exhibit some unique characteristics in their hindlimb bones (Alexander et al. 1979; Kimura, 1991, 1995; Polk et al. 2000) and locomotor behavior, in which they support and accelerate their body more by their hindlimbs than their forelimbs during dynamic and static quadrupedalism; this is referred to as hindlimb dominance (Krüger, 1943; Prost, 1965; Iwamoto & Tomita, 1966; Hildebrand, 1967; Tomita, 1967; Kimura et al. 1979; Kimura, 1985, 1992, 2002; Reynolds, 1985; Demes et al. 1994; Larson et al. 2000; Schmitt & Lemelin, 2002; Schmitt & Hanna, 2004; see also Druelle et al. 2019). By contrast, non-primate mammals usually adopt forelimb dominance (Thompson, 1917; Manter, 1938; Barclay, 1953; Björck, 1958; Pratt & O’Connor, 1976; Kimura et al. 1979). These features are explained in relation to the primate’s substrate use, that is, the arboreal one (Kimura et al. 1979). Human bipedalism is also commonly discussed from the perspective of primate arboreal locomotor patterns (Stern, 1975; Kimura et al. 1979; Kimura, 1985, 2019; Schmitt, 2003; Crompton et al. 2003, 2008; Nakatsukasa, 2004; Thorpe et al. 2014; White et al. 2015; Senut et al. 2018).

2Among primate species, the size and shape of the limb bones have been discussed in relation to locomotor behaviors (Jungers, 1985; Strasser, 1992; Jungers et al. 1998; Schmitt, 2003; Kimura, 2002, 2003; Ruff, 2002; Perry et al. 2017). Due to the special locomotor behavior of humans, bipedalism, their lowerlimb bones have unique characteristics that distinguish them from other primate species, that is, monkeys, including prosimians, and other hominoid species. Humans possess adducted knees and vertically oriented lower leg bones (Latimer et al. 1987; Tardieu & Preuschoft, 1996; Tardieu, 2010; DeSilva & Parakyrikos, 2011; Raichlen et al. 2015). This structure helps to situate the center of body mass directly over the knee and ankle in the frontal plane during bipedal walking, together with the laterally inclined femoral shaft from the knee. The lower articular surface of the human tibia is horizontal in the frontal plane and ankle movement is restricted mainly in the parasagittal plane.

3Conversely, the knees of extant apes are abducted and their lower leg bones incline laterally from the ankle in the frontal plane (Latimer et al. 1987; DeSilva, 2009). Extant great apes adopt a unique locomotor type, knuckle or fist quadrupedalism, on nearly horizontal substrates, and arm-swinging, including forelimb locomotor behaviors, in arboreal environments (Remis, 1998; Thorpe & Crompton, 2005; Sarringhaus et al. 2014; Hunt, 2016). In knuckle or fist quadrupedalism, the dorsal side of the hands supports the body, a type never adopted by other primates or other quadrupedal mammals, except for the giant anteater (Orr, 2005). Great apes sometimes adopt a hindlimb-supported nearly orthograde posture and locomotion, bipedalism (Remis, 1995, 1998: Thorpe & Crompton, 2005; Sarringhaus et al. 2014; Hunt, 2016; Kimura, 2019), but during which, their knees are always abducted and their hips are always flexed (Kimura et al. 1979; Kimura, 1985, 2019; O’Neill et al. 2018).

4Extant lesser apes adopt mainly true brachiation, that is, bimanual locomotion under branches including ricochet. Lesser apes occasionally stand and walk bipedally above mostly horizontal substrates in both arboreal and terrestrial environments. During bipedal positional behavior, their knees are abducted and their hips are always flexed (Kimura et al. 1979; Kimura, 1985; Vereecke et al. 2006). Thus, each subgroup of apes is characterized by its own locomotor type.

5In addition, factors other than locomotor behavior influence bony morphology. Size is an important factor in terms of bone shape. The body size of lesser apes is smaller than that of great apes or humans. Monkeys, including prosimians, are usually much smaller than the great apes and humans. Based on mechanical requirements related to scaling constraints, large-bodied mammals have lager relative bone diameters than smaller bodied ones (Galilei, 1638; Schultz, 1953; Alexander et al. 1979; Jungers, 1985; Kimura, 1994). If the length of an animal doubles and its size is in proportion, then its body mass becomes eight times larger, but the cross section of its bone shafts and articular surfaces becomes only four times larger. To support the compressive force caused by the body mass, the areas of the cross section and articular surface must become larger than the proportional scaling. This large area is usually acquired through large bone diameters. Because the long bone forms a tube with a medullary cavity, not only the outer diameter, but also the cross-sectional geometry (CSG) of the bone is important for detailed mechanical discussions (for nonhuman primate bones, see e.g., Burr et al. 1981; Schaffler et al. 1985; Ruff, 1987, 1989; Demes & Jungers, 1989; Jungers & Burr, 1994; Kimura, 1995, 2002, 2003; Jungers et al. 1998; Connour et al. 2000; Yamanaka et al. 2005; Carlson et al. 2005; Marchi, 2007, 2015; Pina et al. 2012; Mongle et al. 2015). To obtain a large sample size, the CSG was not included in the present study because of the technical difficulties involved with measuring it on a large number of materials in the institutions in which they were stored. Many institutions do not have a useful apparatus to measure the CSG, and it is difficult to remove materials from one institution to another. However, the outer diameters of the long bone can demonstrate the CSG in some instances (Kimura & Takahashi, 1992; Stock & Shaw, 2007).

6Comparisons of the primate long bone shape of the hindlimbs in relation to locomotor type have been carried out focusing mainly on the femur (e.g. Jungers et al. 1998; Kimura, 2002; Yamanaka et al. 2005; Hunt, 2016). The lower leg bones of primates should be examined more precisely (Marchi, 2007, 2015; Turley et al. 2011). Characteristics of vertically standing human lower leg bones should be analyzed in human bipedalism compared with primate bones, especially hominoid bones. Given this background, the present study aimed to compare the morphology and elucidate the characteristics of lower leg bones among living primates from the perspective of habitual locomotor type, with a focus on hominoid bones.

2 Materials and Methods

7The lower leg bones of extant primates, that is, the tibia and fibula, from 316 individuals, 80 species, and 47 genera (Table 1) were examined at the following institutions: the University Museum, the University of Tokyo, Tokyo; Primate Research Institute, Kyoto University, Inuyama; Japan Monkey Centre, Inuyama: Anatomical Department of the Dokkyo University School of Medicine, Mibu; Anthropologisches Institut und Museum, Universität Zürich-Irchel, Zürich; Musée Royal de l’Afrique Central, Tervuren; and Powell-Cotton Museum, Birchington. All bones were adult bones with closed epiphyseal lines. No pathological traits were macroscopically observed except senile changes. Great ape samples included common chimpanzees, bonobos, gorillas, and orangutans.

Table 1

Table 1

Number of materials

8Extant primate species were grouped according to habitual locomotor type (Kimura, 2002, 2003) as follows (Table 2): the first six groups are arranged locomotor types adapted from the different substrate, the arboreal to the ground environments; from brachiation (abbreviation: Brach), limited to only true brachiation by gibbons; arm-swinging, including torso-orthograde forelimb locomotor behaviors, and branch quadrupedalism (As/Qbw), such as many atelines, some leaf and colobus monkeys; slow climbing quadrupedalism (Qsc), adopted only by some prosimian species; branch quadrupedalism (Qbw), the general arboreal four-limb locomotion mainly above branches; ground and branch quadrupedalism (Qgw/bw), four-limb locomotion in both the arboreal and the terrestrial environments by some macaques and cercopithecids; to ground quadrupedalism (Qgw), four-limb locomotion mainly on the ground by baboons, mandrills, and patas monkeys. Next come three other different types: knuckle or fist quadrupedalism and arm-swinging (K/FQ) by great apes; vertical clinging and leaping (Vcl), adopted by some prosimians, tentatively including tarsiers in this paper; and bipedalism (Biped), adopted by humans only.

Table 2

Table 2

Locomotor type

9The above habitual types mainly followed those by Napier and Napier (1985). Hunt and colleagues (1996) reported on the precise primate locomotor modes. The locomotion of each individual could be observed in the field classified by each mode above and quantitatively analyzed. This technique was useful for analyzing the locomotion of an individual. To group primate species from the viewpoint of locomotion, the habitual locomotor type of each species was used in this study, given the limitation that the ‘habitual locomotion type’ could describe few of the other detailed locomotion modes in the same species.

10Linear measurements were performed using a 0.1-mm sliding caliper (Mitsutoyo, Tokyo, Japan) and 1-mm measuring boards. Measurements were mainly made according to the method by Martin and Saller (1957), with some modifications for application to nonhuman primate bones (Kimura, 2002) as follows: the breadth of the tibial mid-length was a projected diameter perpendicular to the maximum antero-posterior diameter; the distal breadth of the tibia was the projected diameter of the bone to the transverse axis of the distal articular surface; the distal depth was measured perpendicular to the breadth; the breadths of the articular surfaces on the distal tibia followed those by DeSilva (2009); and other additional measurements not in Martin and Saller (1957) were as in Kimura (2002). The pair of the tibia and fibula was used from the same side of a single individual, with the right side selected first. If difficulties were encountered while measuring the right side, for instance, the loss of or break of one side in storage, then both left-side bones of the same individual were used.

11Because of the large variety of body sizes in primates, comparisons were made based on relative values. Body mass has typically been used to standardize the size (e.g. Alexander et al. 1979; Kimura, 2002, 2003); however, only around half of the present materials had reported body masses. As a standard, many works have used the average species body mass reported from different samples (e.g. Ruff, 1987; Kimura, 2002). This method is accepted to some extent when comparisons are made at the species level. However, this study aimed to compare individual bones first, so this method was not adopted. The geometric mean of measurements (Deutsch et al. 2020) and Procrustes analysis (Turley et al. 2011; Tallman et al. 2013) are also used to standardize the size. These methods are useful for the detailed analysis of small parts, such as fragmental fossil materials, but would be difficult to apply to the analysis of large bones. In the present study, the linear bone measurements were mainly compared with the bone length, which could be accurately measured in each individual. This method also has some limitations that will be described later.

12Statistical significance between the sample groups was tested using Tukey’s multiple comparative procedure. Least squares linear regressions (LRs) of the groups after transformation to logarithms were compared using analysis of covariance. If the slopes of the LRs were not significantly different between groups, then the difference in intercepts was also tested.

3 Results

13Relative measurements were compared among the locomotor type groups (Fig. 1). The relative maximum mid-length shaft diameter of the tibia was usually significantly large in the Qgw, K/FQ, and Biped locomotor types, that is, in the large-sized hominoid species and the terrestrial Cercopithecoids (Fig. 1: Aa). Specifically, the K/FQ and Biped groups also showed significantly larger relative values in many measurements compared with the other groups, such as the fibular shaft diameter (Fig. 1: Ba), the tibial and fibular proximal and distal breadths (Fig. 1: Ab; Ac; Bb), the distal breadth of articulated lower leg bones (Fig. 1: Ad), and the depth of the tibial medial articular surface (Fig. 1: Ae). The Qgw and Qgw/bw groups showed significantly larger relative diameters of the tibia compared with that in the Qbw group in the depth of the tibial medial articular surface (Fig. 1: Ae), and the mid-length diameters of the tibia and fibula (Fig. 1: Aa; Ba). The former groups employed frequent ground quadrupedalism, and the latter group was the arboreal quadruped. The relative breadth of the malleolus compared with the total distal end of the tibia was significantly larger in the K/FQ, Qsc, and Vcl groups than in many other locomotor groups, including bipedal humans (Fig. 1: Ah). Compared with the length, the fibular distal breadth was significantly large in the Brach and K/FQ groups, namely apes, and in the arboreal Qsc group (Fig. 1: Bc). A significantly large distal breadth compared with the depth in the tibia was observed in the Brach, As/Qbw, and K/FQ groups, who employed brachiation or arm-swinging in their locomotion, and in the Qsc group, all groups used the arboreal environmets (Fig. 1: Af). The Brach and K/FQ groups showed large fibular breadth, that is, the malleolar breadth, compared with depth (Fig. 1: Bd). On the other hand, the fibular distal breadth was significantly small compared with the depth in the Qgw/bw, Qgw and Biped groups, the ground users (Fig. 1: Bd). The Qsc and Vcl groups showed significantly large tibial malleolar breadth compared with the depth (Fig. 1: Ag). The breadth of the anterior margin compared with that of the posterior margin of the tibial lower articular surface was significantly small in the Biped human group compared with the As/Qbw, Qgw, K/FQ, and Vcl groups (Fig. 1: Ai).

Comparisons of relative bone diameters among different locomotor types. Above: Boxplots of each type. Bottom: Tukey’s multiple comparative procedure. *: p<0.05; **: p<0.01. For the abbreviations of locomotor types, see Table 2 and the text. A: Tibia. Aa) Maximum mid-length diameter x 100 / total length; Ab) Proximal breadth x 100 / total length; Ac) Distal breadth x 100 / total length; Ad) Distal breadth of the two articulated lower leg bones x 100 / tibial total length; Ae) Depth of medial articular surface x 100 / total length; Af) Distal breadth / depth; Ag) Malleolar breadth / depth; Ah) Breadths of malleolus / distal end; Ai) Breadths of distal articular surface margins anterior / posterior.

Figure 1B

Figure 1B

B: Fibula. Ba) Maximum mid-length diameter x 100 / maximum length; Bb) Maximum diameter of the head x 100 / maximum length; Bc) Malleolar (=distal) breadth x 100 / maximum length; Bd) Malleolar breadth / depth.

14Based on a comparison of the proportion of dimensions to length using LR analysis (Fig. 2), the Biped and K/FQ groups were distinguishable in terms of the length of both the tibia and fibula. In the present materials, the averages of the total length of the tibia and the maximum length of the fibula were 275.6 mm and 238.7 mm, respectively, in great apes, and 319.3 mm and 316.2 mm, respectively, in humans. The results of the LR analysis of the two groups were then separately compared with those of the other small primate groups, including lesser apes and monkeys. Bipedal human bones, which were the longest among the primate bones, showed similar slope values compared with those of small primates in many tibial calculations, including the maximum diameter of the tibial mid-length, the breadths of the proximal and distal tibia, and the depth of the distal tibia compared with the lengths (Fig. 2: Aa; Ab; Ac; Ad). The intercepts of these measurements in humans were larger than those of the small primates. On the other hand, the LRs of the next longest group, K/FQ, the group consisting of great apes, showed significantly larger slope values than those of the other groups in most comparisons of the tibia (Fig. 2: Ab; Ac; Ad). The exception was the tibial maximum mid-length diameter, which showed the same slopes in all groups (Fig. 2: Aa). On the other hand, the fibular slopes of the Biped and K/FQ groups were significantly different from those of the smaller group in the maximum diameter of the mid-length (Fig. 2: Ba). The K/FQ group showed a significantly large slope in the head diameter compared with the smaller group (Fig. 2: Bb). Because of the very small variety in head diameter, the regression of the Biped group was not significant (Fig. 2: Bb).

Least squares linear regressions (LRs) after transformation to logarithms. Separately calculated LRs of humans (Biped), the great apes (K/FQ), and other small primates (Small). *: p<0.05; **: p<0.01 by Student’s t-test. LRs of the human and great ape groups were separately compared with those of the small primate group, respectively, using analysis of covariance. -: not significant; *: p<0.05; **: p<001 by F-test. When the slopes (b) of two regressions were significantly different, then the intercepts (a) could not be compared (/). A: Tibia. Aa) X: Total length. Y: The maximum mid-length diameter. Ab) X: Total length. Y: Proximal breadth. Ac) X: Total length. Y: Distal breadth. Ad) X: Total length. Y: Distal depth. B: Fibula. Ba) X: Maximum length. Y: Maximum mid-length diameter. Bb) X: Maximum length. Y: Maximum diameter of the head.

4 Discussion

15Among primates, hominoids show a unique locomotor type in each subgroup, namely true brachiation (Brach) by lesser apes, knuckle or fist quadrupedalism and arm-swinging (K/FQ) by great apes, and bipedalism (Biped) by humans. These types of locomotion were not habitually adopted by other monkeys.

16Great apes, who adopt the K/FQ type of locomotion, had uniquely characterized lower leg bones compared with the other groups as follows: the robust fibula, which was thought to imply the presence of well-developed hallucis muscles and the robust shaft size of extant great apes, has been pointed out (Ward, 1998; Marchi, 2007); the large diameters of lower leg bones in gorillas have also been reported (Schultz, 1953; Turley et al. 2011); the relative diameters of the proximal and distal ends and the mid-shaft maximum of the tibia and fibula in the present great apes were larger than those of other types of primates (Fig. 1). One of the reasons for this larger size is the larger body size of the great apes. Humans also showed relatively large diameters (Fig. 1). LRs were calculated between diameters and lengths (Fig. 2). Great apes, the K/FQ group in the figure, usually showed a larger slope than did the small-sized monkeys and gibbons. On the other hand, bipedal humans showed similar slope values in the LRs of the tibial diameters, although with different intercepts. The maximum tibial diameter of the shaft mid-length in the humans and the great apes showed similar slopes in LRs compared with those of small primates. The large diameters of the great apes cannot be explained only from their large body size; they showed different scaling patterns from other primate bones. The long bone lengths of 79 species of quadrupedal mammals, excluding the primate species, were usually allometric to the cube root of the body mass in the log-log standard major axis analysis, except for the tibia length, which showed a slightly negative allometry of 0.300, which was significantly smaller than the geometrical allometry of 1/3 (Kimura, 1994). From the log-log LR analysis, Alexander et al. (1979) showed a nearly geometrical allometry (1/3) to the body mass from six primate samples, including the humans but not the great apes, in the length of the tibia. That study suggested that primate long bone length is allometrically related to body mass, although the sample size was small. Ruff (1987) calculated that the tibial length of primates, consisting of humans, great apes, and macaques, was nearly allometric to the body mass (Fig. 3. The title of Ruff’s Table III could be a mistake for the femora). The great apes in his study showed negative allometry. Although the sample size was again small, the tibial length of great apes could have a different relationship with body mass than other primate species. The lower limbs of bipedal humans support the entire body mass during locomotion. In chimpanzees or orangutans, the hind/forelimb ratio of foot force during knuckle or fist quadrupedal walking is greater than that in small primates (Kimura et al. 1979; Kimura, 1985; Raichlen et al. 2009; Raichlen et al. 2015; Raichlen & Pontzer 2021); thus, the hindlimb dominance of their foot force was strong compared with the small primates. To support the large proportion of body mass, the lower/hindlimb bones of humans and great apes should have relatively larger diameters standardized by the total body mass compared with the small primates, which were not so strongly hindlimb-dominant compared with the above two groups. Large slopes or intercepts in many diameters of humans and great apes compared with those of the small primates could be explained to some extent by their large hindlimb dominance. Compared with humans, however, the uniqueness of great apes was still remarkable.

17The Qgw/bw and Qgw groups showed large relative diameters for many items compared with the As/Qbw and Qsc groups (Fig. 1). The locomotion of the former two groups includes the terrestrial subtrate. In a mechanical study of quadrupedal positional behaviors among quadrupedal mammals, primates were found to have special hindlimb dominance compared with the forelimbs (Iwamoto & Tomita, 1966; Kimura et al. 1979; Kimura, 1985; Demes et al. 1994; Schmitt & Hanna 2004). Among primates, relatively arboreal species exhibited stronger hindlimb dominance than those who utilize the terrestrial environment in their daily activities (Kimura et al. 1979; Kimura, 1985, 1992; Druelle et al. 2019). This hindlimb dominance has been discussed in relation with arboreal life. Marchi (2007) considered that the more arboreal group possessed relatively robust fibulae compared with tibiae. Compared with body mass, however, the humerus, the forelimb bone, of the relatively terrestrial group was more robust than that of the relatively arboreal group (Kimura, 2002, 2003). The large relative diameters compared with the length in the Qgw/bw and Qgw groups in the present lower legs were somewhat different from the above reports. One of the reasons for this could be related to the short hindlimb bones of the relatively terrestrial groups compared with those of the relatively arboreal groups (e.g. Erickson, 1963; Strasser, 1992; Jungers et al. 1998; Kimura, 2003).

18On the other hand, many of the relative diameters of the Vcl group were small compared with the length. This could be because of the long lower legs of leaping animals (Jungers, 1985; Kimura, 2003). This group showed the special characteristic of having a relatively large malleolar breadth compared with depth at both the tibia and fibula (Fig. 1: Ag, Bd). The tibial malleolar breadth compared with the total distal breadth was also large (Fig. 1: Ah). The ankle morphology in this group could be related to the mechanical requirements of strong impacts at the start and end of leaping. In the Qsc group, a relatively large tibial malleolar breadth compared with depth and distal tibial breadth was observed (Fig. 1: Ag, Ah). The morphology of tibial malleolus in this group could be related to the grasping hindlimb during the positional behavior (Walker, 1974; Ishida et al. 1983).

19The tibial malleolar breadth compared with depth was also large in the As/Qbw, and K/FQ groups, who have adopted arm-swinging as part of their repertoires in arboreal environments (Fig. 1: Ag). By contrast, humans showed small relative malleolar breadth compared with both the depth and distal tibial breadth (Fog. 1: Ag, Ah). Bipedal humans have another characteristic of a distal articular surface. The anterior margin of this surface is usually much larger than the posterior margin in other primates, but nearly the same length in humans (Fig. 1: Ai) (DeSilva, 2009; DeSilva & Papakyrikos, 2011). The lower leg bones in humans roll over the talus mainly in the parasagittal direction with small inversion and eversion. Other primate species, especially the relatively arboreal species, have an abducted big toe with large inversion and eversion ankle movements (DeSilva, 2009). Mechanically, a relatively large breadth compared with depth and a relatively large malleolar breadth could aid these ankle movements. The adducted big toe of bipedal humans aligns with other toes in the sagittal direction and pushes off mainly in the sagittal direction on the terrestrial substrate.

20Based on the shape of the lower leg bones, humans and their closest relatives, the great apes, show special characteristics that distinguish them from other monkeys and lesser apes. As discussed above, one of the causes of this specialty could be their large body size, which involves support mainly by the lower/hindlimbs; however, the ankle joints of humans and great apes showed different features. In particular, the transversely extended malleoli were characteristic of great apes, in contrast to the human malleoli (Fig. 1: Ac, Ad, Ag, Bc, Bd). This difference is likely related to the different ankle movements of the two groups in relation to their locomotor types.

Limitations

21The present paper adopted the length of the bone measured to standardize the measurements taken on the same bone. This scaling method was accurate and represented a good alternative to the fact that the body mass of the individual was not always available. Other standards, such as the average body mass calculated from different individuals or the geometric mean/Procrustes analysis of many measurements, also exist. All these methods have inherent limitations as not only the proportions change with size but also the shape and posture. The proportional difference of limbs has partly been discussed in relation to the habitual locomotor behavior of animals (e.g. Erickson, 1963). Therefore, the present results should be carefully analyzed, without going into circular arguments.

22In this study, primate species were grouped by habitual locomotor type. The types used in the present paper were selected to demonstrate large differences among the primate groups; however, at this stage of research, it was impossible to include all detailed locomotor modes of each individual within a locomotor type, i.e. the locomotor repertoires.

5 Conclusion

23Comparisons of lower leg bones were made among 80 extant species of primates according to groups of habitual locomotor types in consideration of arboreal and terrestrial environments. The analyses revealed unique characteristics of the lower leg bones in humans and the great apes. These two primate groups showed many characteristics in different directions, even though they share a phylogenetically close relationship and have a large body size and long lower leg bones among primate species. Two special types of locomotion, knuckle or fist quadrupedalism with strong hindlimb dominance by great apes and bipedalism by humans, were related to numerous characteristics. The differences in ankle movement and abducted halluces may be related to the shape of the distal ends. Some differences in bones, such as many diameters, were also found between primates in the more arboreal vs. more terrestrial environments.

Acknowledgements

24For help with the study materials, I am indebted to G. Suwa, E. Hirasaki, S. Kotera, Y. Nakano, H. Gunji, M. Etoh, N. Shigehara, R.D. Martin, P. Schmid, D. Curtis, W. Wan Neer, D.R. Howlett, and all other present and past staff members. I would like to thank K. Nakamura for assistance with graphics. I thank two anonymous reviewers and F. Druelle for providing useful comments.

Conflict of Interest

25The author declares no competing interests.

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    Ce document est une traduction en français de l'article original rédigé en anglais. Cette traduction a été réalisée par l'INIST CNRS (INstitut de l'Information Scientifique et Technique).

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Table des illustrations

Titre Table 1
Légende Number of materials
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-1.jpg
Fichier image/jpeg, 76k
Titre Table 2
Légende Locomotor type
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-2.jpg
Fichier image/jpeg, 117k
Titre Figure 1A
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-3.jpg
Fichier image/jpeg, 208k
Légende Comparisons of relative bone diameters among different locomotor types. Above: Boxplots of each type. Bottom: Tukey’s multiple comparative procedure. *: p<0.05; **: p<0.01. For the abbreviations of locomotor types, see Table 2 and the text. A: Tibia. Aa) Maximum mid-length diameter x 100 / total length; Ab) Proximal breadth x 100 / total length; Ac) Distal breadth x 100 / total length; Ad) Distal breadth of the two articulated lower leg bones x 100 / tibial total length; Ae) Depth of medial articular surface x 100 / total length; Af) Distal breadth / depth; Ag) Malleolar breadth / depth; Ah) Breadths of malleolus / distal end; Ai) Breadths of distal articular surface margins anterior / posterior.
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-4.jpg
Fichier image/jpeg, 102k
Titre Figure 1B
Légende B: Fibula. Ba) Maximum mid-length diameter x 100 / maximum length; Bb) Maximum diameter of the head x 100 / maximum length; Bc) Malleolar (=distal) breadth x 100 / maximum length; Bd) Malleolar breadth / depth.
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-5.jpg
Fichier image/jpeg, 214k
Titre Figure 2
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-6.jpg
Fichier image/jpeg, 187k
Légende Least squares linear regressions (LRs) after transformation to logarithms. Separately calculated LRs of humans (Biped), the great apes (K/FQ), and other small primates (Small). *: p<0.05; **: p<0.01 by Student’s t-test. LRs of the human and great ape groups were separately compared with those of the small primate group, respectively, using analysis of covariance. -: not significant; *: p<0.05; **: p<001 by F-test. When the slopes (b) of two regressions were significantly different, then the intercepts (a) could not be compared (/). A: Tibia. Aa) X: Total length. Y: The maximum mid-length diameter. Ab) X: Total length. Y: Proximal breadth. Ac) X: Total length. Y: Distal breadth. Ad) X: Total length. Y: Distal depth. B: Fibula. Ba) X: Maximum length. Y: Maximum mid-length diameter. Bb) X: Maximum length. Y: Maximum diameter of the head.
URL http://journals.openedition.org/primatologie/docannexe/image/10570/img-7.jpg
Fichier image/jpeg, 324k
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Tasuku Kimura, « Habitual locomotor types and the shape of lower leg bones in primates, especially in hominoids »Revue de primatologie [En ligne], 12 | 2021, mis en ligne le 24 février 2022, consulté le 18 juin 2024. URL : http://journals.openedition.org/primatologie/10570 ; DOI : https://doi.org/10.4000/primatologie.10570

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Auteur

Tasuku Kimura

The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 181-0033, Japan
Email address: tkimura@um.u-tokyo.ac.jp

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