Hindlimb proportions, allometry, and biomechanics in Old World monkeys (primates, Cercopithecidae).

AMERICAN JOURNAL O F PHYSICAL ANTHROPOLOGY 87:187-213 11992)

Hindlimb Proportions, Allometry, and Biomechanics in Old World Monkeys (Primates, Cercopithecidae) ELIZABETH STRASSER Department of Cell Biology and Anatomy, The John Hopkins University School of Medicine, Baltimore, Maryland 21205

KEY WORDS specializations

Indices, Foot skeleton, Locomotor and substrate

ABSTRACT

The traditional focus on morphological rather than mechanical units has obscured some significant functional differences in the hindlimbs of primates. This paper examines the allometric and biomechanical basis for some distinctive proportional differences among pairs of morphological units in the hindlimb, and especially the foot, of cercopithecid primates. Five major conclusions are reached. First, many hindlimb dimensions scale allometrically with body mass to maintain mechanical similarity within taxonomic and locomotor groups. Therefore, the majority of traditional indices which describe the shape of the foot within cercopithecids reveal differences which are primarily a function of size. Second, the hindlimb segments in colobines, and especially in Presbytis, are relatively long, probably to enhance leaping. Third, the major distinction of terrestrial cercopithecines among the features analysed is reduction in the length of the phalanges, due to the reduced importance of grasping during locomotion and the assumption of digitigrady. Fourth, Theropithecus and male Erythrocebus have high crural indices, relative to their body masses, which can facilitate cursoriality. Female E . patas already has a high crural index as a function of its body mass. Fifth, macaques form a distinctive group among cercopithecines, characterized by relatively short hindlimbs. Relatively very short hindlimbs in Macaca fuscata and M . thibetana suggest that climatic conditions can have an added effect on the lengths of the hindlimb segments. In summary, this analysis of the lengths of the hindlimb segments relative to body size reveals taxonomic differences which are due in part to phylogeny, to differencesin locomotor behavior, and to substrate use.

Since the turn of the century, when Mollison (1910) described the skeletons of a variety of primates, indices have been a popular vehicle for quantifying relative lengths of the postcranial skeletal segments (e.g., Gabis, 1960; Jouffroy and Lessertisseur, 1960, 1976, 1978; Lessertisseur and Jouffroy, 1973; Schultz, 1930, 1963a,b). If it can be established that proportional differences in the skeletal system reflect locomotor differences, it is possible to speculate about the locomotor behavior of animals known only by their skeletal remains, including extinct forms. Many postcranial indices have been documented that distinguish locomotor and/ or taxonomic groups among primates (e.g.,

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1992 WILEY-LISS. INC

Erikson, 1963; Napier and Walker, 1967; Washburn, 1942). However, it is becoming increasingly apparent that in order for indices to be truly useful as taxonomic and locomotor indicators body size must be considered in the interpretation of indices (Aiello, 1981; Biegert and Maurer, 1972; Jungers, 1985; Rollinson and Martin, 1981; Walker, 1974). For several reasons, the primate family Cercopithecidae represents an excellent “natural experiment”with which to examine Received June 20, 1990; accepted July 23, 1991. Elizabeth Strasser’s current address is Department of Anthropology, California State University, Sacramento, Sacramento, CA 95819-6106.

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TABLE 1. Mean values reported for indices by Gabis (1960) and Schultz (1963a,bj (inpurenthesesj Genus

Mucaca Cercocebus P. (Papio) Theropithecus Erythrocebas Cercopithecus Semnopithecus S. (Trachypithecus) Presbytis Nasalis Pyguthrix Colobus

Tibia/ femur

Tarsus/ foot

MtIII/ foot

PhIII/ foot

Power/ load

93 94 91 100 98 97 90 91 93 88 89 93

31 (32) 32 (32) 35 (35) 35 (36) 37 (37) 31 (32) 29 29 29 (30) 29 (29) 29 38 (30)

30 (33) 30 (33) 32 (32) 33 (35) 32 (33) 32 (33) 33 31 31 (32) 30 (32) 30 32 (31)

37 (36) 35 (35) 32 (33) 30 (29) 28 (30) 36 (35) 37 39 38 (38) 38 (39) 38 39 (39)

(22) (23) (25) (25) (23)

the relationship between body size and limb proportions. First, there is little question about the monophyly of the major clades of this family (Strasser and Delson, 1987). Second, these clades differ substantially in the frequency in which they engage in leaping and quadrupedal locomotor behaviors and in their substrate preferences (arboreal vs. terrestrial) (Napier and Napier, 1967; Rose, 1973; Strasser, 1989; see below). Third, there are some well-known proportional differences in the hindlimb skeleton, and especially the foot, in cercopithecids that appear to be related to taxonomy, locomotion, and substrate use (Gabis, 1960; Schultz 1963a,b). However, the effect of size on the distinctive hindlimb proportions among cercopithecids has never been examined. In 1960, Gabis reported some observations on the proportions of the foot that distinguished both taxonomic and locomotor groups among cercopithecids (Table 1). Three years later Schultz (1963a,b) published similar observations on the proportions of the cercopithecid foot (Table 1). Specifically, both authors considered the lengths of the three principal morphological segments of the foot (tarsus, third metatarsal, third digit) a s functions of the total length of the foot. Both Gabis and Schultz drew three conclusions concerning the proportions of the foot: 1)colobines are distinguished from cercopithecines by their relatively short tarsus and relatively long third digit; 2) among cercopithecines, the terrestrial genera (Theropithecus, Papio (Papio), Erythrocebusj can be distinguished from arboreal forms by their relatively very long tarsus and very short third digit; and 3) the relative length of the third metatarsal is invariant in cercopithecids, and can neither separate taxonomic groups nor discriminate

(22) (24) (25)

(22)

between arboreal and terrestrial forms. Gabis also found that the mechanically meaningful crural index (i.e., [tibial length/ femoral length] x 100) did not permit a distinction between arboreal and terrestrial forms; whereas terrestrial Theropithecus and Erythrocebus had high values in the sample for the crural index P. (Papio) had lower values than did colobines and arboreal cercopithecines (Table I). Similarly, Schultz (1963b)found that amongcercopithecids values for the triceps surae's lever-arm index in the foot (i.e., [power-arndload-arm] x 100; see pages 191-192 for definitions of the lever-arms) did not distinguish between arboreal and terrestrial forms or taxonomic groups (Table 1). The taxonomic and locomotor patterns of pedal segment index values are intriguing, but problematic for a number of reasons. First, indices were used by Gabis and Schultz to minimize the effects of absolute body size. Since neither Gabis nor Schultz investigated the size relationship of the index values, it is not known whether the effects of absolute body size were minimized. In addition, indices may be significantly correlated with body size, indicating allometric shape change. Second, the pedal segment ratios of Gabis and Schultz are suspect because the denominator is comprised of the sum of all the numerators. For example, is the tarsus truly short in colobines or is the rest of the foot long? Furthermore, the tarsus itself is made up of several bones. Are all the tarsal bones short in colobines, or only some of the bones, or, indeed, only a portion of one of the bones? Neither Gabis nor Schultz considered these questions. The third reason to reconsider pedal segment indices is that the morphological units that were analysed were either combinations or subdivisions of

HINDLIMBS IN CERCOPITHECIDS

mechanical segments. For instance, the tarsus combines the triceps surae’s power-arm along with part of its load-arm, while foot length combines both the triceps surae’s power- and load-arms along with the loadarm for the digital flexor musculature (i.e., phalangeal length). The three drawbacks outlined above determined the course of this analysis. First, the correlations of indices with body size have to be evaluated. This is necessary to determine whether the index values characteristic of particular locomotor and/or taxonomic groups are functions of their body sizes or reflect “adaptations” to particular habitats and/or locomotor modes. A significant positive correlation between index values and body size indicates positive allometry for the ratios, whereas “isometry”may be indicated by the lack of a significant correlation (Mosimann and James, 1979). Because there is a n obvious relationship in cercopithecines between body size and locomotion (i.e., the larger species are also the more terrestrial) and because the tarsuslfoot and phIII/foot indices were identified by Gabis and Schultz a s distinguishing the large-bodied, terrestrial cercopithecines from arboreal ones, it is necessary to evaluate the correlations of indices with body size in cercopithecine samples which include and exclude the large-bodied terrestrial forms. If the correlations of indices with body size remain significant when terrestrial genera are excluded from the sample, then it is likely that terrestrial forms have their distinctive proportions as a consequence of allometry. Conversely, if the correlation between index values and body size becomes insignificant when terrestrial genera are excluded from the cercopithecine sample, it might be reasonable to consider the differences between arboreal and terrestrial forms a consequence of habitat exploitation and not allometry (i.e., body size). Second, the power relationships of the indices’ numerators and denominators with body size have to be examined to determine the basis for the correlations of the indices with body size. If the numerator has a more positive allometric relationship with body size than does the denominator, the index will have a positive correlation with body size. Conversely, if the numerator has a more negative allometric relationship with body size than does the denominator, the index will have a negative correlation with body size. If the numerator and denominator have the same allometric relationship with

189

body size, then the index will have no correlation with body size. Third, the mechanical basis for the index values and power relationships must be established by considering the relevant physical parameters associated with reported locomotor behaviors and substrate preferences for the taxa under study. To assess the effect of body size on the dimensions of the hindlimb, some model of similarity is necessary. The model of geometric similarity traditionally has been used as the null hypothesis in biomechanical studies to evaluate the proportionate dimensions of the musculoskeletal system in a size-graded series of organisms. A series of different sized organisms are geometrically similar (i.e., isometric) if they are identical in shape. As the linear dimensions in a n organism increase in size, so do its areal dimensions and volume. However, in an isometric series areal dimensions increase a s the square of the ratio of homologous linear dimensions, whereas volumetric dimensions increase a s the cube of the ratio of homologous linear dimensions. Because linear, areal, and volumetric dimensions are increasing a t different rates, the ratio of two dimensions, such as length or area to volume, will not be the same in smaller and larger organisms of a n isometric series: the larger the organism, the smaller the ratio of its different dimensions. If a n organism is to maintain the same function when it is built to a different size, many of its relevant dimensions must change nongeometrically (allometrically) to compensate for the overall size difference (Gould, 1966; Schmidt-Nielsen, 1984). Mechanical equivalency of the musculoskeletal system is dependent upon constant relationships between the dimensions of bones, muscles, and body mass. The maximum tension generated by a muscle is a function of its cross-sectional area, while the torque that a muscle can produce around a joint is a function of its tension and the length of the lever-arms around that joint (Biewener, 1989; Hildebrand, 1988; Smith and Savage, 1956; but see Gans, 1988, for a n alternate view). In a n isometric series of related organisms, the ratio of lever-arms on either side of a joint is the same in small and large animals because lever-arms are linear dimensions, whereas the ratio of muscle cross-sectional area to body mass decreases as body size increases. Thus, a larger animal in a n isometric series will be relatively weaker. If the muscles of a larger animal are to maintain a functional equivalence to those

190

E. STRASSER

of a smaller animal, either the dimensions of the muscles or the ratio of the lever-arms around joints must change. If the relative size of a muscle does not change as a n animal gets bigger or smaller, then in order to maintain the same mechanical advantage, one or both lever-arms around a joint must scale allometrically with body mass in order to compensate for the changing ratio of muscle cross-sectional area and body mass. When no data on muscle mass or crosssectional areas are available for analysis, inferences about the relative size of muscle masses can be based only on the proportions of lever-arms. If the lever-arms of muscles around joints scale positively with body size, and the lever-arms of body weight scale negatively, then it can be tentatively inferred that muscle masses (and their cross-sectional areas) are scaling geometrically with body size. As a consequence, the hypothesis that mechanical equivalency is being maintained would be supported. During the push-off stage of a plantigrade quadrupedal stride or of a leap, the tarsus and metatarsus of the foot are assumed here to function as a second-class lever for the triceps surae, with the fulcrum of the foot a t the third metatarsal head and the load at the talocrural joint. Identifying the fulcrum of the foot a t the metatarsal heads is a reasonable assumption for terrestrial cercopithecids, such as P. (Papio), Erythrocebus, and Theropithecus, in which the hallux is relatively diminutive and not involved during push-off of the foot (Jolly, 1965; Midlo, 1934; Pocock, 1925). This is also a reasonable assumption for arboreal cercopithecids when the ratio of foot width to branch diameter ratio is small, o r when the long axis of the foot is positioned perpendicular to the long axis of the branch, as when preparing to leap across a gap between branches (pers. obs.). However, this assumption may not be reasonable for arboreal cercopithecids which have a high ratio of foot width to branch diameter and which grip the branch between the hallux and lateral digits when progressing along the long axis of a branch. I n this case, the fulcrum of the grasping foot during push-off is probably a t a joint, or a n axis through several joints, proximal to the web between the hallux and lateral digits (Jolly, 1965). Therefore, the lever would not be along the long axis of the foot, terminating at the metatarsal heads. Until more data on foot postures, such as those gathered by Meldrum (19911,are available, we can never be certain of the position of application of the

substrate force and, consequently, of triceps surae’s lever-arm length. Nevertheless, in order to examine the allometric basis for the patterns in index values identified by Gabis and Schultz, the lever-arm of triceps surae is assumed in this study to be along the long axis of the foot in all cercopithecids. MATERIALS AND METHODS

The cercopithecid materials examined in this study are comprised of 574 hindlimb specimens. The specimens represent 48 species distributed over 13 genera (Table 2). The 48 species are somewhat unevenly apportioned to the two major taxonomic groups that constitute the family: 30 species represent Cercopithecinae and 18 species represent Colobinae. The higher-level classification of cercopithecid species used in this study follows Strasser and Delson (1987). Thus, in this paper, Erythrocebus and Miopithecus are generically distinct from Cercopithecus, and (Mandrillus) is considered a subgenus of Papio. The colobine genus Procolobus includes the red (Piliocolobus badius) and olive (Procolobus verus) forms while the genus Colobus includes the blackand-white species. The Asian langurs are distributed among four genera: Presbytis, Semnopithecus [including (Trachypithecus)], Nasalis, and Pygathrix [including (Rhinopithecus)]. The classification of populations into species follows Fooden (1969) for the Sulawesian macaques and Napier (1981, 1985) for all others. Measurements were collected primarily from wild-caught specimens for which provenance data were available (Strasser, 1989). The majority of specimens for most of the species in this study are from large series taken from one or several locations in the wild. However, for seven species, specimens for which there were no locality data were included. In the cases of M . talapoin, E . patas, and P. (Papio) cynocephalus, the specimens either had field numbers which, given their sequence, suggested that they were from the wild, or they were a part of the Kenya National Museums osteology collection and were presumably wild-caught. A specimen of C. vellerosus was from a zoo in Sierra Leone, which suggests that the specimen was of local origin. In the case of most of the specimens of M . sylvana and all of the specimens of M. fuscata, the provenance data were either vague (e.g., Barbary, J a pan) or nonexistent, but these species would not have been represented in this study if these specimens had not been used. Finally,

191


TABLE 2. Skeletal sample used in study’ Species Erythrocebus patas Cercopithecus albogularis Cercopithecus mitis Cercopithecus nictitans Cercopithecus pygerythrus Cercopithecus petaurista Cercopithecus cephus Cercopithecus ascanius Cercopithecus campbelli Cercopithecus mona Cercopithecus pogonias Miopithecus talapoin Macaca arctoides Macaca thibetana Macaca syluana Macaca nemestrina Macaca nigra Macaca fuscata Macaca mulatta Macaca fascicularis Cercocebus torquatus Cercocebus galeritus Cercocebus albigena Papio ursinus Papio anubis Papio cynocephalus Papio hamadryas P. (Mandrillus) sphinx P. (Mandrillus) leucophaeus Theropithecus gelada

M 4 9

8 14 15 1

15 10 2 10 13 4 2 4 4 6

3 3 10 10 11 8 14 4 15 11 5 3 2 4

F

T

Species

2 10 12 5 12 4 4 10 2 2

6 19 20 19 21 5 19 20 4 12 18 11 2 4 5 12 4 3 20 20 18 12 24 8 19 19 7 8 4

Nasalis laruatus Pygathrix nemaeus P. (Rhinopithecus)roxellana Semnopithecus entellus S. (Trachypithecus)obscura S. (Trachypithecus)cristata Presbytis frontata Presbytis melalophos Presbytis aygula Presbytis rubicunda Presbytis hosei Colobus guereza Colobus angolensis Colobus polykomos Colobus uellerosus Colobus satana Procolobus uerus P. (Piliocolobus) badius

5 7 0 0 1 6 1 0 10 10

7 4 10 4 4 8 2 5 2 1 ~

M 8

5 1 2 8 12 2 4 3 11 2 16 2 2 2 2 6 14

F

T

5 3 6 6 7 13 2 4 3 11 2 14 4 2 0 1 3 12

13 8

7 8 15 25 4 8 6 22 4 30 6 4 2 3 9 26

5

‘M, males; F, females; T. total

the complete M . mulatta sample is from the collection of Dr. A. Schultz. While there were no provenance data associated with the specimens, they formed part of the basis for Dr. Schultz’s extensive studies and were therefore used in this one. All individuals analyzed in this study were considered adults a s judged by the epiphyseal fusion of the leg bones, calcaneus, and metatarsals and by the complete eruption of the third molars. The sex of specimens was taken from the collection labels and corroborated by examining the skins and the size of the canines. Nine linear measurements taken on disarticulated specimens form the basis for this analysis (Fig. 1). The measurements were designed to approximate those taken by Gabis (1960) and Schultz (1963a,b). All foot measurements were taken using a n electronic digital caliper (Fowler Max-Cal) attached to a portable computer (Compaq or NEC PC-8201A). Long bone lengths were taken using a ruler fashioned to act a s a n osteometric board. All caliper measurements were taken to the nearest 0.1 mm while the ruler measurements were taken to the nearest 1.0 mm.

Given the assumption that the foot is acting as a second-class lever for triceps surae, the lever-arm of triceps surae (power-arm) includes the lever-arm of body weight (loadarm). In order to simplify the analysis, and to determine how the individual bones (or their parts) are scaling with body size, the powerarm is defined here as extending from the insertion of triceps surae to the level of the talo-crural joint. This definition of the power-arm excludes the load-arm which extends from the level of the talo-crural joint to the head of the third metatarsal. The original measurements were used to construct five derived measurements: foot length, tarsal length, pedal power-arm length, calcaneal load-arm length, and pedal load-arm length (Table 3).The derived measurements differ from those used by Gabis, which were based on specimens in which the articulated tarsus was separated from the metatarsus and phalanges. The derived measurements in this study also differ from Schultz’s measurements, which were taken on completely articulated specimens and were either direct or projected lengths. Furthermore, both Gabis and Schultz included the lengths of the middle and distal phalan-

192

E. STRASSER

B

Fig. 1. Illustration of measurements. A Left femur, anterior view, proximal top, medial left. F1, bicondylar length. B: Left tibia, anterior view, proximal top, medial left. T1, maximum length. C: Left articulated pedal skeleton, dorsal view, proximal top, medial left. Cul, maximum length cuboid taken on medial side of isolated bone; Mtl, length third metatarsal taken on isolated bone between mid-points of articular surfaces; Phl, length third proximal phalanx taken on isolated bone between mid-points of articular surfaces. D: Left calca-

TABLE 3. Derived linear measurements calculated from dimensions illustrated in Figure 1

neus, dorsal view, proximal top, medial left. C1, total length taken between tendo calcaneus sulcus and deepest point of articular surface for cuboid; C2, length proximal calcaneus taken between tendo calcaneus sulcus and distal edge of proximal talar facet; C3, length proximal talar facet taken between proximal and distal edges; C4,length distal calcaneus taken between proximal edge of proximal talar facet and deepest point of articular surface for cuboid.

volume which is, theoretically, the independent variable in most allometric models (Schmidt-Nielsen, 1984), and values for this C 1 + Cul + M t l + P h l Foot length Tarsal length c1+Cul dimension are widely available in the literaC2 - (0.5 X C3) Pedal power-arm ture. Estimates of average body mass were length calculated for each sex of each species. TaCalcaneal load-arm C4 - (0.5 X ‘23) ble 4 presents sex by species body mass length Pedal load-arm length (C4 - (0.5 X C3)) + Cul + Mtl estimates for cercopithecids taken from the literature and specimen labels. Body mass estimates were calculated for each sex by taking a weighted mean of the reported estiges in their study while these were excluded mates, using the sample size reported for in this study, because they are difficult to each datum a s the weighting criterion. If no identify in disarticulated specimens and sample size was reported for a datum, a were frequently missing. The original and sample size of one was assumed. All statistical procedures were carried out derived measurements were used to construct the five indices reported by Gabis and using the statistical package SYSTAT for Schultz. Only the measurements used in the personal computers (Wilkinson, 1988). The crural index are identical to those analysed level of analysis is subfamilial following Gaby Gabis. The indices in which the total bis and Schultz. Mean sex by species values length of the foot is the denominator are are used a s the variates because body mass referred to here as pedal segment indices, to estimates are available only a t this level. distinguish them a s a group from the power1 The mean, one standard deviation, and samload index. ple sizes for each sex by species measureData on body mass were obtained in order ment are presented in the Appendix. Also to examine the effect of body size on the following Gabis and Schultz, Theropithecus, proportions of bones. Body mass is a particu- Papio (Papioj, and Erythrocebus are identilarly useful estimator of body size for two fied here a s “terrestrial” genera, although it reasons: it is approximately proportional to is realized that Cercopithecus pygerythrus

193


also engages in significant amounts of terrestrial locomotion. Among colobines, Semnopithecus entellus and possibly P. (Rhinopithecus) roxellanae are also large bodied and engage in significant amounts of terrestrial locomotion. Unfortunately, the specimens sampled in this study for these taxa had no phalanges, so that the effect of terrestriality on their phalangeal proportions in particular could not be examined. The Pearson product-moment correlations between the natural logs of index values and body mass were calculated for samples including and excluding terrestrial genera for cercopithecines and for all colobines. The strengths of the correlations were evaluated by the magnitude of the probabilities associated with the correlation matrix. The Bonferroni criterion was used to adjust the error rate of the probabilities for multiple comparisons (Alt, 1982; Miller, 1985; Wilkinson, 1988).Following Rollinson and Martin (1981), bivariate plots of index values against body mass were constructed for illustrative purposes. Linear regression was used to determine the effect of body mass on the values of the measurements constituting the indices. Regression equations were calculated for both subfamilies using the natural logs of the variable means. Regression coefficients were estimated using both least squares (LS) and reduced major axis (RMA)methods. The arguments for using these methods are given full treatment by Hofman (1988),Kuhry and Marcus (19771, Rayner (1985), and Sokal and Rohlf (1981). The subfamilial LS exponents were tested for homogeneity of the slopes using analysis of variance and for significance of their differences from the predicted geometric similarity exponent using a t-test. The LS subfamilial adjusted group means were tested for homogeneity using analysis of covariance (ancova). The subfamilial RMA exponents were tested for homogeneity and their difference from the predicted geometric similarity exponent using the tests given by Clark (1980) and Hofman (1988). A 0.01 significance level was used for accepting a type I error for all the statistical analyses. Residual values for the variates of each subfamily from their respective subfamilial LS lines were also calculated. The residual values were standardized in order to identify which variates, if any, fell outside of the 95% confidence interval of the subfamilial lines. Because 92 sex by species variates typically constitute the samples used in the anal-

ysis, and because the values of the majority of the coefficients of correlation and determination were high, most scattergrams of the variates feature dense clouds of overlapping points. This density precludes calling out the species names of the variates in each scattergram. However, points representing variates which lie outside of the 95% confidence belt around each subfamilial slope are identified on the scattergrams. Principal components analysis (PCA) was performed on the correlation matrix of natural log transformed mean sex by species values of seven original and derived dimensions (lengths of the femur, tibia, pedal power-arm, calcaneal load-arm, cuboid, third metatarsal, and third phalanx). PCA was used because it was not necessary to taxonomically classify variates prior to the analysis, as was done for the regression analyses. Therefore, PCA served t o assess the discriminatory ability of all the measurements simultaneously. Bookstein et al. (1985) present compelling reasons for performing a PCA of morphometric data on a covariance, rather than a correlation, matrix. Both types of matrices were used in this study but only the results for the correlation matrix are presented. Whereas the actual values for the eigenvalues and component loadings differed for the PCA of the two matrices, the percentages of total variance explained by the components were the same, a s were the general ordination of variables and bivariate plots of variates along the components. As a consequence, there was no difference in interpretation based on a PCA of either matrix. RESULTS

Correlation of indices with mass Table 5 and Figure 2 show the correlations of indices with body mass for the two subfamilies. The magnitude of the probabilities of the correlations differs between the two subfamilies. For the sample including all cercopithecine variates, four indices are significantly correlated with body mass, while the correlation of the mtIII/foot index with body mass is weak. When the terrestrial genera are removed from the cercopithecine sample, the mtIII/foot index becomes significantly correlated with body mass while the correlation of the phIIUfoot index with body mass becomes insignificant. In colobines only the powerfload index is significantly correlated with body mass. While the majority of the colobine correlations of indices with body mass are not significant, they nevertheless

194

E. STRASSER

TABLE 4. Body mass estimates, i n grams Taxon Erythrocebus patas

Cercopithecus albogularis Cercopithecus mitis Cercopithecus nictitans Cercopithecus pygerythrus Cercopithecus petaurista

Source'

Males2 7,000 11,100 10,000 8,180 8,865 8,655 7,350 8,634 6,500 5,150 7,491 4,582 5,330 3,820

(11 [3] [8] [4] [12] [3] [4] [l] [17] [2]

[5]

Cercopithecus cephus Cercopithecus ascanius Cercopithecus campbelli Cercopithecus mona

Cercopithecus pogonias Miopithecus talapoin Macaca arctoides Macaca thibetana Macaca sylvana Macaca nemestrina

Macaca nigra Macaca fuscata Macaca mulatta Macaca fascicularis Cercocebus torquatus Cercocebus galeritus Cercocebus albigena Papio ursinus Papio anubis

Papio cynocephalus Papio hamadryas

P. (Mandrillus) sphinx P. (Mandrillus) leucophaeus

Mean3

5,000 4,630 [l] 4,500 4,600 [l] 1,380 [7] 10,200 [l] 15,000 [6] 9,300 [2] 11,200 9,753 [a] 10,400 9,988 5,954 10,400 7,990 15,400 11,700 7,712 7,221 6,199 4,930 4,162 10,750 11,413 17,706 10,200 7,311 6,346 31,752 28,602 26,880 28,414 27,700 27,612 24,400 22,979 22,926 19,509 19,660 17,827 26,900 20,750 20.000

[l] [l] [3] [3] [8] [6] [3] [6] [3] [l] [4] [I] 141 [4] [2] [I] [2] [4] [4] [8] [ll] [4] [5] [5] [5] [l]

Mean3 5,300

5,765

5,900 5,600 4,400 [l] 4,446 [lo] 9,194 [l] 4,231 [14] 4,317 [5] 4,000

4,661

3,257 [15]

3,257

3,820

3,020 [5] 3,158 [2] 2,880

3,059

3,300 [2] 2,200 [2]

3,300 2,200 3,067

8,795 7,607

4,000 4,000 4,212 [6] 4,300 [5] 3,8504[3] 6,300

Females'

8.773

4,212 4,300 4,580

4,878 4,254 4,000

2,880

2,700 2,500 [l] 4,000 4,550 1,380 10,200 15,000 9,933 9,974

3,000 3,000 [I] 1,120 191

3,000

9,333 [3] 10,000 4,649 [l] 7,000 7,800 5,826 [3]

9,500

8,065

1,120

6,155

5,168 6,600 4,690 [3]

14,475 7,502

5,367 [9]

5,367

5,055

4,536 [3] 3,130 [6] 3,178 [6]

3,430

12,351

6,333 6,333 [3]

10,200 6,829

5,500 5,671 [3] 4,915 [2]

29,173 26,435

22,950 19,585

14,525 14,755 [I] 14,410 [2] 14,744 [2] 17,900 [I] 17,619 [3] 12,800 [30] 11,680 [2] 12,114 [6] 10,225 121 9,817 [3]

21,153

[6]

5,500 5,369

13,451

12,006 9,980 11,500

11,500 [2] 18,500

10,000

(Continued)

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TABLE 4. Body mass estimates, i n gram (continued) Taxon

Theropithecus gelada Nasalis laruatus

Pygathrix nemaeus P. (Rhinopithecus) roxellana Semnopithecus entellus

S. (Trachypithecus) obscura

S. (Trachypithecus) cristata Presbytis frontata Presbytis melalophos Presbytis aygula Presbytus rubicunda

Presbytis hosei Colobus guereza

Colobus angolensis Colobus polykomos

Colobus vellerosus Colobus satana

Procolobus uerus P. (Piliocolodus) badius

Source'

Males' 17,000 19,000 21,000 16,500 20,370 21,392 15,475 20,300 10,900 10,752 10,896 18,300

18,833

[l] 18,814 [4] [4] [a] [2] [3]

12,748 [19] 18,400 7,319 [12] 7,945 [4] 8,300 7,578 [2] 6,930 [6] 6,421 [7] 8,600 5,570 5,488 [l] 6,478 [25] 6,700 6,685 [2] 6,680 6,683 [3] 6,300 6,190 6,339 6,588 [ll] 5,707 [7] 6,300 6,200 9,327 9,750 11,800 10,800 9,679 10,700 9,800 8,420 8,000 10,400 9,900 8,500 10,000 12,000 10,500 4,280 4,476 3,800 9,348 10.500

Mean3

[8] [l]

Females' 10,000 11,700 14,000 13,800 [l] 9,820 8,363 [3]

Mean3 13,167 8,962

10,839

9,900 8,200 8,064 [l]

8,132

18,300

9,000 [4]

9,000

13,031

9,515

7,530

9,421 [20] 11,400 6,602 [22]

6,723

6,795

7,353 [5] 6,500 6,595 [2] 5,950 [6]

5,984

5,505 [4] 8,100 5,600

5,529 6,501 6,606 6,250

6,200 10,237

5,600 [8] 6,318 [27] 6,600 6,877 [3] 6,671 6,664 141 6,200 5,680 6,056 6,683 [9] 5,999 [7] 6,300 5,570 5,562 [l] 7,826 [12]

6,381 6,588 6,325

5,566 7,936

9,250 [Ill [2] [2] [5] [l] [4] [3] [lJ [4]

9,932

7,403 [5] 9,000

7,669

9,100

7,133 [6] 9,700 [l] 8,400

7,612

9,000 9,500

9,250

4,200 [I] 3,742 [4] 3,600 [5] 6,770 171 5,800

3,717

8,500 10,833 4,131

[5] [7] [7]

9,492

6,649

'Sources: (a) Napier, 1981,1985; (b) Jungers, 1985; (c) Fleagle, 1988 (d) Clutton-Brock & Harvey, 1977;(e)Rowell, 1985; (f) specimen labels; (g) Smithsonian Institution Catalogue; (h) Fooden, 1988 (i) Fooden, 1971;6)Booth, 1957;(k)Takeshita, 1962,in Hill, 1966; (1)Harvey et al., 1987;(m) Hill, 1966,1974;(n) Smuts, 1985;(0)Fleagle, 1977a; (p) Oates andTrocco, 1983; (4)Hill, 1970;(r) Hurov, 1987;(6)Tenazaet al., 1988. 2Nurnbers in brackets is reported sample size. 3Mean body mass weighted by reported sample size. 4Median value.

196

E. STRASSER

TABLE 5. Correlation of In indices with In body mass’ Index Tibia/femur Power/load Tarsus/foot MtIIVfoot PhIIVfoot

All cercopithecines R P -0.720 0.878 0.752 -0.424 -0.547

0.001 0.001 0.001 0.026 0.001

No terrestrial genera R P -0.770 0.869 0.689 -0.607 -0.144

0.001 0.001 0.001 0.001 1.000

Colobines

R

P

-0.391 0.614 0.560 -0.452 -0.060

0.539 0.006 0.024 0.207 1.000

IR, Pearson correlation coefficient; P, Bonferroni-adjusted probabilities.

have the same sign a s do those of cercopithecines, indicating similar bivariate relationships. The crural index is negatively correlated with body mass (all cercopithecines: R = -0.720, P < 0.001;colobines: R = -0.391, P < 0.539),suggesting allometry. There is a slight difference between the subfamilies with regard to their values for the crural index a t comparable body masses (Fig. 2A). On average, colobines have lower values for the crural index than do cercopithecines of comparable body mass. Furthermore, both sexes of Theropithecus gelada and male Erythrocebuspatas have very high values for this index given their body masses. The powernoad index has a strong positive correlation with body mass in cercopithecines (all genera: R = 0.878,P < 0.001)and a weaker one in colobines (R = 0.614,P < 0.006),suggesting allometry. In contrast to the crural index, there does appear to be a strong difference between the subfamilies in their values for the powerAoad index at comparable body masses. Most colobines have a lower value for the index than do the cercopithecines a t comparable body masses (Fig. 2B). The pedal segment indices present divergent patterns of correlation with body mass in both subfamilies (Table 5 ) .The tarsudfoot index has a positive correlation with body mass (all cercopithecines: R = 0.752,P < 0.001;without terrestrial genera: R = 0.689, P < 0.001;colobines: R = 0.560, P < 0.024), whether terrestrial genera are included in the cercopithecine sample or not, suggesting allometry. The mtIII/foot index has a statistically non-significant weak negative correlation with body mass in both subfamilies (all cercopithecines: R = -0.424, P < 0.026; colobines: R = -0.452, P < 0.207). However, examination of Figure 2D suggests that the cercopithecine correlation coefficient is low because of the effect of the outliers Theropithecus and M . thibetana. When the outliers are removed from the cercopithecine

sample the correlation coefficient increases in value and significance (R = -0.574, P < 0.001), suggesting allometry. The phIII/ foot index has a negative correlation with body mass among all cercopithecines (R = -0.547,P < 0.001)and no correlation among colobines (R = -0.060, P < 1.000). When the terrestrial genera are removed from the cercopithecine sample, the correlation is minimal and non-significant (R = -0.144,P < 1.000). The bivariate plots of the three pedal segment indices and body mass illustrate the subfamilial differences noted by Gabis and Schultz. At comparable body masses, colobines have lower values than do cercopithecines for the tarsudfoot index (Fig. 2C). Colobines also have higher values than do cercopithecines for the phIII/foot index (Fig. 2E). Furthermore, these data confirm Gabis’s and Schultz’s observation that the terrestrial cercopithecines (P. (Papio),Theropithecus, and Erythrocebus) have lower values for the phIII/foot index than do arboreal cercopithecines. These data also confirm the observations of Gabis and Schultz that there is little difference between the subfamilies for specific values of the mtIII/foot index (Fig. 2D). However, it is noteworthy that both sexes of T. gelada and most variates of Presbytis have high values, given their body masses, for the mtIII/foot index while Macaca thibetana has a very low value for its body mass.

Scaling of index components Plots of the regressions of the eleven original and derived dimensions against body mass are shown in Figure 3A-L. Regression coefficients and relevant statistics are presented in Table 6. For the regressions of all eleven variables there is never a significant difference between the subfamilial LS or RMA slopes. This is undoubtedly due, in part, to the large values for the standard errors of the slopes in colobines. These large values, in turn, lead to wide confidence inter-

197


0

Cercopitheanes

M. thlbetana

A = -0.424 L

9.5

8.5

7.5

1

7.5

In body mass

-

85

In body mass

9.5

3.3-

Colobines R = 0.614 P < 0.006 Cercopithednes R = 0.878

3.2-

0

Z

'

x

3.1-

8

5

1

0

4.40 6.5

B

P r 0.026

1

PC

0.001

3.0-

L

5 PP-C

n

,

2.9I v

- 2.8E

0

0 2.7'

L _ I

6.5

7.5

8.5

In body mass

9.5

10.5

6.5

7.5

8.5

In body mass

9.5

C 0

0 Cercopithednes

x ij

-.

0 00

R = 0.752 P < 0.001

3.65

0

DI

E 3.55-

2

-

I Y

0

C

3.45' 65

7.5

.

8.5

9.5

10.5

In body mass

vals around the colobine slopes, which generally include the estimated cercopithecine LS or RMA slopes. In seven of the eleven LS regressions, the colobine slopes are also found to fall within, or at the limit of, the 95% confidence intervals around the cercopithecine slopes. However, this is not the case for the RMA estimates, in which only three of the eleven colobine slopes fall within the 95% confidence intervals around the cercopithe-

Fig. 2. Bivariate plots of sex by species mean values for I n indices against I n mean body mass. Measurements used to calculate indices are defined in Fig. 1and Table 3 and body mass values for sex by pecies variates are given in Table 4.Inset in each plot gives Pearson's correlation coefficient (R) and associated Bonferroni probability value (P)for strength of subfamilial bivariate relationships.

cine slopes. Whatever the underlying reason for the lack of a significant difference between the subfamilial slopes, it is important that there are no demonstrable differences in slope, since that assumption must be satisfied before the ancova of the LS estimates can be performed. Visual examination of the distribution of cercopithecine variates in the bivariate plot of the length of the third phalanx with body

198

E. STRASSER

D E

t ?

2.9

-m

z -c

. . . . . . . . . . . . . . . . . . . .

1.9'

7.5

6.5

85

95

1

In body mass

32

d"

5.4

y

-

5.2-

= 3 057 +

0.238~

R = 0.777

30

0 Cercopithecines y = 2.678+ 0.274X

R

= 0.922

28

50-

26

In body mass

.."

F

30 28

5m

-c -m

26

;

34-

24

30 2 8 1 ,/ 65

, 75

,

,

,

,

,

85

In body mass

,

95

I

10 5

-C

22

zoip .4

65

75

8 5

In body mass

95

10 5

199


I

I

Colobines

J

52

5.0

sm E

c

......M.

3 6 k

-m I

thibetana

0

c

E

-c

34

4.8

4.4y

4.6

M. fuacata

4.2

3 . 2 ' . 6.5

. .

. , . 7.5

. . . ,

.

. .

8.5

. , 9.5

. . .

. I 10 5

-

40 6.5

In body mass

75

9.5

8.5

In body mass

3.8

K

3.6

sw

3.4

-m -m

3.2

f

c

3.0

-c

28

2.6 6.5

7.5

8.5

9.5

1

5

303 65

. . . .

,

. . . . , . .

75

. . , .

85

.

,

,

95

In body mass

In body mass

=t/ 3.8

65

75

65

95

10 5

In body mass

Fig. 3. Bivariate plots of linear regressions. Sex by species I n mean values for linear dimensions are defined in Fig. 1 and Table 3 and I n mean body mass estimates are given in Table 4.Dashed line, colobine least squares regression line; solid line, cercopithecine least squares regression line. Variates called out by dotted lines fall outside of 9 5 4 confidence limits for their subfamilial

65

75

8 5

95

10 5

In body mass

least squares line. Upper left inset in each bivariate plot gives regression equation and Pearson's correlation coefficient (R) for each subfamily. Lower right inset gives significance (PI of F values from analysis of variance of subfamilial slopes and from analysis of covariance of subfamilial adjusted group means.

N

LS slope SE

0.267 0.403 0.747 0.722 0.187 0.253 0.472 0.176 0.881 0.825 0.546 0.861

2.678 3.057 0.642 0.558 -0.651 -0.567 0.561 0.269 -0.165 -0.553 1.728 2.058 1.530 1.081 0.866 1.081 2.458 2.474 1.009 0.842 2.084 2.193

0.922 0.777 0.968 0.908 0.965 0.866 0.968 0.893 0.955 0.891 0.933 0.762 0.813 0.852 0.938 0.852 0.953 0.865 0.968 0.917 0.956 0.858

0.242-0.306 0.168-0.308 0.300-0.344 0.277-0.387 0.357-0.413 0.296-0.446 0.234-0.270 0.236-0.338 0.279-0.331 0.282-0.408 0.218-0.270 0.153-0.283 0.152-0.228 0.201-0.329 0.239-0.303 0.201-0.329 0.238-0.286 0.208-0.332 0.295-0.339 0.284-0.386 0.235-0.279 0.198-0.304

Pr>F slope

2.353 2.855

Y-int

0.942 0.813

R

0.280-0.340 0.203-0.341

95% CL

0.001

0.872

0.001

0.001

0.001

0.001

0.101

0.078

0.005

0.622

0.001

0.001

Pr>F means

0.769

0.372-0.428 0.359-0.511

~

0.248-0.291 0.244-0.351

0.306-0.350 0.317-0.421

0.327 0.365 0.269** 0.293

0.252-0.300 0.256-0.380

0.258-0.324 0.253-0.382

0.198-0.276 0.253-0.382

0.237-0.288 0.228-0.359

0.295-0.346 0.330-0.454

0.877

1.435

1.222

0.650

2.230

0.742

2.204

2.504

1.193

0.311-0.356 0.315-0.424

0.243-0.279 0.274-0.377

0.250

0.082

Tlz

0.268-0.330 0.245-0.384

0.308-0.370 0.273-0.411

95% CL

0.275** 0.312

0.289 0.311

0.234** 0.311

0.262** 0.286

0.319 0.387

0.260** 0.321

0.399** 0.428*

0.333 0.266

0.297 0.306

0.338 0.335

RMA slope

33.6

33.9

28.3

30.0

36.3

34.5

34.7

32.9

32.6

33.5

34.3

34.2

DF

ns

ns

ns

ns

ns

ns

ns

ns

ns

ns

ns

ns

Pr Fslope, probability value for test of homogeneity of subfamilial slopes; Pr > F means, probability value for test of homogeneity of subfamilial adjusted group means; RMA slope, reduced major axis slope: TC2,t value for homogeneity of RMA slopes; DF, degrees of freedom for t-test; Pr < Tu, probability of smaller t value. *Slope significantly different from geometric similarity at a = 0.01. **Slope significantly different from geometric Similarity at a = 0.001.

Femur Cercopithecines 57 0.015 0.318 Colobines 35 0.034 0.272 Tibia Cercopithecines 57 0.016 0.274** 0.034 0.238* Colobines 34 Calcaneus Cercopithecines 57 0.011 0.322 0.027 0.332 Colobines 35 Pedal power arm 0.014 0.385** Cercopithecines 57 0.371 Colobines 35 0.037 Calcaneal load arm Cercopithecines 57 0.009 0.252** Colobines 35 0.287 0.025 Cuboid Cercopithecines 57 0.305 0.013 0.345 0.031 Colobines 35 Metatarsal 111 0.244** 0.013 Cercopithecines 57 0.218** 0.032 Colobines 35 Phalanx I11 0.190** Cercopithecines 52 0.019 0.265 0.031 Colobines 29 Phalanx 111 (without terrestrial genera) Cercopithecines 40 0.271** 0.016 Colobines 29 0.265 0.031 Foot Cercopithecines 52 0.262** 0.012 Colobines 29 0.270 0.030 Tarsus Cercopithecines 57 0.317 0.011 Colobines 35 0.335 0.025 Pedal load arm 57 0.257** 0.011 Cercopithecines 0.026 Colobines 35 0.251*

Variable taxon

TABLE 6. Coefficients a n d associated statistics for regressions of variables against body mass1


mass (Fig. 3H) suggests that the great disparity in the slopes of the subfamilial lines, albeit not statistically significant, is probably due to the effect of the values for phalangeal length in the large-bodied terrestrial forms. Therefore, a second set of estimates of the slope for this relationship was calculated for cercopithecines with the Theropithecus, P. (Papio), and Erythrocebus variates removed (Fig. 31).The new exponents are practically identical to those of colobines, confirming the impression that the rotation of the original cercopithecine line was due to the effect of the terrestrial forms (Table 6). Thus, relative to the subfamilial line based on arboreal species, the highly terrestrial cercopithecines fall well below predicted values for arboreal species of their body size. By its definition, the RMA slope is always higher than the LS slope unless the correlation is 1.0. Therefore, it is of interest to see whether the two regression methods produce exponents that require different biological interpretations. Of the twenty-two pairs of LS and RMA slopes, seventeen pairs show no difference in the significance values of the t-tests which examine the similarity of the observed slopes to the expected isometric value. However, the exponents for six pairs are different enough that t-tests produce conflicting results. Close examination of the relevant exponents in Table 6 suggests that while the difference in values for the exponents may produce statistically different results, no regression coefficient changes so dramatically that a negative allometric relationship becomes positive or vice versa. Indeed, for those variables with a negative LS exponent, the higher RMA exponent is nevertheless below the predicted isometric value. As a consequence, the biological interpretation remains the same,whichevermethod is used. Given the discussion above, it seems reasonable to interpret the various exponents a s indicating that the lengths of the femur, calcaneus, cuboid, and tarsus are isometric with body mass, that the lengths of the tibia, calcaneal load-arm, third metatarsal, third proximal phalanx, foot, and pedal load-arm are negatively allometric with body mass, and that the length of the pedal power-arm is positively allometric with body mass. The ancovas reveal that for six of the eleven variables there is a significant (a = 0.001) difference between the subfamilies in the elevation of their regression lines, with the colobine lines falling above the cercopithecine (Table 6). In other words, a t compara-

201

ble body masses the average colobine has a greater value for the six variables than does the average cercopithecine. The six variables are the lengths of the femur, tibia, third metatarsal, third phalanx, foot, and pedal load-arm (Fig. 3A-B, G-J, L). The colobine regression line for the length of the pedal power-arm falls below the cercopithecine line, indicating shorter pedal power-arms a t comparable body masses to cercopithecines (Fig. 3D). The remaining four variables, which do not show a significant difference, are also measurements of tarsal bones (Fig. 3C, E-F, K).

Principal components analysis The first principal component accounts for approximately 90% of the variance in the sample, the second principal component accounts for approximately 8%of the variance, and the third principal component accounts for approximately 2%. Table 7 presents the loadings of variables and eigenvalues for the first three principal components. Figure 4 illustrates the distribution of variates in spaces defined by combinations of the principal components. With the exception of the third phalanx, the variables have high loadings on the first principal component. The first principal component is commonly interpreted in biological studies as accounting for size (Blackith and Reyment, 1971) and that is the interpretation accorded it here. That size should explain 90% of the variance is not uncommon in PCA (Blackith and Reyment, 19711. This interpretation is further justified here by the strength of the correlation between the first principal component scores and In body mass (R = 0.94, P < 0.001). The spread of variates along the axis of the first principal component in Figure 4A, B clearly justifies interpreting the first principal component as accounting for size: Midpithecus lies a t the bottom of the plots, widely separated from other variates, while the P. (Papio) species, male P. (Mandrillus) leucophaeus, and male Nasalis are found at the top of the plots. The length of the third phalanx has the highest loading coefficient on the second principal component, and is taken as the most important variable for segregating variates. Cercopithecids are spread along the axis of the second principal component, reflecting differences in the length of their proximal phalanges (Fig. 4A, C). Genera with short phalanges (Theropithecus, P. (Papio), Erythrocebus) lie a t the negative ex-

202

E. STRASSER

TABLE 7. Loadings o f variables for first three principal components (PCI-3) Variable

PC1

PC2

PC3

Femoral length Tibia1 length Calcaneal load-arm length Metatarsal I11 length Pedal power-arm length Cuboidal length Phalangeal I11 length Eigenvalues

0.988 0.983 0.976 0.974 0.948 0.937 0.801 6.262

0.053 0.016 -0.120 0.130 -0.282 -0.291 0.573 0.532

-0.092 -0.166 0.100 -0.141 0.042 0.138 0.155 0.110

-3 O\..

0 .-.---hM. talapoln 4

-3

treme of the spectrum, whereas colobines, with long phalanges, lie a t the positive end. Between these two extremes fall the remaining cercopithecines. The loadings of the third component are more difficult to interpret. While the amount of variance explained by the third principal component is very small, it is nevertheless significant, as indicated by the separation of taxa in Figure 4B, C. The loadings of the lengths of the third metatarsal, femur, and tibia are taken as the most important for segregating variates along the third component. While the spread of taxa along the third principal component is not as marked as i t is along the axis of the second principal component, the spread is nevertheless significant. Among the short-toed cercopithecines, Theropithecus gelada lies a t the extreme negative end of the axis because of its relatively long limb bones. The more arboreal cercopithecines are also spread along the third principal component. Macaca thibetana lies a t the extreme positive end of the third principal component because it has a n extremely short third metatarsal and long bones. The remaining macaques lie to the right of the cercopithecine genera Cercocebus, P. (Mandrillus), Cercopithecus, and Miopithecus. As with M . thibetana, but to a lesser degree, these macaques have shorter hindlimbs than do other arboreal cercopithecines. Finally, the Presbytis variates are separated from the remaining colobines. This is because Presbytis species have longer femora, tibiae, and third metatarsals than do other colobines. DISCUSSION

Allometric basis and mechanical interpretations for index patterns The correlations of hindlimb indices with body mass show clearly that, with the exception of the phIIVfoot index, the values of the

-2

1

0

2

1

prlnclpal component 2

B

'1

T. gelada

,"A

A.

....

/'

M. thibetana

%

00

0

a

'...... *.= M. talapoin

0-

-3

1

1

3

prlnclpal component 3

P

'1

-I 4 ' -3

0

b::T.

A'%'.

gelada A

I

I

3

principal component 3

Fig. 4. Bivariate plots of principal component sex by species scores. Open circles: Semnopithecus, S. (Trachypithecus), Procolobus (Procolobus), P. (Piliocolobus), Colobus, Pygathrix, P. (Rhinopithecus), Nasalis. Filled-in circles: Presbytis. Open squares: Papio (Mandrillus), Cercocebus, Cercopithecus, Miopithecus. Filled-in squares: Macaca. Triangles: Theropithecus, P. (Papioi, Erythrocebus. Principal component 1 accounts for 90% of the total variation, principal component 2 accounts for 8% of the total variation, and principal component 3 accounts for 2% of the total variation.

203


indices are not independent of body mass. The allometric analysis of the measurements with body mass indicates why indices are negatively and positively correlated with body mass. The principle of mechanical equivalency provides the basis for interpreting the allometric patterns themselves. The subfamilial differences in certain indices are interpreted with reference to reported locomotor behaviors, as are the deviations of terrestrial cercopithecine genera from their subfamilial patterns. Crural index. The allometric basis for the negative correlation of the crural index with body mass is that tibial length is negatively allometric with body mass while femoral length is isometric with body mass. A decrease in the crural index would be expected with increased body mass no matter what the predominant locomotor mode of an animal. The reasoning for this has been most explicitly given by Demes and Gunther (1989) for leaping primates. During the take-off phase of a leap (or push-off phase of a stride) the muscles which extend the distal joints of the hindlimbs require higher force than those of the more proximal joints because the greatest percentage of total body mass is above the distal joints. As body mass increases, the relative strength of the muscles which stabilize the knee, and which produce force at the foothold, decreases. Thus, in order to maintain mechanical similarity with smaller-bodied forms, larger animals must decrease the relative length of the distal segments of the limbs to reduce the load-arm length, and this is reflected in the crural index. Colobines appear to have, on average, slightly lower values for the crural index than do cercopithecines of comparable body mass. One reason for this can be found by examining the difference in the degree of elevation between the subfamilial LS lines for femoral and tibial lengths: the difference between the subfamilies is greater for femoral length than for tibial length. The likely functional explanation for colobines having lower values for the crural index than cercopithecines is that colobines may be similar t o indriids in being “thigh-powered leapers (Gebo and Dagosto, 19881, whereas cercopithecines are primarily quadrupedal walkers and runners. Table 8 summarizes some locomotor fre-

TABLE 8. Frequencies of locomotor modes during travel and feeding’ Species

C. guereza Travel2 Feeding3 P. melalophos4 Travel Feeding P. rubicundas Travel Feeding S. obscura4 Travel Feeding M. fascicularis6 Travel Feeding C. aethiops7 Locomotion

Quadrupedal walking and running

Leaping

42% 48%

35% 15%

21% 36%

43% 11%

32% 51%

45% 1291

51% 69%

40% 15%

65%

11%

74%

4%

54%

10%

‘Values for frequencies are rounded up and represent only part of the reported data. Therefore, frequencies do not add up to totality. 2Morbeck, 1976. jRose, 1978. 4Fleagle, 1978. “avies, 1984. %ant, 1988. ’Rose, 1979.

quency data for cercopithecids taken from the literature. One distinction which emerges from these studies of locomotor patterns is that of the species studied, the colobines engage in leaping much more frequently than do cercopithecines. It should be noted that the data presented in Table 8 are not strictly comparable because they were gathered and presented using different methods. For instance, Morbeck (1976) and Fleagle (1978) summarize locomotor activities a s a percentage of observations while Rose (1978, 1979) reports them in terms of the percentage of total time budgets. Cant (1988) on the other hand reports the percentages of distance moved. Nevertheless, the conclusion that colobines leap more frequently than cercopithecines seems inescapable. The extrapolation of leaping propensity from the study of four species to the whole colobine subfamily is not without empirical justification: the colobine regression lines for both femoral and tibial length are elevated well above the cercopithecine lines, indicating significantly longer hindlimb long bones in colobines. Long hindlimbs increase the distance an animal can leap since acceleration distance is a function of hindlimb length (Hildebrand, 1988). Thus, it seems reasonable to interpret

204

E. STRASSER

the relatively long hindlimbs of all colobines as enhancing leaping. It is also likely that elongation of the hindlimb in colobines is related to dissipating the forces at the end of a leap because the same muscles which generate force to lift the center of gravity at the take-off of a leap must generate enough force to decelerate a t landing. It would strengthen the interpretation that the long hindlimbs of colobines are related to leaping if it could be demonstrated that this same distinction in relative hindlimb length holds for species known to differ in leaping frequency. Locomotor differences between the Semnopithecus (Trachypithecus) and Presbytis species have been well studied (Table 8). Semnopithecus (Trachypithecus) obscura prefers walking quadrupedally along the large boughs of the continuous main canopy and emergent stratum, for which it shows anatomical specializations (Curtin, 1976; Fleagle, 1977a,b, 1978). In contrast, the Presbytis species travel more in the discontinuous understory, and consequently engage in more leaping behaviors for which they also show anatomical specializations (Davies, 1984; Fleagle, 1977a,b, 1978; Washburn, 1942). An examination of the residual values for the regressions of the relevant dimensions against body mass (Table 9) reveals that the S. (Trachypithecus) species have shorter hindlimbs than expected for colobines of their body mass, while most of the Presbytis species have longer hindlimbs than predicted for colobines of their body mass. Thus, the low average crural index values and long hindlimb elements in all colobines compared to cercopithecines support the interpretation that the length and proportions of the hindlimb bones in colobines are related to leaping. Both sexes of Theropithecus gelada and the males of Erythrocebus patas have high values for the crural index given their body masses (Fig. 2A). Examination of these species’ residual values from the cercopithecine regressions of tibal and femoral length against body mass shows that the underlying basis for the high crural indices is not the same. The male E. patas has a rather long tibia for its body mass, giving rise to a high crural index, whereas T. gelada has rather a short femur for its body size, and therefore a high crural index value. One of the factors which may be emphasized to enhance cursorial locomotion in terrestrial forms such as Erythrocebus and Theropithecus is elongation of the distal limb elements relative to

TABLE 9. Standardized residual values f o r variates f r o m subfamilial LS regression lines Species

Sex

Foot

Femur

Tibia

S. obscura S. obscura S. cristata S. cristata P. frontata P. frontata P. melalophos P. melalophos P. aygula P. a y g d a P. rubicunda P. rubicunda P. hosei P. hosei

F M F M F M F M F M F M F M

-0.803 -1.293 -2.052 -1.370

-1.202 -0.941 -1.248 -1.158 1.475 0.699 0.845 0.719 0.304 0.927 0.649 1.152 0.135 1.801

-1.467 -1.146 -1.676 -1.196

0.663 0.644 0.583 0.578 -0.552 0.511 1.054 -0.783 1.796

0.977 1.073 0.785 0.492 0.953 0.700 1.318 0.393 2.140

the proximal elements (Hildebrand, 1988; Smith and Savage, 1956). Elongation of the lighter part of the limb keeps its center of gravity in a proximal position, thus requiring less muscle force to move the limb while increasing the angular velocity of the limb. These changes would be expected in animals engaging in terrestrial cursoriality and would be expressed a s a high value for the crural index a t a particular body mass. It is uncertain why female E. patas do not have a high value for the crural index given their body mass. One possible explanation is that given the degree of sexual dimorphism in Erythrocebus, only the large-bodied males must compensate for their body size. Female E. patas have the equivalent value to males for the crural index and already may be functioning a t an energetically efficient level. Poweriload index In this study the powerlload index is found to have a positive relationship with body mass. The pedal power-arm has a positive allometric relationship with body mass while the pedal load-arm, and in particular the calcaneal and metatarsal portions of the pedal load-arm, has a negative allometric relationship with body mass. This allometric pattern allows larger animals to maintain mechanical equivalence to small animals. Not only does this allometry reduce the amount of muscle force which must be expended during push-off in large animals, but it also contributes to reducing compressive and bending loads experienced by the bones. Colobines have lower values for the power1 load index than do cercopithecines at comparable body masses, because at comparable


body masses colobines have a shorter pedal power-arm and longer pedal load-arm. As discussed by Hildebrand (19881, this “highgear” ratio is expected in leaping animals, since it also contributes to increasing takeoff velocity. A “lower-gear”ratio is expected in more generalized quadrupeds such as cercopithecines. Tarsuslfoot index The tarsuslfoot index is positively correlated with body mass, because the tarsus is isometric with body mass while the foot is negatively allometric. Large-bodied animals have large values for the tarsuslfoot index because the metatarsal and phalangeal components of the composite foot variable are negatively allometric with body mass, making foot length negatively allometric. As a consequence, the tarsus appears to be relatively larger, but it is in fact the other components of foot length which are relatively shorter in larger animals. This suggests, then, that a long tarsus is not a special attribute of all terrestrial cercopithecines. In addition, the tarsus appears t o be shorter in colobines because the other morphological components of the foot are relatively long. Erythrocebus patas, however, is distinctive among terrestrial cercopithecines for the length of its tarsal bones. Of the tarsal bones, both the pedal power-arm and cuboid are longer than expected for this species given its body mass (Fig. 3D, F).It may seem paradoxical that E . patas has a relatively elongated power-arm, since cursors are expected to have shorter power-arms and longer load-arms around joints (Smith and Savage, 1956).However, it could also be that less muscle mass in the leg is advantageous to fleet cursorial primates (see above in crural index), and therefore mechanical advantage is compensated by a longer power-arm. This same argument probably explains the identical elongation of the tarsal bones in the highly terrestrial colobine, Semnopithecus entellus.

205

sion of the powerAoad index. Similarly, the explanation for the high values characterizing the mtIII/foot index in Presbytis species (Fig. 2D) was given above. It is important to note that while the mtIII/ foot index itself does not distinguish the subfamilies, it is the third metatarsal which is the one morphological segment of the of the non-phalangeal foot skeleton that shows the greatest changes in its length relative to body mass, PhIIIlfoot index

The phIIYfoot index shows no correlation with body mass because the scaling exponents, although negatively allometric, are similar for the two components of the index (for cercopithecines this is true when the terrestrial genera are removed from the sample). As a result, the phIIUfoot index is the only one of the five considered here which is not correlated with body mass, but instead reveals distinctive proportions that are a consequence of habitat or locomotor modes. Colobines have markedly longer phalanges than arboreal cercopithecines at comparable body masses. It is clear that the long phalanges of colobines are not simply related to arboreality vs. terrestriality since strictly arboreal cercopithecines have relatively shorter phalanges at comparable body masses. The long colobine phalanges may be related to maintaining contact with the substrate while the hindlimb is generating momentum for leaping (see above). Colobines also may have longer phalanges than arboreal cercopithecines because of differences in their grasps, muscular configurations, muscle sizes, or utilized substrate morphology and elasticity. However, all of this is conjecture until field or laboratory studies are carried out which focus on pedal grasping in cercopithecids. The data presented above do not support Gabis’s and Schultz’s observations that all terrestrial cercopithecines have a long tarsus as a special adaptation to terrestriality. However, the data do support their observaMtIIUfoot index tions that all terrestrial cercopithecines The mtIII/foot index is negatively corre- have relatively short phalanges. Indeed, lated with body mass because the third phalangeal length in terrestrial cercopithemetatarsal has a more negative allometric cines is much shorter than expected for their relationship with mass than does the foot. body masses despite the negative allometry Because the third metatarsal contributes characteristic of the subfamily. By definithe greatest length to the pedal load-arm, tion, terrestrial species spend relatively litthe explanation for the allometry expressed tle time in the trees where grasping the in this index was given above in the discus- substrate is necessary. As a consequence,

206

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terrestrial cercopithecines can afford to have shorter phalanges than arboreal forms. There is a n additional explanation for the short proximal phalanges in terrestrial cercopithecines: since grasping is not required on the ground, terrestrial monkeys can assume a more digitigrade posture during locomotion (Meldrum, 1991). The assumption of a digitigrade posture can effectively elongate the limbs, thus increasing stride length and therefore speed (Hildebrand, 1988). Digitigrady also has repercussions for the role of the phalanges in resisting a ground reaction force. In arboreal cercopithecids which are grasping a branch, the ground reaction force which must be resisted by the extrinsic digital flexors is probably minimal and grasping primates can afford to have relatively long phalanges as these do not contribute to loadarm length. In a terrestrial, digitigrade animal the load borne by the phalanges must be greater than in arboreal forms. If the amount of tensile force in the long flexor tendons is limited, either the power-arm of the tendons around the metatarsophalangeal joint (i.e., metatarsal head height) must increase or the load-arm must decrease. Thus, digitigrade animals might be expected to have relatively shorter phalanges for their body mass than would plantigrade forms. Theropithecus gelada has extremely short phalanges, given its body mass and the amount of phalangeal shortening seen in other terrestrial cercopithecines. Reported accounts of habitat utilization in cercopithecines indicate that all of the P. (Papio) species (with the exception of some populations of P. (Papio) ursinus) and E. patas utilize trees t o sleep, escape predators, and feed (Dunbar, 1977; Hall, 1962, 1963, 1965a,b; Hall et al., 1965; Iwamoto and Dunbar, 1983; Kalter, 1977; Moreno-Black and Maples, 1977; Rowell, 1966; Tappen, 1960). Only T. gelada exclusively occupies the ground, seeking cliff-faces for sleep. Thus, the likely explanation for extremely short phalanges in T. gelada is that it is more committed to terrestriality than are the P. (Papio) species or E. patas. Exceptional species Macaca fuscata and M. thibetana consistently fall below the lower 95% confidence limit for the cercopithecine regressions of numerous dimensions. In the case of M. fuscata every dimension except the lengths of the cuboid and proximal phalanx are below the lower 95% confidence limit, whereas M. thibetana falls below the lower limit for the

regressions of femoral, tibial, and third metatarsal lengths. One possible reason that these variates have extreme negative residual values is that the sample sizes (n = 3 and 4,respectively) are small and biased. However, it is also possible that M . fuscata and M . thibetana have shorter extremeties in response to climatic conditions. Both species are among the most northerly distributed species of cercopithecids, and thus may be following Allen’s Rule. In addition, both species frequent mountainous terrains, so that the combination of altitude with latitude could produce even colder ambient conditions. In both species it is the long bones of the hindlimb and the sole of the foot that are reduced in length rather than the digits, suggesting that the necessity to maintain prehensility is more important for the digits than the conflicting demand of thermal adaptation. This conjecture is intriguing, but since the data are very limited any further extrapolation must await additional documentation.

Principa.1 component analysis The multivariate analysis supports the conclusions reached through regression analysis and the examination of residuals. In addition, one other observation, not apparent in regression analysis or the analysis of residuals, was revealed by PCA. This is that macaques form a distinctive cluster separate from other arboreal cercopithecines because macaques have short hindlimbs. Too little is known about the positional behavior of all these species to proffer a behavioral explanation. However, it is in keeping with taxonomic descriptions of macaques as stocky animals (e.g., Napier, 1981). SUMMARY

It is clear that in a sample of cercopithecids, which range in body mass from 1.3kg to 29 kg, the lengths of the major segments of the hindlimb and foot scale allometrically with body mass to maintain mechanical similarity within locomotor groups. Thus, the first major conclusion of this study is that indices that describe the relative lengths of morphological segments irrespective of the mechanical role of those segments reveal differences that are primarily a function of the size of the animals. Indeed, the traditional focus on morphological, and not mechanical, units has obscured the implications of some significant functional differences in the hindlimbs of cercopithecids. Thus, the


tarsus appears to be long in terrestrial cercopithecines because the metatarsals are short and the tarsus appears to be short in colobines because the metatarsals are long. Indeed, the one morphological segment of the foot which changes its relative length the most in cercopithecids is the metatarsus, contra Gabis and Schultz. The second conclusion revealed by the analysis of mechanically meaningful segments of the hindlimb and foot is that colobines have long hindlimb elements, including the foot, probably to enhance leaping. Among colobines the Presbytis species are especially distinctive for their relatively very long hindlimbs, suggesting that they are the most strongly committed of the subfamily for leaping. In addition to relatively long hindlimbs, colobines are characterized by extremely long phalanges, a conclusion consonant with that of Gabis and Schultz. The presence of extremely long phalanges suggests that colobines rely upon grasping the substrate differently than do arboreal cercopithecines, but without field observations it is impossible to suggest how the two grasps differ. The third conclusion of this study is that the terrestrial cercopithecines have relatively short phalanges, confirming the observations of Gabis and Schultz. Because grasping is not so important in the positional behavior of terrestrial species, as it is for more arboreal species, terrestrial cercopithecines can afford to reduce the length of the phalanges and assume a more digitigrade position of the foot during locomotion. In the P. (Papio) species no other dimension of the foot and hindlimb, in this analysis, reveals a special relationship to terrestriality. The fourth conclusion is that Theropithecus and male Erythrocebus present a high crural index relative to body mass as another feature related to terrestrial life. Female E. patas have a high crural index a s a function of their small body mass. A high crural index contributes to increasing the angular velocity of the limb by keeping the bulk of the mass of the limb in a proximal position. Thus, all terrestrial cercopithecines share short phalanges, but only Theropithecus and male Erythrocebus add a high crural index to their list of specializations. This suggests, then, that Theropithecus and Erythrocebus are more committed to cursoriality than are the P. (Papio) species. The fifth conclusion is that for the dimensions analysed here, macaques form a distinctive group among cercopithecines, char-

207

acterized by relatively short hindlimbs. Thermal conditions may also have as profound a n effect on the lengths of the segments of the hindlimb, relative to body mass, as do specializations for particular locomotor modes and substrate effects. This observation may be corroborated by the shortened long bones and foot bones of Macaca fuscata and M . thibetana, two of the most northerly distributed species in the family. It is of interest that the only bones not affected by cold were the phalanges, suggesting the importance of grasping in the positional repertoire of these animals. In summary, taxonomic differences in the relative lengths of hindlimb segments can be identified if body size is accounted for. Some are interpretable mechanically in terms of locomotor behaviors and substrate preferences while others appear to be characteristic of phylogenetic groups. ACKNOWLEDGMENTS

I thank Drs. B. Corner, E. Delson, T. 01son, M. Rose, C. Ruff, E. Sarmiento, F. Szalay, A. Walker, and C. Ward, Mr. L. Witmer, and Ms. H. Grausz for their discussions with me on aspects of this work; Drs. B. Demes and W. Jungers and two anonymous reviewers for valuable comments on a n earlier version of this manuscript; Ms. Lorraine Meeker and Mr. Chester Tarka of the Department of Vertebrate Paleontology, American Museum of Natural History, for advice on preparation of Figures 2-4; Dr. J. Russo of the Smithsonian Institution for writing the computer program with which I collected data; and the curators and staffs of the Departments of Mammalogy, Anthropology, a n d o r Paleontology of the following institutions for access to collections in their care: American Museum of Natural History, National Museum of Natural History, Museum of Comparative Zoology, Field Museum of Natural History, Tappen (University of Wisconsin-Milwaukee) collection, Oates (Hunter College) collection, British Museum (Natural History), Powell-Cotton Museum, Musee Royal de 1'Afrique Centrale, Rijksmuseum van Natuurlijke Historie, Zoologisk Museum (Copenhagen), Zentrum Anatomie der Georg-August-Universitat (Gottingen), Natur-Museum Senckenberg, Zentrum der Morphologie der Klinikum der Johann Wolfgang Goethe-Universitat, Anthropologisches Institute und Museum der Universitat Zurich-Irchel, Museum National dHistoire Naturelle (Paris), and the National Museums of Kenya.

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Research upon which this work is based was supported by a n NSF Dissertation Improvement grant (BNS-8407911),a C.U.N.Y. Mina Rees Award, a Smithsonian predoctoral fellowship, a Wenner-Gren grant, and a postdoctoral fellowship from the Department of Cell Biology and Anatomy a t The Johns Hopkins University School of Medicine. LITERATURE CITED Aiello LC (1981) The allometry of primate body proportions. Symp. Zool. SOC. Lond. 48:331-358. Alt FB (1982)Bonferroni inequalities and intervals. In S Kotz and NL Johnson (eds.):Encyclopedia of Statistical Sciences, Vol. 1.New York: John Wiley & Sons, pp. 294-300. Biegert J, and Maurer R (1972) Rumpfskelettlange, Allometrien und Korperproportionen bei catarrhinen Primaten. Folia Primat. 17t142-156. Biewener AA (1989) Scaling body support in mammals: Limb posture and muscle mechanics. Science 245t4548. Blackith RE, and Reyment RA (1971)Multivariate Morphometrics. London: Academic Press. Bookstein F, ChernoffB, Elder R, Humphries J, Smith G, and Strauss R 11985)Morphometrics in Evolutionary Biology. Philadelphia: The Academy of Natural Sciences of Philadelphia, Special Publication 15. Booth AH 11957)Observations on the natural history of the olive colobus monkey, Procolobus uerus (van Beneden). Proc. Zool. SOC.,Lond. 129t421-430. Cant JGH (1988) Positional behavior of long-tailed macaques lMacaca fascicularis) in northern Sumatra. Am. J. Phys. Anthropol. 76:29-38. Clark MRB (1980)The reduced major axis of a bivariate sample. Biometrika 67:441446. Clutton-Brock TH, and Harvey P (1977)Primate ecology and social organization. J. Zool., Lond. 183t1-39. Curtin SH (1976) Niche separation in sympatric Malaysian leaf-monkeys (Presbytis obscura and Presb.ytis melalophos).Yrbk. Phys. Anthropol. 2Ot421-439. Davies AG (1984) An ecological study of the red leaf monkey (Presbytis rubscunda) in the dipterocarp forest of northern Borneo. Ph.D. dissertation, University of London. Demes B, and Gunther MM (1989) Biomechanics and allometric scaling in primate locomotion and morphology. Folia Primat. 53:125-141. Dunbar RIM (1977) The gelada baboon: Status and conservation. In HSH Prince Rainier 111ofMonaco and GH Bourne (eds.): Primate Conservation. New York: Academic Press, pp. 363-383. Erikson GE (1963) Brachiation in New World monkeys and in anthropoid apes. Symp. Zool. Soc., Lond. 1Ot135-164. Fleagle J G (1977a) Locomotor behavior and muscular anatomy of sympatric Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos). Am. J. Phys. Anthropol. 46.297-308. Fleagle J G (1977b) Locomotor behavior and skeletal anatomy of sympatric Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos). Yrbk. Phys. Anthropol. 20:440453. Fleagle J G (1978) Locomotion, posture, and habitat utilization in two sympatric, Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos). In GG Montgomery (ed.): Ecology of Arboreal Folivores.

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Appendix. Summary statistics for measurements analysed in this study'

E. patas C. albogularis C. mitis C. nictitans

C. pygerythrus C. petaurista C. cephas

C. ascanius

C. campbelli C. mona C. pogonias M. talapoin

M.arctoides M. thibetana M. syluana

M. nemestrina M. nigra M. fuscata M. mulatta

M. fascicularis C. torquatus C. galeritus C. albigena P. ursinus P. anubis

P. cynocephalus P. hamadryas

P. sphinx

Femur

Tibia

Calcaneus

Pedal power arm

167.3 i 14.50 (2) 203.3 f 5.77 (3) 145.0 f 5.05 (10) 178.9 f 13.44 (8) 148.0 f 5.68 (12) 174.3 f 6.89 (8) 154.9 i 8.31 (5) 179.2 f 8.10 (14) 133.3 7.79 (12) 150.5 f 12.44 (15) 133.5 i 4.82 (3) 147 (1) 136.5 f 5.87 (4) 156.2 f 6.59 (15) 128.5 f 4.66 (91 155.0 f 7.10 (10) 128.3 f 2.48 (2) 152.3 f 6.72 (2) 130.5 i 3.54 (2) 162.3 i 5.67 (10) 133.1 f 3.15 (5) 154.7 f 4.38 (13) 90.1 t 5.55 (7) 96.4 f 6.33 (4) (0) 172.8 i 9.55 (2) .. (0) 178.5 f 5.87 (4) 181 (1) 202.0 f 2.74 (4) 166.0 f 13.46 (6) 201.3 i 18.25 (6) 157 (1) 189.0 f 2.29 (3) (0) 171.8 i- 6.53 (3) 163.9 f 7.08 (10) 185.6 f 7.78 (10) 125.7 f 4.70 (10) 145.1 f 6.98 (10) 179.0 f 3.79 (7) 218.1 f 11.17 (11) 192.6 11.72 (4) 207.3 f 18.09 (8) 174.7 f 4.66 (10) 201.8 f 4.34 (14) 214.2 f 7.69 (3) 270.0 f 23.20 (4) 224.0 f 9.60 (4) 257.3 i 9.93 (13) 227.1 f 7.70 (8) 258.1 f 14.72 (11) 207.8 i 10.96 (2) 236.9 i 12.88 (5) 207.0 9.07 (4) 287.0 f 2.83 (21

163.0 f 14.14 (2) 202.3 f 8.87 (4) 143.0 f 8.06 (10) 172.9 f 14.93 (9) 143.9 f 5.45 (12) 169.4 f 7.07 (8) 152.8 t 8.20 (5) 173.1 i 8.64 (14) 126.4 f 7.64 (12) 142.6 f 12.10 (15) 129.7 f 4.16 (3) 143 (1) 134.0 f 5.34 (4) 154.1 t 5.85 (15) 123.5 i 3.95 (9) 151.0 f 7.66 (10) 124.8 f 4.60 (2) 149.5 k 4.95 (2) 127.3 i 5.30 (2) 158.7 i- 6.68 (10) 131.5 f 3.34 (5) 151.2 f 5.19 (13) 89.3 f 5.10 (7) 97.5 f 6.29 (4) (0) 154.8 i 3.18 (21

34.00 i 2.462 (2) 41.06 f 1.629 (4) 27.53 f 1.443 (10) 33.27 f 1.583 (9) 28.09 f 0.905 (12) 32.85 f 1.141 (8) 28.37 f 1.156 (5) 33.41 f 1.559 (14) 26.04 i 0.782 (12) 28.25 f 2.177 (15) 24.17 f 0.293 (4) 27.5 (1) 25.71 f 1.619 (4) 28.97 f 1.120 (15) 23.63 t 0.729 (10) 28.40 f 1.143 (10) 22.75 i 1.563 (2) 30.45 f 0.467 (2) 24.09 f 0.188 (2) 31.00 f 1.288 (10) 25.09 t 1.111 (5) 28.84 f 0.891 (13) 16.98 f 1.108 (7) 18.11 f 0.723 (4) (0) 36.43 f 1.535 (2) (0) 38.14 t 0.524 (4) 33.8 (1) 39.25 k 1.602 (4) 30.13 f 1.996 (6) 35.54 t 2.413 (6) 29.4 (1) 34.89 i 0.460 (3) in) 35.52 k'i1535 (3) 32.13 f 1.277 (10) 35.99 i 1.127 (10) 23.62 f 1.008 (10) 27.47 f 1.739 (10) 31.93 i 0.955 (7) 38.93 i 1.931 (11) 32.00 f 1.380 (4) 37.45 f 1.403 (8) 29.81 f 1.589 (10) 36.60 f 1.269 (14) 43.14 f 3.037 (4) 49.68 f 3.400 (4) 43.26 f 2.115 (4) 49.86 f 3.029 (15) 40.29 f 1.032 (8) 46.91 f 2.757 (11) 38.22 t 2.524 (2) 43.51 f 2.083 (5) 35.92 i 2.366 (5) 50.30 f 0.378 (3) 36.60 f 2.541 (2) 45.04 i 1.141 (2) 39.3 (1) 44.14 f 3.024 (4) 38.33 f 0.734 (5) 43.75 f 1.580 (8) 32.16 i- 0.686 (3) 38.66 i 1.348 (5) 36.35 f 1.307 (6) 42.6 (1) 40.72 i 1.205 (6) 44.52 k 1.733 (2) 30.11 f 1.169 (71 32.26 i 0.864 i8j 28.28 f 1.160 (13) 30.56 & 1.317 (12) 31.42 t 1.275 (2) 31.08 t 0.251 (2) 32.55 f 1.711 (4)

16.71 2.361 (2) 21.03 f 1.496 (4) 12.63 f 1.005 (10) 16.08 f 1.055 (9) 13.27 i 0.727 (12) 15.82 i 0.517 (81 13.20 f 0.393 (5) 15.66 f 0.953 (14) 12.14 f 0.882 (12) 13.39 f 1.251 (15) 10.52 f 0.690 (4) 13.0 (1) 11.50 f 0.516 (4) 13.56 i 0.689 (15) 11.06 i 0.693 (10) 13.25 f 0.949 (10) 10.27 f 0.319 (2) 14.46 0.359 izj 11.03 f 0.211 (2) 14.33 f 0.789 (10) 11.30 f 0.622 (5) 12.76 f 0.772 (13) 7.29 f 0.646 (7) 7.64 f 0.483 (4) (0) 17.67 f 0.800 (2)

+

+

P. leucophaeus T. gelada

N . larvatus

P. nemaeus P. roxellanae 5'. entellus T. obscara T. cristata

P. frontata P. melalophos

215.0 f 1.41 (2) 215.0 & 5.61 (4) 243.1 i 10.02 (8) 210.0 f 3.54 (2) 233.1 i 8.49 (5) 197.7 t 6.06 (6) 230 (1) 217.8 i 4.98 (6) 243.0 f 4.24 (2) 176.1 f 9.24 (71 184.7 8.40 (8j 170.1 f 6.07 (13) 177.1 8.77 (12) 199.5 2.83 (2) 189.0 f 3.54 (2) 198.4 f 7.73 (4) 197.8 f 6.98 (4)

+

**

in) \"#

160.6 f 5.68 (4) 161 (1) 183.8 2.33 (4) 153.3 f 10.11 (6) 181.2 i 15.02 (6) 145 (1) 172.5 f 2.50 (3) .. (0) 159.5 f 6.54 (3) 151.3 f 7.14 (10) 169.2 f 6.55 (10) 118.7 f 3.69 (9) 134.8 f 6.43 (10) 165.9 f 2.46 (7) 201.3 f 9.04 (11) 173.1 t 9.31 (4) 190.6 i 14.99 (8) 162.9 f 6.88 (101 188.3 t 4.72 (i4j 193.5 i 20.08 (3) 232.0 f 22.64 (4) 190.8 f 10.56 (4) 225.5 f 11.05 (15) 201.3 f 7.62 (8) 227.1 f 13.10 (11) 183.5 f 9.19 (2) 206.4 i 11.23 (5) 188.8 f 10.25 (5) 260.0 i 7.94 (3) 182.5 t 17.68 (2) 250 (1) 191 (1) 214.5 f 3.54 (2) 188.3 f 4.24 (5) 217.4 i 6.07 (8) 191.3 i 1.16 (3) 207.1 f 4.55 (5) 172.5 f 7.63 (5) 203 (1) 189.9 f 6.62 (5) 210.8 i 8.13 izi 157.4 f 7.06 (7) 165.1 f 8.80 (8) 151.1 i 4.90 (13) 160.6 f 6.19 (12) , , (0) 176.0 f 1.41 (2) 183.3 f 7.63 (4) 180.7 i 9.50 (3)

+

*

+

mi xu,

18.41 f 1.052 (4) 15.9 (1) 18.85 f 0.927 (4) 13.77 f 0.913 (61 17.17 f 1.709 (6) 14.6 (1) 17.31 f 0.511 (3) (0) 17.59 f 1.499 (3) 15.45 f 0.869 (10) 17.39 1.150 (10) 11.24 f 0.634 (10) 13.22 f 1.305 (10) 14.73 i 0.417 (7) 18.79 f 0.929 (11) 15.81 f 0.711 (4) 18.30 f 1.331 (8) 13.87 0.641 (10) 16.81 f 0.930 (14) 21.43 i 1.665 (4) 26.99 f 3.139 (4) 21.94 f 1.366 (4) 25.76 f 1.807 (15) 22.42 f 7.176 (8) 23.83 i 2.587 (11) 19.63 f 1.006 (2) 22.19 i 0.960 (5) 18.49 i 0.968 (5) 27.52 f 1.644 (3) 17 29 f 1.145 (2) 22.39 f 0.472 (2) 19.5 (1) 22.14 f 1.592 (4) 16.92 f 0.783 (5) 20.56 f 1.411 (8) 14.55 f 1.023 (3) 17.90 f 0.680 (5) 17.02 f 0.794 (6) 20.0 (1) 19.83 f 0.831 (6) 21.00 f 0.606 (2) 13.31 i 0.879 (7) 14.90 f 0.724 (8) 12.53 f 0.820 (13) 13.43 f 0.622 (121 14.25 f 0.337 (2) 14.18 f 0.530 (2) 15.61 f 1.793 (4)

* *

Calcaneal load arm 15.44 f 0.089 (2) 18.92 f 0.488 (4) 14.27 i 0.752 (10) 16.72 f 0.701 (9) 14.50 f 0.590 (12) 16.08 i 1.034 (8) 14.47 f 0.897 (5) 16.75 f 1.299 (14) 13.50 f 0.575 (12) 14.13 f 1.004 (15) 13.19 f 0.524 (4) 14.7 (1) 13.85 f 1.169 (4) 14.45 f 0.738 (15) 12.68 f 0.572 (10) 14.51 f 0.861 (10) 12.32 f 0.561 (2) 15.55 f 0.225 (2) 12.86 f 0.436 (2) 15.45 f 1.289 (10) 13.40 f 0.753 (5) 15.34 f 0.506 (13) 9.49 f 0.643 (7) 10.11 f 0.341 (4) (0) 17.81 i 0.610 (2) (0) 18.80 t 0.631 (4) 16.6 (1) 19.28 f 1.127 (4) 15.58 f 1.468 (6) 17.70 i 0.549 (6) 15.3 (1) 16.64 k 1.283 (3) (0) 17.28 i 1.173 (3) 15.52 f 0.582 (10) 17.25 f 0.343 (10) 12.42 f 0.763 (10) 14.20 i 1.079 (10) 16.15 f 0.945 (7) 18.54 i 1.202 (11) 15.54 i 1.244 (4) 18.08 f 0.843 (8) 15.51 f 0.658 (10) 17.24 i 0.444 (14) 20.39 i 1.911 (4) 22.19 f 0.750 (4) 20.38 t 1.437 (4) 23.04 i 1.459 (15) 19.17 i 1.039 (8) 21.43 i 1.333 (11) 17.44 f 1.212 (2) 20.47 f 1.288 (5) 18.29 f 1.339 (5) 21.66 f 2.633 (3) 18.73 i 0.426 (2) 21.75 f 0.472 (2) 17.8 (1) 20.27 f 1.678 (4) 19.98 f 0.503 (5) 21.42 f 0.869 (8) 16.30 f 0.629 (3) 18.49 f 0.916 (5) 18.61 f 0.759 (6) 21.0 (1) 19.20 f 0.854 (6) 21.16 i 0.930 (2) 15.16 i 0.973 (7) 16.27 t 1.081 (8) 14.57 f 0.707 (13) 15.70 f 0.908 (12) 16.01 f 1.010 (2) 15.98 f 0.414 (2) 16.68 f 0.661 (4) 16.17 f 1.524 (4)

211

HINDLIMBS IN CERCOPITHECIDS ~

Metatarsal I11 45.04 f 3.185 (2) 57.12 12.369 (4) 42.87 f 2.681 (10) 51.04 f 4.108 (9) 43.90 f 2.103 (12) 51.77 f 2.083 (8) 49.10 f 2.378 (5) 52.11 13.553 (14) 38.10 f 1.782 (12) 42.93 C 3.607 (14) 39.52 i 1.824 (4) 44.8 (1) 39.65 i 1.421 (3) 45.98 i 1.174 (15) 37.23 & 1.703 45.99 11.931 (10) 37.69 i 0.934 (2) 46.22 & 1.257 (2) 39.39 f 1.068 (2) 49.20 11.822 (10) 40.12 i- 1.667 (4) 46.45 f 1.591 (13) 27.97 i 1.725 (7) 31.54 i 1.936 (4) (0) 49.19 f 3.000 (2) (0) 48.30 f 1.194 14) , _ 50.9 (1) 57.74 i 1.726 (4) 45.53 f 1.584 (6) 53.08 f 4.636 (6) 43.5 (1) 52.14 I 1.927 (3) (0) 48.90 i 2.390 (3) 46.87 2.474 (10) 53.02 i 3.238 (10) 37.00 f 1.055 (10) 41.73 f 2.031 iioj 49.26 f 1.713 (7) 60.30 f 2.718 (11) 49.25 i 2.067 (4) 54.83 f 3.155 (8) 46.48 f 2.133 (10) 54.07 f 2.819 (14) 57.17 f 3.667 (4) 65.81 5.632 (4) 56.40 i 3.268 (4) 67.02 i 4.351 (15) 57.61 i 1.819 (8) 64.25 i 5.089 (11) 53.80 f 1.599 121 60.41 zk 3.421 i5j 52.27 i 4.362 (5) 71.78 f 2.584 (3) 52.24 f 4.967 (2) 66.54 C 2.398 (2) 58.1 (1) 62.05 f 2.534 (4) 59.14 1.702 (5) 68.81 i 1.865 (8) 55.15 10.279 (2) 60.24 f 0.921 (5) 50.73 f 2.433 (6) 60.4 (1) 60.99 i 2.565 (6) 65.81 f 3.044 (2) 47.59 i 2.864 (7) 51.00 f 2.169 (8) 47.89 f 2.143 (13) 49.61 i 2.316 (12) 52.36 i 0.431 (2) 52.94 i 2,990 (2) 56.15 i 2.979 (4) 56.27 i 1.705 (4)

(14

*

*

Phalanx 111 20.8 (1) 25.1 (1) 21.88 f 1.709 (8) 26.97 f 1.814 (6) 23.61 f 0.592 (11) 27.10 f 1.136 (7) (0) 25.5 (1) 19.94 i 1.454 (7) 21.14 f 1.766 (10) 21.81 & 0.718 (2) 23.6 (1) 20.1 (1) 20.7 (1) 19.05 i 0.881 (9) 22.75 f 1.101 (10) 20.6 (1) 23.79 f 0.269 (2) 20.59 f 0.575 (2) 25.24 f 0.886 (7) (0) 23.79 f 2.209 (2) 15.27 10.636 (5) 16.74 f 0.654 (4) (0) (0) (0) 30.40 f 0.621 (3) 26.7 (1) 31.41 i 0.997 (2) 25.97 f 1.368 (4) 30.07 f 2.652 (5) 25.6 (1) 27.38 f 0.808 (2) (0) 26.05 f 2.048 12) , , (0) 28.45 i 0.269 (2) 20.82 f 1.001 (6) 23.41 f 1.139 (10) 25.97 i 0.560 (4) 31.39 f 1.454 (7) 24.9 (1) 28.31 I 1.728 (5) 24.81 f 0.693 (9) 28.09 10.975 (11) 26.19 f 2.505 (2) 29.68 f 6.466 (2) 28.2 (1) 31.34 f 1.555 (5) 25.88 f 0.854 (4) 28.52 f 1.292 (10) 24.70 f 1.257 (2) 1.476 (4) 27.01 I 28.50 1.831 (4) (0) 29.15 f 2.703 (2) 36.4 (1) 21.6 (1) 22.92 f 0.106 (3) 34.05 f 1.188 (3) 38.32 f 1.549 (6) 34.0 (1) 34.7 (1) (0) (0) (0) (0) 30.45 f 1.051 ( 2 ) 29.26 i 0.496 (3) 26.82 f 2.183 (7) 28.46 f 1.332 (6) (0) 28.1 (1) 30.28 f 2.236 (3) 30.16 1.649 (4)

*

*

~

Cuboid

~~~~

~~

Tarsus

Pedal load arm

13.76 f 1.959 (2) 16.23 f 0.369 (4) 10.03 f 0.681 (10) 12.05 i 0.807 (9) 10.04 i 0.727 (12) 11.68 f 0.911 (8) 10.61 10.471 (5) 12.30 f 0.872 (14) 10.33 f 0.468 (12) 11.03 0.774 (15) 9.58 f 0.516 (4) 9.7 (1) 10.20 f 1.237 (4) 11.25 i 0.459 (15) 8.81 0.374 (lo) 10.85 f 0.700 (10) 9.11 f 0.027 (2) 10.69 f 0.871 (2) 9.37 f 0.206 (2) 11.91 10.802 (10) 9.95 f 0.317 (5) 11.01 f 0.436 (13) 6.89 i 0.322 (7) 7.69 t 0.117 (4) (0) 14.34 f 0.144 (2) (0) 15.51 i 0.533 (4) 13.0 (1) 15.99 i 0.533 (4) 12.12 f 0.638 (6) 13.90 f 1.011 (6) 11.4 (1) 13.92 10.197 (3)

47.75 f 4.422 (2) 57.29 zk 1.502 (4) 37.56 f 2.046 (10) 45.32 f 2.273 (9) 38.12 i 1.513 (12) 44.53 f 1.601 (8) 38.98 f 1.523 (5) 45.71 f 2.313 (14) 36.37 i 1.130 (12) 39.28 f 2.863 (15) 33.75 f 0.695 14) , , 37.2 (1) 35.91 i 2.757 (4) 40.22 i 1.234 (15) 32.44 f 0.697 (10) 39.25 f 1.601 (10) 31.86 f 1.590 (2) 41.14 f 0.404 (2) 33.45 i 0.395 (2) 42.91 i 1.767 (10) 35.04 f 1.141 (5) 39.85 f 1.198 (13) 23.88 i 1.316 (7) 25.79 i 0.827 (4) (0) 50.77 f 1.679 (2) (0) 53.64 f 0.720 (4) 46.8 (1) 55.23 I 1.778 (4) 42.26 i 2.477 (6) 49.44 3.289 (6) 40.8 (1) 48.81 f 0.522 (3)

74.24 f 5.233 (2) 92.27 f 2.735 (4) 67.17 13.743 (10) 79.81 i 5.079 (9) 68.43 f 2.868 (12) 79.53 f 3.144 (8) 71.18 i 3.440 (5) 81.16 15.009 (14) 61.93 f 2.529 (12) 68.12 15.248 (14) 62.29 f 1.085 (4) 69.3 (1) 62.61 f 2.556 (3) 71.68 f 1.727 (15) 58.72 I 2.000 (10) 71.36 f 2.248 (10) 59.13 f 1.522 (2) 72.45 f 0.611 (2) 61.61 i 1.710 (2) 76.55 12.940 (10) 63.20 f 1.748 (4) 72.80 f 1.984 (13) 44.34 f 2.385 (7) 49.33 i 2.057 (4) (0) 81.34 f 3.753 (2)

(0)

(0)

(0)

49.28 f 3.289 (3) 44.40 1.673 (10) 49.72 C 1.571 (10) 32.86 i 1.532 (10) 38.49 i 2.480 (10) 43.86 f 1.434 (7) 53.61 f 2.602 (11) 44.32 i 2.123 (4) 51.15 f 1.783 (8) 41.91 2.161 (10) 48.09 f 1.673 (14) 59.76 f 3.838 (4) 68.69 f 5.166 (4) 59.76 -C 2.572 (4) 68.74 f 3.569 (15) 55.63 f 1.219 (8) 65.07 f 3.087 (11) 52.92 f 3.161 (2) 60.07 f 2.324 (5) 49.05 3.418 (5) 67.47 f 1.631 (3) 49.44 & 1.976 (2) 62.08 i 1.437 (2) 54.6 (1) 60.97 i 4.044 (4) 52.93 f 0.992 (5) 60.16 i- 1.626 (8) 44.40 f 0.989 (3) 53.94 i 1.265 (5) 49.87 i 1.659 (6) 59.0 (1) 56.53 f 2.118 (6) 60.78 1.086 (2) 42.28 f 1.440 (7) 44.76 i 1.421 (8) 39.69 i 1.344 (13) 42.35 i 1.637 (12) 43.62 f 1.302 (2) 43.09 f 0.503 (2) 45.56 f 2.517 (4) 44.53 f 2.279 (4)

79.94 f 4.367 (3) 74.66 f 3.094 (10) 83.99 3.723 (10) 58.67 f 2.009 (10) 66.96 13.597 (10) 77.34 i 2.993 (7) 93.52 i 4.010 (11) 77.11 i 4.034 (4) 86.60 f 3.279 (8) 74.09 f 3.046 (10) 84.79 i 3.423 (14) 94.17 f 6.322 (4) 107.00 f 8.102 (4) 93.29 f 4.024 (4) 108.94 f 6.043 (15) 92.11 f 1.569 (8) 103.84 f 5.438 (11) 85.94 I 3.449 (2) 97.44 i 4.569 (5) 83.68 i 6.535 (5) 110.62 f 3.781 (3) 83.82 f 4.827 (2) 105.33 f 3.166 (2) 91.1 (1) 99.15 f 4.500 (4) 93.73 i 2.333 (5) 106.65 f 2.326 (8) 84.01 f 1.002 (2) 94.01 I 1.065 (5) 82.86 I 3.073 (6) 98.0 (1) 95.99 & 4.237 (6) 103 22 f 3.327 (2i 74.92 f 3.926 (7) 79.76 f 1.877 (8) 73.87 f 2.600 (13) 77.10 13.272 (12) 80.57 f 1.468 (2) 80.93 f 2.650 (2) 85.84 4.415 (4) 84.54 i 1.257 (4)

*

*

13.76 C 1.003 (31 12.27 f 0.655 (10) 13.73 i 0.572 (10) 9.24 0.747 (10) 11.03 f 0.898 (10) 11.93 f 0.565 (7) 14.68 f 0.882 (11) 12.32 f 0.804 (4) 13.69 i 0.627 (8) 12.10 i 0.671 (10) 13.49 f 0.534 (14) 16.62 i 0.833 (4) 19.01 i1.885 (4j 16.50 f 1.478 (4) 18.88 11.092 (15) 15.33 f 0.425 (8) 18.16 f 1.178 (11) 14.70 -i- 0.638 (2) 16.56 10.464 (5) 13.13 F 1.115 (5) 17.17 f 1.406 (3) 12.85 f 0.566 (2) 17.04 f 0.296 12) 15.3 (1) 16.83 f 1.092 (4) 14.61 f 0.876 15) 16.42 f 0.846 (8j 12.24 i 0.346 (3) 15.28 f 0.534 (5) 13.52 f 0.373 (6) 16.5 11) 15.80 f 0.9,4 (6) 16.26 i 0.647 (2) 12.17 f 0.388 (7) 12.49 f 0.769 (8) 11.41 f 0.335 (13) 11.79 f 0.397 (12) 12.20 i 0.027 (2) 12.01 f 0.754 (2) 13.01 0.915 (4) 12.10 f 0.856 (4)

*

*

+

*

*

*

*

mi

82.61 i'2:028 (4) 80.4 (1) 93.00 i 1.658 (4) 73.23 f 3.104 (6) 84.69 & 5.883 (6) 70.2 (1) 82.70 i 2.181 (3)

*

+

Foot 118.9 (1) 142.2 (1) 100.78 f 4.527 124.53 f 8.947 105.01 i 3.247 123.27 f 4.174 (0) 122.6 (1) 94.16 i 4.254 101.77 I- 8.306 96.19 f 1.203 105.7 (1) 91.7 (1) 106.1 (1) 88.78 f 3.031 107.99 f 3.284 91.9 (1) 111.14 f 0.583 93.43 f 2.038 116.87 k 3.920 (0) 109.49 f 5.604 66.33 f 3.421 74.07 f 3.084

(8) (6) (11)

(7) (7) (10) (2)

(9) (101 (2) (2) (7) (2) (5) (4)

(0) (0) (0) 131.71 2.'230 124.3 (1) 144.52 13.637 112.11 i 4.295 131 09 i 9.901 109.8 (1) 127.56 f 3.449

*

(3) (2) (4) (5)

(2) (0) 122.76 19.214 (2) (0) 131.50 f 3.062 (2) 91.29 f 3.561 (6) 103.64 f 4.793 (10) 121.12 f 1.875 (4) 146.06 f 6.366 (7) 117.1 (1) 132.93 15.602 (5) 112.14 f 2.944 (9) 129.67 f 4.574 (11) 145.48 f 12.797 (2) 166.85 C 23.897 (2) 145.4 (1) 164.99 f 8.097 (5) 137.97 f 1.432 (4) 155.89 i 5.7'22 (10) 131.42 f 6.017 (2) 148.20 f 7.158 (4) 128.31 9.612 (4) (0) 130.84 i 9.646 (2) 167.7 (1) 134.3 (1) 144.19 f 6.736 (3) 147.32 f 3.410 (3) 167.99 i- 3.880 (6) 133.8 (1) 147.6 (1) (0)

*

(0) (0)

(0) 123.63 14.139 124.50 f 2.566 112.80 i 4.129 120.65 C 5.157 (0) 125.8 (1) 130.69 f 8.117 130.97 13.077

(2) (3) (7) (6) (3) (4)

(Continued)

212

E. STRASSER

Appendix. Summary statistics for measurements analysed in this study' (Continued)

P. aygula

P. rubicunda

P.hosei C. guereta C. angolensis C. polykomos C. uellerosus C. sutana

P. uerus P. badius

Femur

Tibia

Calcaneus

Pedal power arm

193.2 f 10.56 (3) 201.3 f 9.78 (3) 195.4 rt 4.22 (9) 201.3 f 5.40 (10) 183 (1) 209.5 t 1.41 (2) 186.4 f 6.61 (13) 199.1 f 9.46 (16) 191.6 f 8.84 (4) 192.5 f 1.41 (2) 204 (1) 210 (1)

177.8 i 10.80 (3) 183.3 t 8.08 (3) 178.5 f 4.40 (11) 185.3 f 5.43 (10) 169.8 f 10.25 (2) 195.0 i 4.24 (2) 171.3 f 6.27 (14) 184.6 f 9.96 (16) 177.0 f 10.13 (4) 177.3 f 6.01 (2) 191 (1) 192 (1)

32.96 f 1.570 (3) 31.02 f 0.980 (3) 31.32 f 0.706 (11) 32.34 f 0.952 (11) 30.80 f 1.814 (2) 33.06 f 1.032 (2) 34.40 t 1.591 (14) 35.52 f 2.171 (16) 34.10 f 1.632 (4) 35.01 t 0.008 (2) 35.35 f 1.410 (2) 38.96 f 1.185 (2)

15.99 t 1.109 (3) 14.28 t 0.150 (3) 14.53 i 0.571 (11) 14.65 f 0.556 (11) 14.00 jl 1.495 (2) 15.71 i 0.831 (2) 15.96 t 1.002 (14) 16.91 f 1.444 (16) 15.14 t 0.554 (4) 15.50 t 0.292 (2) 16.68 t 0.198 (2) 18.44 t 0.938 (2)

(0)

201.0 rt 0.71 (2) 213 (1) 229.5 f 0.71 (2) 147.0 f 4.24 (2) 150.2 i 4.13 (5) 196.6 f 30.84 (12) 185.5 f 8.50 (13)

(0)

189.0 f 1.41 190 (1) 202.3 f 2.48 139.3 f 1.06 141.9 i 5.30 169.3 i 8.71 166.3 f 9.46

(2)

(2) (2) (4) (12) (12)

(0)

(0)

36.77 t 0.772 (2) 35.6 (1) 37.08 t 1.823 (2) 26.36 f 0.745 (3) 27.94 f 0.296 (6) 34.37 f 1.487 (12) 34.26 i 1.930 (14)

16.49 f 1.922 (2) 16.0 (1) 17.14 0.337 (2) 10.88 t 0.915 (3) 12.54 i 0.447 (6) 16.46 i 1.342 (12) 15.58 1.010 (14)

'Females first row, males second row. Statistics are mean f one standard deviation (sample sire)

*

+

Calcaneal load arm 16.07 f 1.073 (3) 15.92 t 0.889 (3) 15.95 f 0.466 (11) 16.63 i 0.562 (11) 15.22 f 0.713 (2) 16.90 f 0.660 (2) 16.95 t 0.903 (14) 17.02 f 1.158 (16) 16.53 t 1.131 (4) 17.48 f 1.540 (2) 17.30 f 1.491 (2) 19.17 f 0.499 (2) (0) 18.52 i 1.069 (2) 17.8 (1) 18.31 f 0.822 (2) 13.58 f 0.764 (3) 14.41 i 0.565 (6) 16.62 f 0.695 (12) 17.02 f 1.332 (14)

213


Metatarsal I11

Phalanx 111

Cuboid

Tarsus

Pedal load arm

55.94 i 2.682 (3) 53.90 1.987 (3) 56.86 f 1.475 (11) 57.82 1.551 (11) 53.09 f 5.226 ( 2 ) 60.09 f 1.985 ( 2 ) 52.59 i 2.437 114) 56.22 3.033 (i5j 55.19 i 2.541 (4) 55.35 1.446 (2) 58.62 f 3.825 (2) 58.01 f 0.323 (2) (0) 57.88 0.638 (2) 56.6 (1) 61.47 f 2.012 (2) 44.60 f 2.055 (3) 44.18 f 1.839 (6) 56.29 f 2.578 (12) 53.99 i 3.292 (14)

30.68 f 1.221 (3) 28.36 f 1.711 (3) 30.17 1.022 (6) 30.98 0.641 (9) 28.1 (1) 31.43 f 1.213 ( 2 ) 30.95 f 1.511 17) 32.15 f 1.978 (9) 32.91 i 1.033 (2) 31.7 (1) 34.8 (1) 33.96 0.718 (2) (0) 33.04 f 0.692 (2) 35.6 (1) (0) 26.08 0.491 (3) 25.89 f 0.707 (5) 32.61 f 1.340 il0) 32.59 f 1.968 (7)

11.83 f 0.476 (3) 11.26 f 1.073 (3) 11.05 f 0.439 (11) 11.10 f 0.536 (11) 11.13 f 0.701 ( 2 ) 12.50 f 0.126 (2) 11.86 f 1.032 114) 12.75 f 1.027 (16) 13.19 f 0.761 (4) 13.43 f 0.296 ( 2 ) 12.30 i 1.033 (2) 13.75 f 0.350 ( 2 ) (0) 12.50 -t 0.180 (2) 13.0 (1) 14.36 0.808 ( 2 ) 9.72 -t 0.940 (3) 9.91 & 0.545 (6) 12.02 f 0.701 (12) 12.13 0.731 (14)

44.79 f 1.349 (3) 42.28 j, 1.436 (3) 42.37 f 0.798 (11) 43.44 1.334 (11) 41.92 f 2.515 (2) 45.56 f 0.907 (2) 46.26 +- 2.369 (14) 48.27 i 3.058 (i6j 47.29 f 2.371 (4) 48.44 0.305 ( 2 ) 47.65 f 2.443 (2) 52.71 k 0.835 (2) (0) 49.26 i 0.593 (2) 48.6 (I) 51.44 2.631 ( 2 ) 36.08 f 1.645 (3) 37.84 i 0.521 (6) 46.39 1.876 (12) 46.39 i 2.458 (14)

83.84 f 3.311 (3) 81.08 f 3.303 (3) 83.86 i 1.831 (11) 85.55 f 2.233 (11) 79.43 f 6.640 (2) 89.49 f 2.519 (2) 81.40 C 3.546 (14) 86.02 f 4.731 (15) 84.90 f 3.716 (4) 86.26 f 0.202 (2) 88.23 f 6.349 (2) 90.94 f 1.172 (2) (0) 88.89 -t 1.886 ( 2 ) 87.4 (1) 94.14 dz 3.642 (2) 67.91 f 2.307 (3) 68.49 2.534 (6) 84.93 f 3.415 (12) 83.14 f 4.378 (14)

* *

*

*

*

**

+

*

+

+

* *

+

+

*

Foot

* * * *

131.41 3.981 124.54 i 4.622 129.55 i 3.246 132.55 3.336 117.6 (1) 137.08 i 4.104 130.14 4.667 136.49 7.587 136.93 C 1.634 134.3 (1) 145.5 (1) 144.68 i 1.230 (0) 140.18 f 0.646 140.9 (1) (0) 106.76 f 3.056 108.70 f 0.899 136.05 f 5.104 136.35 4.602

*

(3) (3) (6) (9) (2) (7) (gj (2)

(2) (2)

(3) (5) (10) (7)

Pheochromocytoma in Old World Primates (Macaca mulatta and Chlorocebus aethiops).

Erosive arthritis and spondyloarthropathy in Old World primates.

Fore- and hindlimb proportions in Plio-Pleistocene hominids.

Ancestral facial morphology of Old World higher primates.

Eocene primates of South America and the African origins of New World monkeys.

Amylase iso-enzymes in primates of the families Lemuridae, Cebidae, Cercopithecidae, Hylobatidae and Pongidae.

Osteoarthritis, calcium pyrophosphate deposition disease, and osseous infection in Old World primates.

Contrasted patterns of variation and evolutionary convergence at the antiviral OAS1 gene in old world primates.

Phylogenetic significance of the skin of New World monkeys (order primates, infraorder Platyrrhini).

The involucrin gene of Old-World monkeys and other higher primates: synapomorphies and parallelisms resulting from the same gene-altering mechanism.

Evolution of the pseudoautosomal boundary in Old World monkeys and great apes.

Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy.

Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans.

Scale effects and morphological diversification in hindlimb segment mass proportions in neognath birds.

Occlusal force and craniofacial biomechanics during growth in rhesus monkeys.

Old world monkeys and new age science: the evolution of nonhuman primate systems virology.

S-cone visual stimuli activate superior colliculus neurons in old world monkeys: implications for understanding blindsight.

Identification of a derived dental trait in the papionini relative to other old world monkeys.

Complete mitochondrial genome of the sooty mangabey, Cercocebus atys atys (Mammalia: Primates: Cercopithecidae).

Jaw-muscle force and excursion scale with negative allometry in platyrrhine primates.

Male reproductive strategies in new world primates.

Functional assessment of subfamily variation in maxillomandibular morphology among Old World monkeys.

Functional evolution of the OAS1 viral sensor: Insights from old world primates.

Draft Genome Sequence of Plasmodium gonderi, a Malaria Parasite of African Old World Monkeys.