ANTHROPOLOGICAL SCIENCE Vol. 115, 107–117, 2007

Distal humerus and ulna of Parapresbytis (Colobinae) from the Pliocene of Russia and Mongolia: phylogenetic and ecological implications based on elbow morphology Naoko EGI1*, Masato NAKATSUKASA2, Nikolay P. KALMYKOV3, Evgeny N. MASCHENKO4, Masanaru TAKAI5 1Japan Monkey Centre, 26 Kanrin, Inuyama, Aichi, 484-0081 Japan 2Department of Zoology, Kyoto University, Kyoto, Japan 3Southern Scientific Center, Russian Academy of the Sciences, Rostov-on-Don, Russia 4Paleontological Institute, Russian Academy of the Sciences, Moscow, Russia 5Primate Research Institute, Kyoto University, Inuyama, Japan

Received 8 October 2006; accepted 22 February 2007

Abstract Parapresbytis eohanuman is a colobine known from two middle Pliocene localities south- east of Lake Baikal, northern East Asia. This study examined the morphology of postcranial speci- mens, a distal humerus and an ulna, of Parapresbytis. A total of 18 and 13 linear measurements were taken from the humerus and the ulna, respectively, and compared with those of extant and European fossil colobines using principal components analysis. The distal humeral specimen of Parapresbytis is slightly larger than those of male Semnopithecus and Nasalis, while the ulnar specimen is much larger than those of extant colobines and is nearly as large as that of a male Papio ursinus. Morphologically, the distal humeri and ulnae of terrestrial colobines such as Semnopithecus, Dolichopithecus, and Meso- pithecus can be distinguished from those of arboreal colobines. The morphology of the Parapresbytis elbow is within the range of the arboreal colobines, contradicting previous suggestions that this genus is terrestrially adapted and is phylogenetically close to Dolichopithecus. Because the arboreally adapted elbow is shared by most extant colobines, the morphology of the elbow does not provide evi- dence for phylogenetic proximity between Parapresbytis and a particular taxon of arboreal colobine such as Rhinopithecus. The elbow morphology suggests that Parapresbytis was adapted to arboreal locomotion as much as the extant arboreal colobines are. This is congruent with the paleoenvironmen- tal evidence, which indicates the presence of forests in the Lake Baikal area during the middle Pliocene.

Key words: Parapresbytis eohanuman, Colobinae, Pliocene, Asia, evolution

Introduction northern distribution of all the colobines, and its occurrence is peculiarly isolated from the other Neogene primate local- The distribution of colobines is today limited to Southeast ities in Eurasia (Jablonski, 2002; Fortelius, 2003). The phy- Asia, South Asia, and equatorial Africa, but colobines previ- logenetic position of the genus and the nature of its adapta- ously had a much wider geographical distribution. Meso- tion to such high latitudes are still the subject of debate pithecus and Dolichopithecus were widespread throughout (Delson, 1988, 1994; Kalmykov and Maschenko, 1992, Europe and West Asia during the late Miocene and the 1995; Jablonski, 2002; Kalmykov et al., 2005; Maschenko, Pliocene (Figure 1) (Delson, 1994; Fortelius, 2003). In East 2005). Asia, Parapresbytis is known from the middle Pliocene of The Siberian fossil colobine was first discovered at Transbaikalia, Siberia (Borisoglebskaya, 1981; Kalmykov Shamar in Mongolia (50°06′14″N, 106°11′30″E: Fortelius, and Maschenko, 1992, 1995), a fossil from the late Pliocene 2003). Based on a mandibular specimen, a new species, of Japan has been assigned to Dolichopithecus (Delson, Presbytis eohanuman Borisoglebskaya, 1981, was estab- 1994; Iwamoto et al., 2005), and Rhinopithecus existed in lished. Later, maxillary and fragmentary frontal specimens central China during the Pleistocene (Figure 1) (Jablonski, were found at Udunga in Russia (51°8′23″N, 105°58′55″E: 2002). The adaptability of cercopithecid monkeys in gener- Erbajeva et al., 2003). The complete dentition is known (i.e. al, and colobines in particular, has been briefly discussed in I1/–M3/ for the Udunga materials and i/1–m/3 for the Jablonski (2005). Parapresbytis from Siberia has the most Shamar materials), and based on their morphology and size, the materials from the two localities are considered to be- * Corresponding author. e-mail: [email protected] long to the same species (Kalmykov and Maschenko, 1992, phone: +81-568-61-2327; fax: +81-568-62-6823 1995; Maschenko, 2005). Kalmykov and Maschenko (1992) Published online 25 May 2007 erected a new genus, Parapresbytis, for the species. in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.061008 Maschenko (2005) and Kalmykov et al. (2005) suggested

© 2007 The Anthropological Society of Nippon 107 108 N. EGI ET AL. ANTHROPOLOGICAL SCIENCE

that Parapresbytis is a member of Rhinopithecomorpha. On the other hand, Jablonski (2002) noted that Parapresbytis has dental and postcranial similarities to Semnopithecus, Na- salis, Pygathrix, and Rhinopithecus. Delson (1988, 1994) proposed, in contradistinction to the above, that the P. eoha- numan materials are not significantly different from those of Dolichopithecus and that the species should therefore be placed in Dolichopithecus. The known materials of Parapresbytis also include post- cranial elements: a distal humerus and an incomplete ulna lacking its distal portion and the olecranon process (Figure 2). A range of inferences on the morphologies of these materials have been drawn by different researchers. In addition to the dentognathic materials, Delson (1988, 1994) described the morphology of the postcranial materials to be quite similar to those of Dolichopithecus, which is the most Figure 1. Locations of Udunga and Shamar, where Parapresbytis terrestrially adapted colobine known. Jablonski (2002) as- eohanuman has been discovered. Other fossil colobine localities are signed the substrate preference of Parapresbytis as “?terres- indicated in grey (from Delson, 1994). trial”. Maschenko (2005) suggested that Parapresbytis is ar- boreally adapted based on postcranial comparisons with Macaca and Papio.

Figure 2. Postcranial specimens of Parapresbytis eohanuman. Left distal humerus (PIN 3381-210) in anterior (a), medial (b), posterior (c), lateral (d), and distal (e) views. Right ulna (PIN 3381-211) in anterior (f), medial (g), posterior (h), lateral (i), and proximal (j) views. Vol. 115, 2007 DISTAL HUMERUS AND ULNA OF PARAPRESBYTIS 109

Table 1. Comparative materials Species Sample size Locomotion Extant Asian colobines Rhinopithecus roxellana male 2, female 2 arboreal Pygathrix nemaeus male 1, female 1 arboreal Simias concolor male 1 arboreal Nasalis larvatus male 2, female 3 arboreal Semnopithecus entellus male 3, female 4 semi-terrestrial Trachypithecus cristatus male 3, female 4 arboreal Trachypithecus francoisi female 1 arboreal Trachypithecus obscurus male 1, female 2 arboreal Trachypithecus pileatus male 1 arboreal Presbytis melalophus female 1 arboreal Extant African colobines Colobus angolensis male 2, female 2 arboreal Colobus guereza male 3, female 2 arboreal Procolobus verus male 1, female 1 arboreal Mio–Pliocene European colobines Mesopithecus pentelicus humerus 4, ulna 1 semi-terrestrial Mesopithecus monspessulanus ulna 1 semi-terrestrial Dolichopithecus ruscinensis humerus 2 semi-terrestrial

This study aims to clarify the characteristics of the elbow Table 2. List of measurements and values for morphology of Parapresbytis in comparison with those of Parapresbytis eohanuman (mm) other arboreal and terrestrial colobines. Then, implications Distal humerus for the phylogenetic position of Parapresbytis and the corre- 1 minimum anteroposterior diameter of the distal 12.8 spondence between the reconstructed locomotor adaptation part of the shaft and the paleoenvironmental evidence are discussed. 2 biepicondylar width 40.7 3 width of the lateral epicondyle and the articular 34.5 surface Materials and Methods 4 articular width 29.9 The distal humerus (PIN 3381-210) and the ulna (PIN 5 capitular height 15.4 6 capitular anteroposterior depth 10.5 3381-211) of Parapresbytis from the Shamar site are stored 7 width of the capitular and the trochlear gutter 11.9 in the Paleontological Institute, Russian Academy of Scienc- 8 capitular width 17.4 es, Moscow. Because taking the fossils outside Russia is dif- 9 trochlear width 12.4 ficult, the measurements and morphological observations 10 width of the trochlear groove distally 18.9 were carried out using casts of the specimens. 11 maximum trochlear height 17.1 In order to evaluate the morphological characteristics of 12 minimum trochlear diameter 15.7 13 coronoid fossa width 9.1 the Parapresbytis elbow, it was compared with those of ex- 14 radial fossa width 11.3 tant and extinct colobines (Table 1). All the compared spec- 15 olecranon fossa height 11.5 imens are adults, with closed epiphyses at the distal humerus 16 olecranon fossa width 15.4 and the proximal ulna. The extant colobine sample includes 17 anteroposterior thickness of the medial epi- 21.3 a total of nine genera with 13 species and 43 individuals. The condyle smallest species in the sample is Procolobus verus, which 18 anteroposterior thickness of the lateral epi- 23.6 condyle has a female mean body mass of 4.2 kg (Smith and Jungers, 1997). The largest species is Semnopithecus entellus, which Proximal ulna has a male body mass of up to 23.6 kg (Macdonald, 2001), 1 trochlear notch height 20.0 and Nasalis larvatus, which has a male mean body mass of 2 anteroposterior depth at the olecranon 22.2 20.4 kg (Smith and Jungers, 1997). The fossil colobine sam- 3 anteroposterior depth at the olecranon beak 28.9 ple includes Dolichopithecus and Mesopithecus from the 4 anteroposterior depth at the sigmoid notch 17.8 Mio-Pliocene of Europe. No well-preserved ulnae from 5 anteroposterior length of the coronoid process 17.1 6 anteroposterior depth at the coronoid process 32.6 Dolichopithecus were available for this study. 7 width of the olecranon beak 18.3 Among the comparative taxa, Dolichopithecus, Mesopith- 8 width of the sigmoid notch 14.2 ecus, and Semnopithecus have been suggested to be adapted 9 width of the inferior part of the trochlear notch 25.3 to semi-terrestrial locomotion (Jablonski, 2002), while the 10 width of the coronoid process 14.1 rest are primarily arboreal. We first examined whether or not 11 width of the radial notch 13.9 these two groups of colobines, arboreal and semi-terrestrial, Ulnar mid-shaft can be distinguished one from the other. We then evaluated 12 anteroposterior diameter 15.7 the similarities of Parapresbytis to these two groups. 13 mediolateral diameter 13.9 The extant species were examined at the Japan Monkey 110 N. EGI ET AL. ANTHROPOLOGICAL SCIENCE

specimen were transformed into the natural logarithmic scale. Comparisons were carried out by means of principal components analysis (PCA) performed on the covariance matrices (Wilkinson, 2002). Because the humeri and the ul- nae are not associated in the fossil colobine specimens, the PCA was conducted separately for the humeral and ulnar measurements.

Figure 3. Schematic explanation of measurements on the distal Results humerus (a) and the proximal ulna (b). See Table 2 for the list of vari- ables. In the PCA of colobine distal humeri and ulnae, the first three principal components (PCs) contribute more than 90% of the total variance. The loading values, eigenvalues (vari- Centre (Inuyama, Aichi, Japan) and Department of Mam- ances), and percentage variances of the first, second, and malogy, United States National Museum of Natural History third PCs are shown in Table 3. (Washington, DC). The fossil colobines were examined at The first PC in an analysis based on covariances between the Département Histoire de la Terre, Muséum National linear measurements is generally considered as an indicator d’Histoire Naturalle (Paris, France) and the Laboratoire de of size. The overall sizes of the distal humerus and the ulna Paléntologie, Université Montpellier II (Montpellier, were evaluated using the first PC scores (Figure 4). Percent- France). age variances of the first PC are 80% and 85% for the distal The humeral and ulnar specimens of Parapresbytis humeral measurements and for the ulnar measurements, re- (Figure 2) are incomplete; the preserved part of the humerus spectively (Table 3). In terms of the size of the distal hume- is limited to the distal 30–40%, the olecranon of the ulna is rus (Figure 4a), Parapresbytis is similar to a larger male broken, and the ulnar shaft is broken at a point proximal to Semnopithecus and Dolichopithecus. It is slightly larger than the pronator crest. Because the entire lengths of the two ele- the largest male Nasalis (associated body mass, 22 kg) and ments are unknown, morphological comparisons among Rhinopithecus (male average body mass, 17.9 kg: Smith and colobines were carried out using linear measurements of the Jungers, 1997). In terms of ulna size (Figure 4b), Parapres- distal humerus, the proximal ulna, and the ulnar shaft. bytis is larger than any extant colobine. The size of the prox- A total of 18, 11, and 2 measurements (Table 2 and imal ulna of Parapresbytis is similar to that of male Papio Figure 3) were taken on the distal humerus, the proximal ul- ursinus (species mean male body mass = 29.8 kg: Smith and na, and the ulnar mid-shaft, respectively. These measure- Jungers, 1997) although the latter species is not included in ments were modified after Birchette (1982) and Harrison the quantitative comparison (Figure 5). (1982). Measurement values for Parapresbytis are shown in The size difference between Parapresbytis and extant ar- Table 2. These measurements were taken using calipers to boreal colobines is more obvious in the ulna than in the dis- the nearest tenth of a millimeter. The measurements of each tal humerus. The humeral specimen (PIN 3381-210) of

Table 3. Loadings of the first, second, and third principal components (PCs) of the distal humeral and the ulnar measurements (eigenvalue and percent variance of each PC are indicated in the last two rows) 1st PC 2nd PC 3rd PC 1st PC 2nd PC 3rd PC Distal humerus Proximal ulna and ulnar shaft Measurement 1 0.201 −0.021 −0.030 0.178 −0.048 0.040 2 0.162 0.010 0.012 0.158 −0.006 −0.037 3 0.179 0.011 0.007 0.197 0.019 −0.011 4 0.181 0.017 0.014 0.211 0.062 0.007 5 0.190 0.002 −0.021 0.192 0.012 0.015 6 0.195 0.060 0.019 0.196 0.026 0.017 7 0.183 0.019 0.018 0.187 −0.009 −0.031 8 0.184 0.030 0.013 0.199 0.012 −0.009 9 0.156 0.010 0.013 0.182 −0.027 −0.002 10 0.178 −0.008 −0.024 0.171 −0.017 −0.079 11 0.203 −0.054 −0.081 0.156 −0.138 0.018 12 0.194 0.016 −0.028 0.178 0.050 0.014 13 0.133 −0.161 0.093 0.217 0.023 0.043 14 0.119 0.050 0.028 15 0.182 0.047 0.082 16 0.175 −0.005 0.040 17 0.216 −0.051 −0.061 18 0.190 0.015 −0.029 eigenvalue 0.586 0.043 0.033 0.456 0.031 0.013 %variance 80.5 5.9 4.5 84.6 5.7 2.5 Vol. 115, 2007 DISTAL HUMERUS AND ULNA OF PARAPRESBYTIS 111

The second and subsequent PCs are considered to reflect variation in shape after removing the size factor. The com- parison of distal humeral shapes among colobines is summa- rized in a graph of the third PC score versus the second (Figure 6). Along the second PC, large positive loadings are found for capitular anteroposterior depth, radial fossa width, olecranon fossa height, and capitular width, while large negative loadings are found for coronoid fossa width, trochlear height, anteroposterior depth of the medial epi- condyle, and anteroposterior diameter at the distal shaft (Table 3). The loadings of the third PC are positive and large for coronoid fossa width, olecranon fossa height, and radial fossa width, and negative and large for trochlear height, medial epicondyle depth, anteroposterior diameter at distal shaft, lateral epicondyle depth, minimum trochlear diameter, trochlear width at the distal aspect, and capitular height (Table 3). The three terrestrial colobines, Semnopithecus, Mesopith- ecus, and Dolichopithecus, have low scores along both sec- ond and third PCs (Figure 6). Their distal humerus is charac- terized by a high trochlea and capitulum, anteroposteriorly thick medial and lateral condyles, an anteroposteriorly elon- gated cross-section at the distal shaft, and a wide trochlear groove relative to the articular width. These terrestrial colobines are mostly separated from the other colobines (se- lected species are shown in Figure 5b–e). The arboreal taxa overlap with one another except that the Nasalis individuals tend to exhibit higher scores along the second and third PCs. The arboreal colobines generally have a mediolaterally wide distal humeral articulation. Their capitulum is wide relative to the whole articulation, and its shape is round. The olecra- non fossa is superoinferiorly large, so that a long olecranon of the ulna can fit. In Nasalis, the trochlear rim is low, and the relatively large capitulum expands laterally. A humeral trochlea with well-developed lateral and medi- al rims and a wide trochlear groove are suggested to increase stability, especially in a semi-flexed posture (Rose, 1988, 1993; Harrison, 1989; Nakatsukasa, 1994). Thus, the tro- chlea of the terrestrial colobines is more efficient in parasag- ittal movement of the elbow than that of the arboreal colobines. In contrast, development of the trochlear rim is weak, and the capitulum is round and expands laterally in the arboreal colobines, particularly in Nasalis. These mor- phologies allow rotational movements of the radius during elbow flexion (Rose, 1988, 1993; Harrison, 1989; Figure 4. Comparison of distal humeral and ulnar sizes based on Nakatsukasa, 1994). the first principal component scores. Genera are indicated along the Parapresbytis is within the range of the arboreal rather horizontal axis. Symbols: square, male; circle, female; cross, fossil. than of the terrestrial colobines. The medial rim of the tro- Trachypithecus, Colobus, and Mesopithecus include multiple species. chlea is clear in Parapresbytis, but this morphology is prob- ably related to its large body size (Rose, 1993). The trochlear groove and the capitular tail can increase the contact area Parapresbytis was previously thought to associate with the with the rims of the radial head, and will enhance the stabil- ulnar specimen (PIN 3381-211), but the comparisons con- ity between the large round capitulum and the radial head ducted here suggest that these two elements belonged to dif- during the rotation of the radius (Rose, 1993). It is concluded ferent individuals. The humerus belonged to an individual that Parapresbytis shares a distal humeral morphology with with a body size of a male Nasalis, while the ulna belonged arboreal colobines such as Colobus, Procolobus, Trachy- to another individual with a body size of a male Papio. This pithecus, Pygathrix, Simias, and Rhinopithecus. size difference can be regarded as evidence of intraspecific Ulnar shape does not clearly differentiate the terrestrial variation of body size in Parapresbytis as in extant colobine from the arboreal colobines (Figure 7). The loadings of the species. second PC are positively large for anteroposterior depths at 112 N. EGI ET AL. ANTHROPOLOGICAL SCIENCE

Figure 5. Comparison of Parapresbytis with other colobines and Papio. Left distal humeri in anterior view (a–f) and right proximal ulnae in lateral view (g–l). Parapresbytis (a, g), Trachypithecus (b, h), Rhinopithecus (c, i), Semnopithecus (d, j), Dolichopithecus (e), Mesopithecus (k), and Papio (f, l). All to the same scale.

Figure 7. Projection of colobine ulnar morphology onto the sec- ond and third principal component shape plane. See Figure 6 for leg- ends.

Figure 6. Projection of colobine distal humeral morphology onto diameter of the ulnar shaft and height of the trochlear notch, the second and third principal component shape plane. while loadings are negative and large for the widths of the sigmoid notch and the olecranon beak and for the anteropos- terior depth at the olecranon (Table 3). the sigmoid notch, at the coronoid process, and at the olecra- Mesopithecus is distinguished from the other colobines in non beak and for the anteroposterior and mediolateral dia- having higher second PC scores. The other terrestrial meters of the ulnar shaft. The loadings of the second PC are colobine, Semnopithecus, also tends to indicate high second negative and large for the widths of the radial notch, the PC scores, although the range overlaps with that of the arbo- coronoid process, and the inferior part of the trochlear notch, real colobines. In the ulna of these terrestrial colobines, the and for the height of the trochlear notch (Table 3). Along the medial surface of the proximal trochlea and the lateral sur- third PC, loadings are positive and large for the mediolateral face of the distal trochlea are inclined. The diameter of the Vol. 115, 2007 DISTAL HUMERUS AND ULNA OF PARAPRESBYTIS 113 trochlear notch is small. The anteroposterior depths are large terrestrial and arboreal species may have become clearer at the olecranon beak and the sigmoid notch. The ulnar shaft than it currently is. The relatively large anteroposterior is robust. Among the arboreal colobines, Nasalis, Simias, depths at the olecranon beak and at the sigmoid notch in Me- Pygathrix, and Rhinopithecus tend to have lower second PC sopithecus and Semnopithecus seem to reflect their posteri- scores than Trachypithecus, Colobus, and Procolobus, with orly flexed olecranon process. a large radial notch, a wide distal trochlea, and a large In the comparison of the ulna, Parapresbytis is plotted in trochlear notch. Mesopithecus, Pygathrix, Rhinopithecus, the middle of the range of the arboreal colobines; thus, the Procolobus, and Presbytis have relatively low third PC scores, ulnar shape of Parapresbytis is equally similar to those of which seem to be associated with a wide sigmoid notch and the arboreal colobines and differs from that of the terrestrial a wide olecranon beak relative to other measurements. colobines such as Semnopithecus and particularly Mesopith- There appear to be some relationships between the above ecus (selected species are shown in Figure 5h–k). summarized ulnar and distal humerus morphologies. The In sum, the major difference between the distal humerus medial and lateral rims of the humeral trochlea are well-de- and ulna of Parapresbytis and those of the other colobines is veloped in terrestrial colobines, and these surfaces fit with in terms of size. The smaller individuals of Parapresbytis the inclined medial surface of the proximal trochlea and the probably had a body mass similar to that of the largest extant inclined lateral surface of the distal trochlea of the ulna, re- colobines, while the larger individual of Parapresbytis was spectively (Rose, 1993). The ulnar trochlear notch diameter much larger. The distal humeral and ulnar morphologies of is small so that the ulnar trochlea fits to the deep humeral tro- Parapresbytis are distinct from those of the terrestrial chlear groove, enhancing stability during parasagittal move- colobines and similar to those of the arboreal colobines, sug- ment. Load transmission through the ulna increases in the gesting that Parapresbytis was as arboreally adapted as are forearm of the terrestrial forms, so the ulna is robust in the extant arboreal colobines. The elbow morphologies of extant terrestrial colobines. In arboreal colobines, the capitulum arboreal colobines are similar, with the exception of Nasalis. and the radial head are large (Rose, 1993), which is reflected Parapresbytis is equally similar to the extant arboreal in the large radial notch of the proximal ulna. The wide ulnar colobines except Nasalis. trochlea contacts with the cylindrical humeral trochlea, al- lowing some rotational movement in the elbow. Discussion The orientation and relative length of the olecranon pro- cess, the insertion for m. triceps brachi, are one of the fea- Elbow morphology and phylogenetic hypotheses of Para- tures that distinguish terrestrial from arboreal animals (Jolly, presbytis 1967; Birchette, 1982; Rose, 1993). Terrestrial species gen- Elbow morphology adaptations (arboreal and terrestrial) erally have a posteriorly flexed and shorter olecranon pro- were overplotted on colobine cladograms in order to clarify cess, allowing a greater range of elbow extension, while ar- their distributions in an evolutionary context (Figure 8). The boreal species tend to have a straight and long olecranon phylogenetic relationships within Colobinae are poorly re- process, gaining a longer lever arm for the main elbow ex- solved, but at least many researchers agree with the dichoto- tensor (Jolly, 1967; Birchette, 1982; Rose, 1993). The ole- my between extant Asian and African genera (e.g. Strasser cranon process in the Parapresbytis specimen is incomplete, and Delson, 1987; Delson, 1994; Disotell, 2000). Molecular so that we could not include measurements of this skeletal data suggest four old lineages among the extant Asian part in the comparison. If comparisons of the olecranon mea- colobines (i.e. Semnopithecus, Trachypithecus, Rhinopithe- surements had been available, differentiation between the cus/Pygathrix, and Nasalis), leaving an unsolved multitomy

Figure 8. Distribution of elbow morphology types in the colobine phylogenetic tree. The European fossil colobines are placed next to the Asian colobines (a) or as sister groups of the crown colobines (b). Elbow types are: terrestrial (grey), arboreal (black; except Nasalis), and Nasalis (dark grey). Parapresbytis, having an arboreal type elbow, can be inserted onto any branch indicated in black without increasing the number of steps of the tree. Thick branches have been supported by the molecular studies, and the thin branches connecting with the thick branches are based on morphological studies. 114 N. EGI ET AL. ANTHROPOLOGICAL SCIENCE at the base of the Asian colobines (Disotell and Stewart, data The elbow morphology examined in the present study was shown in Fleagle, 1999; Disotell, 2000). The grouping of demonstrated to be similar among the extant arboreal Rhinopithecus and Pygathrix has been supported by some colobines, with the exception of Nasalis. Likewise, Para- molecular studies (Disotell, 2000 and references therein). presbytis was found to be equally similar to all the extant ar- Presbytis has been suggested to be close to either Semnop- boreal colobines examined except Nasalis. Thus, Parapres- ithecus or Trachypithecus, while Simias is traditionally clas- bytis can be inserted in any parts of the arboreal branches of sified with Nasalis based on morphological studies (Strasser the colobine cladogram (black branches of Figure 8) without and Delson, 1987). Because most of the extant colobines increasing the number of homoplasies of the phylogenetic have the arboreal type of distal humerus and ulna, the arbo- tree. Although Parapresbytis has been claimed to be closer real type (indicated as black branches in Figure 8) is the like- to some arboreal taxa such as Presbytis (Borisoglebskaya, ly primitive condition for the crown colobines. 1981), Rhinopithecus (Jablonski. 2002; Maschenko, 2005; Extinct European colobines, Mesopithecus and Dolichop- Kalmykov et al., 2005), and Pygathrix (Jablonski. 2002), ithecus, have been suggested to be closer to the Asian than to based on dentognathic morphologies and the robustness of the African colobines (Figure 8a) (Delson, 1994; Jablonski, the skeletal materials, the elbow morphology does not sug- 1998). In this case, the likely primitive condition for all gest phylogenetic closeness between Parapresbytis and any colobines is also the arboreal type. On the other hand, a re- particular arboreal colobine. cent molecular study estimated the time of the Asian–Afri- can colobine split as 10.9 Ma (with a 95% confidence inter- Paleoenvironment and arboreal adaptation of Parapres- val of 12.3–9.6 Ma) (Raaum et al., 2005). This is in the bytis chronological range of Mesopithecus, the fossil record of The results of this study suggested that the elbow of Para- which begins in MN 9 (11.2–9.5 Ma) (Jablonski, 2002; presbytis is adapted to arboreal locomotion. This implies Fortelius, 2003), suggesting that Mesopithecus may be too that Parapresbytis lived in a forested environment. Thus, it old to be a member of the Asian clade. Alternatively, the Eu- is worth examining the paleoenvironmental data to evaluate ropean fossil genera are placed as sister groups of the crown whether or not the presumed locomotor habit of Parapresby- colobines (Figure 8b). Given this tree topology, the terrestri- tis is congruent with its surroundings. al type becomes the likely primitive condition for all Table 4 lists the mammalian taxa of the Udunga and colobines, because the outgroup (cercopithecines) is gener- Shamar faunas (Devyatkin and Zazhigin, 1974; Zazhigin, ally thought to be more terrestrially adapted than colobines 1989; Kalmykov, 1992; Erbajeva et al., 2003 and cited there- (Fleagle, 1999). in; Fortelius, 2003). The Udunga fauna is divided into three Parapresbytis has been suggested to be phylogenetically units, but only the mammalian species from the middle unit, close to Dolichopithecus (Delson, 1988, 1994). However, where Parapresbytis was recovered, are listed. The mam- the results of the present study indicate that the elbow mor- mals co-occuring with Parapresbytis include 33 genera and phology of Parapresbytis lacks the terrestrial adaptations 38 species from Udunga and 34 genera and 37 species from seen in Dolichopithecus. The fossil record of Dolichopithe- Shamar. Simpson’s index of faunal resemblance between the cus begins in the late Miocene (Fortelius, 2003). If Dolicho- two faunas is 42% at the generic level and 27% at the specif- pithecus is the closest relative of Parapresbytis, Mesopithe- ic level. Both faunas yield lagomorphs, rodents, carnivorans, cus and Dolichopithecus must have acquired their terrestrial artiodactyls, perissodactyls, and a primate. The major taxo- adaptations independently (Figure 8a), and Parapresbytis nomic differences between the two faunas are in insectivores must have split from Dolichopithecus at the very beginning and ungulates; insectivores are known only from Shamar of this lineage. If Dolichopithecus and Mesopithecus are and ungulates are more abundant in Udunga than in Shamar. considered as sister groups of the crown colobines The former fauna also includes large ungulates such as a (Figure 8b), the arboreally adapted elbow is considered to be proboscidean and a rhinoceros. an apomorphy that appeared at the root of the crown Among herbivorous mammals, hypsodont grazers are colobines. If Dolichipithecus is the closest relative of Para- generally considered to be associated with an open habitat, presbytis, and if this clade is a sister group of the crown while mesodont or brachyodont herbivores live in more colobines, Parapresbytis must have acquired arboreal adap- closed habitats (e.g. Jernvall and Fortelius, 1996; Mendoza tations independently from the crown colobines. Thus, the et al., 2002; Fortelius, 2003). In the Udunga and Shamar fau- comparison of the elbow morphologies suggests that group- nas, Ovis and Hipparion are hypsodont grazers, Gazella, Ax- ing Parapresbytis with Dolichopithecus increases the is, Orchoceros, and Stephanorhinus are mesodont, and homoplasies of arboreal-terrestrial transitions, thereby odocoileine cervids and Zygolophodon are brachyodont lending support to the notion that Dolichopithecus is unre- browsers (based on data from Fortelius, 2003); thus, both lated to Parapresbytis. grassland-living and forest-living ungulates are known in Parapresbytis has been also suggested to have some these faunas. similarities to Semnopithecus (Borisoglebskaya, 1981; Among the small herbivores of the two faunas, all lago- Jablonski, 2002). The oldest fossil record for Semnopithecus morphs are hypsodont grazers (data from Fortelius, 2003). comprises dentognathic and talar specimens from the Plio– Among the rodents, possible grazers with hypsodont teeth Pleistocene deposits of the Siwaliks (Jablonski, 2002). If we include a dipodine dipodid (Allactaga), alvicoline murids assume that Parapresbytis split from Semnopithecus before (except Mimomys cf. minor), and a myospalacine murid the latter acquired terrestrial adaptations, Semnopithecus be- (Prosiphneus). Earlier forms of Micromys (alvicoline murid) comes a candidate for the closest relative of Parapresbytis. had not developed strong hypsondonty (Lindsay, 2003), and Vol. 115, 2007 DISTAL HUMERUS AND ULNA OF PARAPRESBYTIS 115

Table 4. Mammals co-occurring with Parapresbytis in the Udunga and Shamar faunas (Devyatkin and Zazhigin, 1974; Zazhigin, 1989; Kalmykov, 1992; Erbajeva et al., 2003 and cited therein; Fortelius, 2003) UDUNGA SHAMAR Lagomorpha Insectivora Leporidae Erinaceidae Hypolagus multiplicatus Erinaceus indet. Hypolagus transbaikalicus Soricidae Ochotonidae Soricinae Beremendia indet. Ochotona aff. sibirica Soriculini indet. Ochotona indet. (middle size) Neomys indet. Ochotonoides complicidens Sorex indet. Ochotona aut Ochotonoides sp. Lagomorpha Rodentia Leporidae Castoridae Hypolagus indet. Castor indet. Ochotonidae Muridae Ochotona cf. gromovi Arvicolinae Mimomys cf. minor Ochotona cf. intermedia Promimomys cf. gracilis Ochotona minor Promimomys cf. stehlini Ochotonoides cf. complicidens Villanyia ex gr. eleonorae Rodentia Cricetinae Cricetinus cf. varians Castoridae Gromovia daamsi Sinocastor cf. zdanskyi Kowalskia sp. Dipodidae Murinae Orientalomys cf. sibiricus Dipodinae Allactaga cf. saltator Myospalacinae Prosiphneus praetingi Sicistinae Sicista pliocaenica Primates Muridae Cercopithecidae Arvicolinae Mimomys cf. hintoni coelodus Parapresbytis eohanuman Promimomys indet. Carnivora Synaptomys mogoliensis Ailuridae Villanyia eleonorae Ailurus sp. Cricetinae Cricetulus cf. barabensis Parailurus sp. Murinae Chardinomys sibiricus Canidae Micromys indet. Nyctereutes indet. Myospalacinae Prosiphneus cf. praetingi Felidae Primates Felinae Lynx issiodorensis Cercopithecidae Machaerodontinae Homotherium crenatidens Parapresbytis eohanuman Hyaenidae Carnivora Pliocrocuta perrieri Canidae Mustelidae Nyctereutes megamastoides Guloninae Gulo cf. minor Vulpes indet. Melinae Arctomeles sp. Felidae Parameles suillus Achinonychinae Acinonyx indet. Ursidae Felinae Lynx issiodorensis Ursus ruscinensis minimus Pantherinae Panthera indet. Artiodactyla Viretailurus indet. Bovidae Hyaenidae Antilopinae Antilospira zdanskyi Chasmaporthetes lunensis Gazella sinensis Pachycrocuta brevirostris Caprinae Ovis indet. Mustelidae Cervidae Melinae Parameles suillus Cervinae Axis shansius Mustelinae Mustela indet. Orchonoceros gromovi Pannonictis pachygnatha Odocoileinae Capreolus constantini Artiodactyla “Alcinae” indet. Bovidae Perissodactyla Antilopinae Gazella sinensis Equidae Cervidae Hipparion houfenense Cervinae Orchonoceros gromovi Hipparion tchicoicum Perissodactyla Rhinocerotidae Equidae Stephanorhinus indet. Hipparion houfenense Proboscidea Hipparion tchicoicum Mammutidae Zygolophodon indet. 116 N. EGI ET AL. ANTHROPOLOGICAL SCIENCE

Mimomys cf. minor from Udunga is brachyodont (data from Brigitte Senut at the Département Histoire de la Terre, Fortelius, 2003). Erbajeva et al. (2003) mentioned that crice- Muséum National d’Histoire Naturalle (Paris, France), and tine murids from Udunga, such as Cricetinus, Gromovia, Jean-Jacque Jaeger and Bernard Marandat at the Laboratoire and Kowalskia, do not exhibit high hypsodonty. Sicista (si- de Paléntologie, Université Montpellier II (Montpellier, cistine dipodid), Cricetulus (cricetine murid), and Micromys France). Financial support was provided by the MEXT (murine murid) from Shamar are also brachyodont browsers Grant-in-Aid for JSPS Fellows (No. 15004748 to Egi), Sci- (data from Fortelius, 2003). Although castorids have hyps- entific Research B (No. 16370103 to Prof. N. Shigehara, odont teeth, they are browsers with a semi-aquatic locomo- Kyoto University), Overseas Scientific Research (No. tion (Fortelius, 2003) that live in damp environments 09041161 to Prof. N. Shigehara, Kyoto University; No. (Macdonald, 2001). Similar to the ungulates, the small her- 14405019 to Takai), and the 21st Century COE Program bivores of the Udunga and Shamar faunas include both (A14 to Kyoto University), and the JSPS Bilateral Joint hypsodont and brachyodont species. Projects with RFBR (to M. Takai). The paleoenvironments of Udunga and Shamar can also be inferred from locomotor adaptations seen in the insecti- References vores and carnivorans. The Shamar insectivores include two semi-aquatic species, Neomys and Nectogalini (Beremendia) Birchette M.G. (1982) The postcranial skeleton of Paracolobus (Macdonald, 2001), indicating that some water systems are chemeroni. Ph.D. dissertation, Harvard University, Cam- represented at Shamar. Among the carnivorans, Acinonyx bridge, MA. Borisoglebskaya M.B. (1981) A new species of monkey (Mamma- and hyaenids are fast-running taxa that are presently distrib- lia, Primates) from the Pliocene of Northern Mongolia. Trudy uted in open environments (Nowak, 1991; Macdonald, Sovmestnoj Sovetsko-Mongol’skoj Paleontologicekoj Eks- 2001). Ailurids, Lynx, Gulo, and Ursus are scansorial pedicii, 15: 95–108, 125 (in Russian with English summary). (VanValkenburgh, 1987); thus, they require a forested envi- Delson E. (1988) Catarrhini. In: Tattersall I., Delson E., and Van ronment. Overall, insectivores and carnivorans contain ele- Couvering J.A. (eds.), Encyclopedia of Human Eevolution ments of both forested/humid and dry, open environments. and Prehistory. Garland, New York, pp. 111–116. In sum, the presence of forested environments at Udunga Delson E. (1994) Evolutionary history of the colobine monkeys in paleoenvironmental perspective. In: Davies A.G. and Oates and Shamar is supported by the co-occurrence of browsing J.F. (eds.), Colobine Monkeys: Their Ecology, Behaviour, and herbivores, semi-aquatic mammals, and scansorial car- Evolution. Cambridge University Press, Cambridge, pp. 11– nivorans, although the environment probably also contained 43. some patches of grassland. Thus, the arboreal adaptation Devyatkin E.V. and Zazhigin V.S. (1974) Eopleistocene deposits recognized in the postcrania of Parapresbytis is congruent and new mammalian find-localities of Northern Mongolia. c with the paleoenvironment of the localities. Trudy Sovmestnoj Sovetsko-Mongol’skoj Paleontologi ekoj Ekspedicii, 1: 357–363, 369 (in Russian with English sum- Müller et al. (2001) estimated climate changes in the Lake mary). Baikal area using mineralogical contents and the relative Disotell T.R. (2000) The molecular systematics of the Cercopithe- amounts of diatoms in drilling cores from sediments of the cidae. In: Whitehead P.F. and Jolly C.J. (eds.), Old World lake. They concluded that a major climatic change occurred Monkeys. 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(1982) Small-bodied apes from the Miocene of East It has been suggested that the European colobines accom- Africa. Ph.D. dissertation, University of London. plished their northern invasion with their terrestrial adapta- Harrison T. (1989) New postcranial remains of Victoriapithecus tions. In contrast, as indicated in this study, Parapresbytis from the Middle Miocene of Kenya. Journal of Human Evo- lacks terrestrial adaptations. It is reasonable to consider that lution, 18: 3–54. the northern distribution of Paprapresbytis was achieved via Iwamoto M., Hasegawa Y., and Koizumi A. (2005) A Pliocene a widespread forested habitat in East Asia during the middle colobine from the Nakatsu Group, Kanagawa, Japan. Anthro- pological Science, 113: 123–127. Pliocene and that the genus kept its arboreal adaptations Jablonski N.G. (1998) The evolution of the doucs and snub-nosed from the ancestor of the crown colobines. monkeys and the question of the phyletic unity of the odd- nosed colobines. In: Jablonski N.G. (ed.), The Natural History of the Doucs and the Odd-nosed Monkeys, World Scientific, Acknowledgments Singapore, pp. 13–41. Access to the specimens was provided by the following Jablonski N.G. (2002) Late Neogene cercopithecoids. In: Hartwig W.C. (ed.), The Primate Fossil Record. Cambridge University personnel: Linda Gordon at the Department of Mammalogy, Press, Cambridge, pp. 255–299. United States National Museum of Natural History (Wash- Jablonski N.G. (2005) Primate homeland: forests and the evolution ington, DC), Tomo Takano at the Japan Monkey Centre of primates during the Tertiary and Quaternary in Asia. (Inuyama, Aichi, Japan), Pascual Tassy, Claire Sagne, and Anthropological Science, 113: 117–122. Vol. 115, 2007 DISTAL HUMERUS AND ULNA OF PARAPRESBYTIS 117

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