Primates (2010) 51:23–35 DOI 10.1007/s10329-009-0161-2

ORIGINAL ARTICLE

Locomotor evolution of Mesopithecus (: ) from Greece: evidence from selected astragalar characters

Dionisios Youlatos Æ George D. Koufos

Received: 21 May 2009 / Accepted: 14 July 2009 / Published online: 14 August 2009 Ó Japan Monkey Centre and Springer 2009

Abstract This paper reports our investigations into slight preference of terrestrial substrates. The results functional aspects of the astragalus of four samples of the mainly conform to paleoenvironmental reconstructions of genus Mesopithecus from Greece. More particularly, it the fossiliferous localities and denote that Mesopithecus aims to infer substrate preferences of M. delsoni/pentelicus was mainly a semiterrestrial radiation throughout its from the Middle Turolian site of Perivolaki (central evolutionary history, with differential rates of use between Greece), M. pentelicus from the late Middle Turolian site arboreal and terrestrial substrates. These adaptations could of Pikermi (southern Greece), and M. cf. pentelicus and have promoted the dispersal of the genus throughout M. cf. monspessulanus from the Late Turolian site of Eurasia during the latest Miocene and Early Pliocene. Dytiko (northern Greece). For these purposes, selected astragalar functional features, such as trochlea wedging, Keywords Mesopithecus Á Colobinae Á Astragalus Á proximal facet curvature, and head rotation were expressed Functional morphology Á Locomotion Á Turolian Á as linear measurements on both fossil and selected extant Miocene Á Greece colobines. The size-adjusted measurements were used for univariate comparisons as well as a multivariate principal components analysis. Both approaches revealed that the Introduction selected characters were able to discriminate between extant arboreal and semiterrestrial colobines, but all fossil In this paper, we examine functional aspects of selected forms presented mosaic morphology. Thus, the oldest astragalar features of the Miocene colobine Mesopithecus representative, M. delsoni/pentelicus was reconstructed as from Greece. Previous reports analyzed combined astrag- mainly semiterrestrial. On the other hand, the astragalus of alar and calcaneal features of M. pentelicus from Pikermi M. pentelicus appeared to reflect semiterrestrial habits with by means of multivariate analyses (Youlatos 1999), as well a moderate adaptation to arboreality. Similar habitus as calcaneal features via univariate comparisons (Youlatos reconstruction was allocated to the more recent M. cf. 2003). The astragalus is a proximal foot bone that is fre- pentelicus, whereas the sympatric and synchronous M. cf. quently well preserved and considered as a good indicator monspessulanus showed semiterrestrial adaptations with a of locomotor and postural patterns. More particularly, fossil astragali have often been used to infer substrate preference in many fossil primates, and many astragalar D. Youlatos (&) features, such as the shape of the trochlea, the curvature of Department of Zoology, School of Biology, the proximal astragalocalcaneal facet, and the torsion angle Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece of the head, have been well described functionally e-mail: [email protected] (e.g. Szalay and Decker 1974; Conroy 1976; Szalay and Langdon 1986; Langdon 1986; Strasser 1988; Gebo 1989; G. D. Koufos Lewis 1989; Carrano 1997; Seiffert and Simons 2001). Laboratory of Geology and Palaeontology, Department of Geology, Aristotle University of Thessaloniki, Herein, we consider the functional morphology of 54124 Thessaloniki, Greece selected astragalar characters, aiming to trace the evolution 123 24 Primates (2010) 51:23–35 of locomotor behavior of the genus Mesopithecus in Greece throughout the Turolian (Late Miocene). Mesopi- thecus Wagner, 1839, is known from numerous cranial, dental, and postcranial specimens from many Eurasian Late Miocene to Late Pliocene sites (8.5–3 Ma), representing three or four different species (Delson 1975; Szalay and Delson 1979; de Bonis et al. 1990, 1997; Zapfe 1991; Jablonski 2002; Koufos et al. 2004; Delson et al. 2005; Harrison and Delson 2007; Pradella and Rook 2007; Tsoukala and Bartsiokas 2008; Koufos in press b). It appears to bear close affinities to Asian colobines (Szalay and Delson 1979; Hohenneger and Zapfe 1990; Zapfe 1991; Jablonksi 1998; Pan et al. 2004), but the primitive nature of its character still classifies it as Colobinae in- certae sedis (Szalay and Delson 1979; Strasser and Delson 1987; Jablonski 2002). For the purposes of our study, we examined the astragali of four samples of Mesopithecus, here considered as chronospecies, from different localities of the Turolian age in Greece. The oldest fossil material is attributed to M. delsoni/ pentelicus and was recently discovered in the Middle Turolian site of Perivolaki (MN-12) in central Greece, with a magnetostratigraphic record suggesting an age of 7.3– 7.1 Ma (Koufos 2006a; Koufos et al. 2006a). The richest known material belongs to M. pentelicus and originates from the classic late Middle Turolian locality of Pikermi (MN-12) in southern Greece (Gaudry 1862–1867; Szalay and Delson 1979; Zapfe 1991). The age of the Pikermi Fig. 1 Biochronological table of the Greek localities bearing Mesopithecus fauna is still under debate, but an age of about 7.0 Ma is accepted by most authors (Koufos 2006b, 2008 b). Finally, to examine functional aspects of selected characters of rich fossil remains that are attributed to both M. cf. pen- the astragalus of the different intermediate forms of the telicus and M. cf. monspessulanus have been discovered in recognized species of Mesopithecus from Greece. The the Late Turolian sites of Dytiko 1, 2, 3 (DTK, DIT, DKO) inference of substrate preference via this functional anal- in the Axios valley of Macedonia, northern Greece, all of ysis will provide evidence for the evolution of locomotor MN-13 age, ca. 7–5.3 Ma (de Bonis et al. 1990, 1997; behavior and paleoecology of the genus in the Late Koufos et al. 2004; Koufos 2006b, in press a). All the Miocene in Greece and the Greco-Iranian paleobiogeo- known Mesopithecus-bearing Greek localities and their graphic province. geological ages are summarized in Fig. 1. These samples appear to represent different chronospecies, and perhaps intermediate forms between the recognized species of Methods Mesopithecus. Inferences of substrate preference of the recognized The fossil material consisted of 12 astragali (Table 1, forms of Mesopithecus vary, mainly due to the mosaic Fig. 2). For comparative purposes, we examined the character of their postcranium (Szalay and Delson 1979). astragali of 72 recent Colobinae representing eight genera The Early Turolian M. delsoni has been compared with and 19 species (Table 2). The extant specimens belong to terrestrial cercopithecids, inferring terrestrial habits. On the adult wild-shot individuals and are housed in the collec- other hand, habitus reconstruction for the Middle-Late tions of the Laboratoire d’Anatomie Compare´e and Labo- Turolian M. pentelicus varies from arboreal (Escarguel ratoire d’Anthropologie Biologique of the Muse´um 2005), semiterrestrial (Simons 1972; Szalay and Delson National d’Histoire Naturelle, Paris, France, and the 1979; Youlatos 1999; 2003) to terrestrial (Gaudry 1862; Mammal Collections, Department of Zoology, Natural Ko¨hler et al. 1999; Jablonski 2002). Lastly, the Early History Museum, London, UK. Each species was classified Pliocene M. monspessulanus has been suggested as rela- as semiterrestrial when activities were shared between tively arboreal (Szalay and Delson 1979). Our study aimed ground and trees or when there appeared to be great 123 Primates (2010) 51:23–35 25

Table 1 Fossil astragali of Museum Catalog no. Side Location Age Species Mesopithecus examined in this study LGPUT PER-1290 L Perivolaki Middle Turolian delsoni/pentelicus MNHN PIK-236 R Pikermi Middle Turolian pentelicus MNHN PIK-237 R Pikermi Middle Turolian pentelicus MNHN PIK-238 L Pikermi Middle Turolian pentelicus NHMW 1863-1/6 L Pikermi Middle Turolian pentelicus LGPUT Aristotle University of Thessaloniki, Laboratory of LPUW Unnumb. L Pikermi Middle Turolian pentelicus Geology and Paleontology, LGPUT DKO-72 R Dytiko 3 Late Turolian cf. pentelicus LPUW Laboratory of LGPUT DKO-171 L Dytiko 3 Late Turolian cf. pentelicus Paleontology, Universita¨t Wien, LGPUT DIT-82 L Dytiko 2 Late Turolian cf. pentelicus MNHN Laboratory of Paleontology, Muse´um National LGPUT DTK-277 L Dytiko 1 Late Turolian cf. pentelicus d’Histoire Naturelle, Paris, LGPUT DTK-279 R Dytiko 1 Late Turolian cf. pentelicus NHMW Naturhistorisches LGPUT DIT-76 R Dytiko 2 Late Turolian cf. monspessulanus Museum, Wien

Cercopithecids—in general and in our case—colobines show unmistakable signs of terrestriality in their feet, as it seems clear that they have gone through a terrestrial phase in their evolution (Strasser 1988, 1992; Harrison 1989; Gebo 1989, 1993). Arboreal locomotion is hypothesized to have been secondarily developed (Harrison 1989; Strasser 1988, 1992), and tarsal morphology of arboreal species should differ only slightly from that of more terrestrial ones, rendering difficult any morphofunctional associations with substrate preferences. This would have been even more difficult when tarsal elements were considered, as in this report. For these reasons, we conducted a preliminary qualitative and quantitative study within the subfamily in order to assess those astragalar features that could rela- tively safely discriminate between the different functional groups. The assessment within the subfamily demarcated three astragalar character complexes: the wedging of the trochlea in the upper ankle joint, the curvature of the proximal astragalocalcaneal facet in the proximal lower ankle joint, and the lateral rotation of the astragalar head in the transverse tarsal joints. These features were subse- quently expressed as linear measurements defined as follows (Fig. 3): (1) astragalar trochlea proximal width is the distance between the proximal edge of the medial border Fig. 2 Dorsal view of the astragali of Mesopithecus delsoni/pente- and the proximal edge of the lateral border of the trochlea licus (PER-1290), M. pentelicus (PIK-238), M. cf. pentelicus (DTK- 279), and M. cf. monspessulanus (DIT-76); scale bar represents 1 cm perpendicular to the long axis of the trochlear groove; (2) astragalar trochlea distal width is the distance between the distal edge of the medial border and the distal edge of the variation in support preference across its distribution; or lateral border of the trochlea; (3) proximal astragalo- arboreal when almost all active time was spent in trees, calcaneal facet height is the maximal height of the facet rarely descending to the ground, based on published reports when the astragalus is posed on a horizontal plane standing of positional behavior and/or ecology (Ripley 1967; Rose on the medial and lateral edges of the facet; (4) proximal 1979; Fleagle 1980, 1988; Kirkpatrick and Long 1994; astragalocalcaneal facet length is the maximal distance Oates et al. 1994; Gebo and Chapman 1995; McGraw between the medial and lateral edges of the facet; and (5) 1998; Boonratana 2000; Ren et al. 2001; Byron and Covert astragalar head rotation is the angle between the medio- 2004; Workman and Covert 2005; Solanksi et al. 2008). lateral axis of the astragalar head and the horizontal plane.

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Table 2 Skeletal sample of astragali of extant Colobinae included in (Delson et al. 2000), and the new measurements were this study plotted against log-transformed body weights of the studied Species Sample number Substrate preference species to examine for any effects of allometry (Zar 1996). For Mesopithecus, we used the means of male and female Colobus angolensis 4 Arboreal estimates, assuming that M. delsoni/pentelicus bears a Colobus guereza 2 Arboreal similar size to M. delsoni, M. cf. pentelicus to that of Colobus polykomos 3 Arboreal M. pentelicus, and M. cf. monspessulanus to M. monspes- Piliocolobus badius 5 Arboreal sulanus. In some cases, this may have resulted in relatively Piliocolobus tephrosceles 2 Arboreal large ranges of the size-adjusted measurements, and this is Presbytis obscura 10 Arboreal indicated in the Results section. The size-adjusted mea- Presbytis melalophos 3 Arboreal surements were then tested between functional groups by Prebsytis hoisei 2 Arboreal means of one-way analyses of variance (ANOVAs) with Presbytis comata 1 Arboreal Tukey’s honest significance (HSD) post hoc tests, using a Presbytis rubicunda 1 Arboreal criterion of p \ 0.05 for statistical significance (Zar 1996). Semnopithecus entellus 7 Semiterrestrial Finally, to assess the influence of each size-adjusted Trachypithecus vetulus 4 Arboreal measurement in the general separation of functional groups Trachypithecus phayrei 3 Arboreal and the placement of fossil specimens, a multivariate Trachypithecus johnii 2 Arboreal technique was utilized. We opted for a principal compo- Trachypithecus barbei 1 Arboreal nents analysis (PCA) to describe the function and interre- Trachypithecus pileatus 1 Arboreal lations of both functional groups and measurements in a Rhinopithecus roxellanae 12 Semiterrestrial multidimensional morphological space. Pygathrix nemaeus 3 Arboreal Nasalis larvatus 6 Arboreal Results

This study examined metric functional features of the astragalus in three joints: (a) the upper ankle joint, (b) the proximal lower joint, and (c) the distal transverse tarsal joint. The upper ankle joint comprises the distal ends of tibia and fibula and the astragalar trochlea. The main movements accomplished are dorsal and plantar flexion accompanied by conjoint abduction and adduction of the foot (Langdon 1986; Szalay and Langdon 1986; Strasser 1988). Therefore, the shape of the astragalar trochlea would be strongly associated with these movements. In this study, this shape was quantitatively estimated by the proximal and distal trochlear widths. Both adjusted measurements did not show any allometric correlations to body size (proximal width: r2 = 0.3448, p = 0.094; distal width: r2 = 0.3546, p = 0.091). In all examined colobines, the relative width of the proximal part of the trochlea was larger than the distal one (Table 3, Fig. 4). This resulted in a relatively wedged trochlear surface. In terms of proximal width, the semiter- restrial forms were characterized by relatively narrow proximal surfaces, whereas more arboreal forms possessed Fig. 3 Astragalar measurements used in the study: ACFH astragalo- significantly wider ones (p = 0.0005; Table 3, Fig. 4). On calcaneal facet height, ACFL astragalocalcaneal facet length, HROT the other hand, all Mesopithecus forms displayed more or astragalar head rotation, TRDW trochlear distal width, TRPW less similar values that were placed within the range of trochlear proximal width arboreal colobines, with an insignificant shift of M. delsoni/ pentelicus toward the semiterrestrial side (Table 3, Fig. 4). For extant colobines and fossil Mesopithecus species, the The distal trochlear width presented a similar disposition above measurements were size adjusted by dividing values (Table 3, Fig. 4). Once more, semiterrestrial forms pos- by the cube root of body mass (g) from the literature sessed narrow distal trochlear surfaces, whereas more 123 Primates (2010) 51:23–35 27

Table 3 Means and 1 standard deviation of the size-adjusted astragalar functional characters Distal trochlear width Proximal trochlear width AC facet length AC facet height Head rotation

Semiterrestrial colobines (n = 19) 36.5 ± 5.4 48.5 ± 8.7 45.0 ± 6.9 14.9 ± 3.4 22.4 ± 4.1 Arboreal colobines (n = 54) 41.4 ± 8.0 56.0 ± 5.5 55.3 ± 5.5 18.1 ± 2.9 29.4 ± 5.1 Mesopithecus pentelicus (n = 5) 43.6 ± 5.5 54.8 ± 5.1 52.6 ± 1.1 14.6 ± 0.9 29.8 ± 2.3 M. cf. pentelicus (n = 5) 45.7 ± 1.2 56.4 ± 1.3 51.4 ± 4.2 14.7 ± 2.7 31.0 ± 2.7 M. cf. monspessulanus (n = 1) 41.4 55.1 47.5 14.5 28.0 M. cf. delsoni (n = 1) 40.8 54.6 44.1 12.0 26.0 AC astragalocalcaneal

proximal dorsal facet of the calcaneus forms the proximal lower ankle joint. The movements of the astragalus and calcaneus upon these facets appear to partly contribute to the eversion and inversion movements of the proximal foot (Szalay and Decker 1974; Langdon 1986; Lewis 1989; Gebo 1993). Therefore, the curvature and relative length of the proximal astragalar facet would be strongly related to these movements. In our study, the relative shape of this facet was estimated by the mediolateral length and the height. Neither size-adjusted measurements correlated to body weight (facet length: r2 = 0.3442, p = 0.097; facet height: r2 = 0.3146, p = 0.116). Colobines, as the rest of cercopithecids, are generally characterized by relatively short and slightly curved facets compared with other pri- mate groups (Strasser 1988). However, within colobines, our study showed that the different functional groups dis- played different lengths and heights (Table 3, Fig. 5). Thus, arboreal genera showed relatively long facets, whereas more terrestrial forms exhibited significantly shorter facets (p = 0.0001; Table 3, Fig. 5). Differences were also evident in the different forms of Mesopithecus. Thus, M. delsoni/pentelicus possessed a short facet, similar to semiterrestrial colobines, whereas the other three forms shifted more toward the arboreal side, with M. cf. pente- licus and M. pentelicus scoring the highest values (Table 3, Fig. 5). When, the height of the facet was considered, Fig. 4 Box and whisker plot (mean, standard error, and 1 standard deviation ) of (top) the astragalar trochlear distal width and (bottom) semiterrestrial and arboreal forms occupied opposite sides: the astragalar trochlear proximal width. ST semiterrestrial colobines, arboreal forms were characterized by high, and therefore MP Mesopithecus cf. pentelicus, MM M. cf. monspessulanus, MD well-curved, facets, whereas the more terrestrial species M. delsoni/pentelicus, MPE M. pentelicus, A arboreal colobines possessed lower, and therefore less curved, facets (p = 0.0022; Table 3, Fig. 5). Once more, M. delsoni/ arboreal forms displayed insignificantly higher values pentelicus scored an especially low value, indicating a (p = 0.124). The four forms of Mesopithecus laid more on smoother facet, whereas M. cf. pentelicus, M. pentelicus, the arboreal side, with M. cf. pentelicus showing a very and M. cf. monspessulanus appeared to be characterized by narrow distal trochlear surface. M. pentelicus also possessed almost identical, less curved facets, similar to that of a relatively narrow distal trochlear surface but showed a semiterrestrial forms (Table 3, Fig. 5). However, the for- large range that could be due to sex differences. In contrast, mer showed a very large variation in size range that could once more, M. delsoni/pentelicus tended insignificantly be due to sex differences of the studied specimens. toward semiterrestrial forms (Table 3, Fig. 4). The distal foot is composed of multiple joints that The articulation between the proximal kidney-shaped generally do not accommodate a great range of move- concave ventral facet of the astragalus and the convex ments. However, among transverse tarsal joints, details of 123 28 Primates (2010) 51:23–35

Fig. 6 Box and whisker plot (mean, standard error, and 1 standard deviation) of the astragalar head rotation angle. ST semiterrestrial colobines, MP Mesopithecus cf. pentelicus, MM M. cf. monspessul- anus, MD M. delsoni/pentelicus, MPE M. pentelicus, A arboreal colobines

presented significant differences between them, with arbo- real forms showing significantly greater angles and, thus, strongest head rotation (p = 0.0001; Table 3, Fig. 6). Lastly, the angles of M. pentelicus, M. cf. pentelicus, and, to a lesser degree, M.cfmonspessulanus, were more or less similar to that of arboreal forms (Table 3, Fig. 6). In con- trast, M. delsoni/pentelicus exhibited a lower head rotation angle that shifted more toward the semiterrestrial forms. Fig. 5 Box and whisker plot (mean, standard error, and 1 standard Although univariate tests provided significant results deviation) of (top) the proximal astragalocalcaneal facet length and concerning the allocation of the four samples of fossil (bottom) the proximal astragalocalcaneal facet height. ST semiterres- Mesopithecus to functional groups within the colobines, we trial colobines, MP Mesopithecus cf. pentelicus, MM M. cf. mons- wanted to test the placement of these fossil forms within pessulanus, MD M. delsoni/pentelicus, MPE M. pentelicus, A arboreal colobines the multidimensional space determined by the examined functional features of the astragalus through a PCA. Table 4 displays the summary statistics of the analysis and the articulation between the astragalar head and the navic- shows that the first two axes accounted for 72% of the total ular reflect the degree to which an individual is able to explained variance. The plot of these two axes (Fig. 7) invert or evert the distal part of the foot (Langdon 1986; demonstrated that arboreal (A) and semiterrestrial (ST) Strasser 1988; Lewis 1989; Gebo 1993). Therefore, among colobines were separated quite well, with arboreal and astragalar head features, the rotation of the astragalar head semiterrestrial species occupying relatively opposite would be indirectly associated with the position of meta- spaces, especially on the first axis. This division appears to carpal I relative to the lateral digits and the positioning of be supported by the negative scores on the first axis of all the foot upon specific substrates (Conroy 1976; Strasser the examined astragalar features (Table 5). M. delsoni/ 1988). In our study, this was estimated via the angle of the pentelicus was placed comparatively closer to semiterres- lateral head rotation in respect to the horizontal plane, trial forms, and more particularly, to Rhinopithecus, than which was positively correlated to body weight the rest of the fossil specimens (Fig. 7, see also Appendix). (r2 = 0.0533, r = 0.2308, p = 0.036). Cercopithecids, On the other hand, M. cf. monspessulanus was situated at compared with other anthropoids, exhibit lower astragalar the center of the axes and relatively closer to arboreal head angles, but within the family, colobines tend to present forms, such as Presbytis and Trachypithecus (Fig. 7, higher angles than cercopithecines due to their higher see also Appendix). Finally, both M. cf. pentelicus and commitment to arboreal habits (Strasser 1988). A similar M. pentelicus were mainly within the arboreal cluster; the difference, related to substrate preferences, was also evident former placed near Colobus, whereas the latter was much within colobines. In effect, the two functional groups closer to Presbytis (Fig. 7, see also Appendix). 123 Primates (2010) 51:23–35 29

Table 4 Statistics of the principal components analysis of the five These characteristics were tested on the fossil astragali of variables defining astragalar functional characters four forms of the Late Miocene colobine Mesopithecus Factor Eigenvalue % of variance Cumulative Cumulative % from Perivolaki, Pikermi, and Dytiko localities in Greece eigenvalue of variance and showed that all four presented a mosaic morphology, as with other postcranial elements that have been examined 1 2.61 52.24 2.61 52.24 (Table 6; Szalay and Delson 1979; Youlatos 2003). These 2 0.98 19.73 3.59 71.98 features are functionally analyzed below. 3 0.82 16.42 4.42 88.40 The astragalar trochlea is the articulating surface 4 0.43 8.71 4.85 97.12 between the lower leg and the tarsus. At this level, the 5 0.14 2.88 5.00 100.00 trochlea mainly permits movements that are restricted to the dorsal and plantar flexion of the foot and facilitate the fore and aft motion at the sagittal plane (Szalay and Langdon 1986). Additionally, the wedged morphology of A 3 the trochlea compels the tibia and fibula to transcribe arcs of different radii about the distal condyles of the tibia and 2 fibula, permitting variable degrees of conjunct adduction A AMP A AA A A A A 1 AA A MPE MP and abduction of the foot (Barnett and Napier 1953; Gebo A A AA A MPE A MPEMPE AA AAA 1989; Langdon 1986; Szalay and Langdon 1986; Strasser AA A A A A A A MM ST ST A A AA STST A MP ST MD STST 0 A A MPE 1988). Therefore, a generally wider trochlea, both proxi- A STST A STAA A A A ST A ST mally and distally, would favor an increased degree of Axis 2: 19,74% 2: Axis -1 ST ST ST A foot abduction and adduction in the upper ankle joint that A ST A ST A would facilitate the placement of the foot upon uneven -2 A A arboreal substrates (Strasser 1988; Lewis 1989). This was ST ST the case with the arboreal colobines that were character- -3 -4 -2 0 2 4 ized by distally and proximally wide astragalar trochlea. Axis 1: 52,24% Similar proximally and distally wide trochlea were also encountered in M. pentelicus and M. cf. pentelicus,a Fig. 7 Plot of the first two axes of the multivariate principal morphology that would suggest comparably enhanced components analysis (PCA) based on the five size-adjusted astragalar measurements. Mesopithecus pentelicus (MPE), M. cf. pentelicus upper ankle mobility. In contrast, relatively narrower (MP), and M. cf. monspessulanus (MM) are all nested within the trochlea would limit the extent of upper ankle joint con- cluster of arboreal colobines (A), whereas M. delsoni/pentelicus (MD) junct abduction and adduction, reorienting the foot shifts more on the semiterrestrial (ST) side through a more hinge-like articulation, to more direct sagittal movements that are required during more terres- Discussion trial activities (Langdon 1986; Lewis 1989; Nakatsukasa et al. 1997). M. delsoni/pentelicus and, to a lesser extent, The inference of substrate preference and paleobiology of M. cf. monspessulanus exhibited a similar morphology, fossil requires the use of postcranial features that most likely indicating a higher degree of stability in the can be robustly associated with regional functions, which upper ankle joint that would be beneficial for movements in turn suggest limb movements involved in specific to a sagittal plane. positional modes. In this study, we used astragalar features On the plantar surface of the astragalus lies the proximal that are associated with joint movements that suggest kidney-shaped astragalocalcaneal facet that articulates with specific hind foot function performed on certain substrates. the proximal calcaneal facet. The length and curvature of Thus, astragalar trochlear wedging, the curvature of the the former facet is associated with the morphology of the proximal astragalocalcaneal facet, and the lateral rotation latter and promotes proximal subtalar mobility (Olivier and of the astragalar head appeared to have successfully dis- Fontaine 1957; Szalay and Decker 1974; Langdon 1986; criminated between arboreal and semiterrestrial colobines. Strasser 1988). Arboreal colobines possessed relatively Associated functional aspects of the morphology of these long and high facets that denoted pronounced curvature. characteristics have been extensively investigated and This morphology is associated with a long, tightly curved, associated with specific tarsal movements that accommo- proximal calcaneal facet that permits a larger extent of date the foot on particular substrates (Szalay and Decker movements of the astragalus upon the calcaneus, providing 1974; Conroy 1976; Szalay and Langdon 1986; Langdon relatively extensive inversion and eversion of the proximal 1986; Strasser 1988; Gebo 1989; Lewis 1989; Prasad and foot (Olivier and Fontaine 1957; Langdon 1986; Strasser Godinot 1994; Carrano 1997; Seiffert and Simons 2001). 1988). This contributes to the overall mobility of the tarsus 123 30 Primates (2010) 51:23–35

Table 5 Factor score Factor 1 2 3 4 5 coefficients of the five variables defining astragalar functional Head rotation -0.097402 0.969779 -0.019693 -0.31181 0.17558 characters AC facet height -0.294483 -0.250323 -0.344398 -1.18667 -0.08174 AC facet length -0.308039 0.051895 -0.549223 0.76420 -1.31027 Trochlear proximal width -0.355552 -0.080513 0.131909 0.45059 1.97246 Trochlear distal width -0.255538 -0.031702 0.882918 -0.06178 -1.13771 AC astragalocalcaneal

Table 6 Summary of functional inferences of the fossil forms of Mesopithecus based on the studied astragalar characters Mesopithecus Mesopithecus Mesopithecus cf. Mesopithecuscf. delsoni/pentelicus pentelicus pentelicus monspessulanus

Distal trochlear width Semiterrestrial Arboreal Arboreal Semiterrestrial Proximal trochlear width Arboreal semiterrestrial Arboreal Arboreal Arboreal Astragalocalcaneal facet length Semiterrestrial Arboreal Semiterrestrial arboreal Semiterrestrial Astragalocalcaneal facet height Semiterrestrial Semiterrestrial Semiterrestrial Semiterrestrial Head rotation Semiterrestrial arboreal Arboreal Arboreal Arboreal below the upper ankle joint level so that the foot can be foot accommodated on a more or less horizontal plane, accommodated on arboreal substrates. In contrast, semi- as on terrestrial substrates. In contrast, a pronounced terrestrial colobines presented relatively short, low facets angle, similar to that recorded for arboreal colobines, that depicted a smaller curvature, which appear to limit the would suggest habitual distal foot inversion (Gebo and extent of these proximal subtalar movements. Among the Dagosto 1988; Strasser 1988). A strong astragalar head different fossil forms, only M. delsoni/pentelicus was rotation would align the navicular and the entocuneiform characterized by a quite short and even lower facet, indi- more vertically, facilitating the medial elevation of the cating a gentle curvature that is usually associated with a tarsus and the toes distally, enabling an actively oppos- smoothly curved and short calcaneal facet, which in turn able hallux to face the other four digits (Elftman and suggests restricted astragalocalcaneal movements and Manter 1935; Conroy 1976). This morphology would overall mobility at this level (Langdon 1986; Strasser 1988; thus accommodate the foot on arboreal substrates that Lewis 1989). This would contribute to a relatively stable require firm foot prehension and is thus related to fre- tarsus able to withstand powerful loadings that develop quent arboreal activities. Therefore, the high angle of during frequent terrestrial activities (Strasser 1988, 1992). head rotation in M. cf. pentelicus, M. pentelicus, and M. cf. monspessulanus exhibited a similar morphology to M. cf. monspessulanus would most likely suggest a M. delsoni/pentelicus, but the facet was slightly higher, comparably enhanced distal foot inversion, enabling the probably indicating a moderately greater degree of foot to be well accommodated on arboreal substrates mobility. The facet was similarly low but slightly longer in also. On the other hand, the weaker rotation observed in M. pentelicus and M. cf. pentelicus, with the former M. delsoni/pentelicus, which was intermediate between showing a even longer facet, comparable with those of that of arboreal and semiterrestrial forms, would suggest arboreal colobines, that would suggest a relatively higher a more limited distal foot inversion that would favor a degree of subtalar movements, probably associated with a shared use of both arboreal and terrestrial substrates. more extensive use of arboreal substrates. Overall, the astragali of the four forms of Mesopithecus In the distal part of the astragalus, the astragalar head examined in this study revealed an interesting mosaic of is a major component of the astragalonavicular joint, the functional adaptations. Thus, in the upper ankle joint, details of which reflect the degree of distal inversion and M. cf. pentelicus and M. pentelicus appeared to be mor- eversion of the foot (Strasser 1988). In this context, the phologically and functionally similar to extant arboreal lateral rotation of the astragalar head appears to deter- colobines (Table 6). M. cf. monspessulanus displayed a mine the rotational angle of the tibia relative to meta- more intermediate morphology, whereas M. delsoni/pen- tarsals (Carrano 1997). A weak angle, as the one telicus lay more on the semiterrestrial side of the colobine observed in semiterrestrial colobines, would set the plane spectrum (Table 6). A different functional interpretation of the metatarsals in a more perpendicular angle to the was inferred for the morphology of the astragalocalcaneal long axis of the tibia and would imply an everted distal proximal facet in the lower ankle joint, where M. delsoni/

123 Primates (2010) 51:23–35 31 pentelicus, M. cf. monspessulanus, and M. cf. pentelicus substrates. In an analogous manner, the synchronous and showed clear similarities to extant semiterrestrial colo- sympatric M. cf. monspessulanus also appears to present a bines, whereas M. pentelicus was intermediate toward the mixture of astragalar characteristics that would suggest arboreal forms (Table 6). Finally, in the midtarsal joints, mainly semiterrestrial habits, with perhaps a slight prefer- the rotation of the head in M. cf. pentelicus, M. pentelicus, ence for terrestrial substrates. The Late Turolian Dytiko and M. cf. monspessulanus implied functional similarities localities are usually reconstructed as an alternation of to arboreal forms, whereas that of M. delsoni/pentelicus wooded and bushy areas with some more closed environ- appeared closer to that of semiterrestrial ones (Table 6). ments, characterized by the presence of waterholes sur- Finally, when all functional characters were considered rounded by dense forested patches (de Bonis et al. 1992, together in the multivariate analysis, all Mesopithecus 1999; Merceron et al. 2005; Koufos 2006c, in press b). forms were plotted within the arboreal cluster, and only Such a diverse habitat could have provided niches for the M. delsoni/pentelicus showed a shift toward the semiter- two different sympatric forms. M. cf. pentelicus could have restrial side. exploited the more closed and wooded patches, whereas M. When this assortment of functional associations of the cf. monspessulanus could have utilized the interface different astragalar features in Mesopithecus is consid- between the two habitats, making more extensive use of the ered, M. delsoni/pentelicus from the Middle Turolian of open grasslands. If this is confirmed, as the coexistence of central Greece could be reconstructed as a primarily two different biospecies (i.e. M. pentelicus and M. mons- semiterrestrial monkey with limited use of arboreal sub- pessulanus), then Dytiko would have been a place of brief strates. These habits appear to conform to the paleo- coexistence of a mother and daughter species prior to environmental reconstruction of the bearing locality. the extinction of the former (Delson et al. 2005). Thus, Apparently, Perivolaki corresponds to a relatively open M. mospessulanus would have evolved into a semiterres- environment with grasslands, composed mainly of trial species that would show higher terrestrial tendencies Graminae, surrounded by bushes and shrubs (Koufos et al. than its earlier congeners within an open woodland habitat 2006b). This is comparable with south Bulgarian sites at the margins of humid areas (Eronen and Rook 2004; (Koufos et al. 2003; Merceron et al. 2006), as well as the Delson et al. 2005). earlier Ravin des Zouaves-5 site in Greece, where The findings of our study denote that the radiation of M. delsoni has been recovered (de Bonis et al. 1992, Mesopithecus consists mainly of semiterrestrial monkeys 1999; Koufos in press b). that appear to have differed in relative rates of terrestrial On the other hand, M. pentelicus presented an interest- use. This was also the case with other crown colobines ing mixture of astragalar features that denoted a relatively (e.g. Dolichopithecus), which appear to be adapted to a mobile upper ankle and astragalonavicular joint, with rel- variable regime of terrestriality (Jablonski 2002; Delson ative stability at the proximal subtalar joint. Based on these et al. 2005; Egi et al. 2007, Ingicco 2008). The earliest characteristics, the late Middle Turolian M. pentelicus representative of the lineage, the Early Turolian M. del- could be reconstructed as a primarily semiterrestrial mon- soni is described as a robustly built monkey similar to key that would show a slight preference for arboreal over extant semiterrestrial colobines (Koufos et al. 2003), terrestrial activities. These findings appear to mainly con- exploiting relatively open and dry habitats (de Bonis et al. form to previous studies that have considered this species 1992, 1999; Koufos et al. 2003). Subsequently, the as mainly semiterrestrial (Szalay and Delson 1979; Strasser Middle Turolian M. pentelicus would have also been 1988; Youlatos 1999; 2003) and partly justifies Escarguel’s semiterrestrially adapted but with important arboreal (2005) study that suggested arboreality for this fossil spe- tendencies within a mixed savanna–forest environment. cies. In addition, the Middle Turolian locality of Pikermi is This species would have later evolved into the more usually reconstructed as either savanna–woodland enriched semiterrestrial/terrestrial M. monspessulanus (Delson et al. by gallery forests (de Bonis et al. 1992, 1999), or a more 2005). The two forms of the late Turolian site of Dytiko forested environment (Solounias et al. 1999). In all cases, it would most likely represent two intermediate forms. One would have been suitable for a semiterrestrial monkey would have retained semiterrestrial habits with slight exploiting both fruit and leaves (Reitz 2002; Pan et al. terrestrial tendencies (M. cf. monspessulanus), whereas 2004) on the tree crown peripheries of dispersed feeding the other (M. cf. pentelicus) would have evolved to a tree sites. more semiterrestrial form, utilizing arboreal and terrestrial The more recent M. cf. pentelicus from Late Turolian of substrates equally well. As the climate became gradually northern Greece presented a more or less similar astragalar more humid through Late Turolian and Early Ruscinian, profile, with an even more restricted subtalar joint, and and forested environments started spreading through the could be also reconstructed as a semiterrestrial monkey, eastern Mediterranean, the former intermediate form exhibiting equal use of both terrestrial and arboreal would have most likely have evolved into the more 123 32 Primates (2010) 51:23–35 gracile, semiterrestrial M. monspessulanus that was suit- Appendix ably adapted to such an environment (Delson et al. 2005). The genus Mesopithecus (8.5–3 Ma: Szalay and Delson See Table 7. 1979) is the oldest Eurasian colobine fossil; it postdates the genetically timed African-Asian colobine split (10.8 Ma: Raaum et al. 2005; Sterner et al. 2006) and Factor score coefficients of fossil Mesopithecus and modern colobines subsequent migration of the Asian clade from Africa to for the first three factors Eurasia (10 Ma: Stewart and Disotell 1998). The claimed close phylogenetic relationships of Mesopithecus to the Genus Factor 1 Factor 2 Factor 3 Asian Presbytini, and more particularly to the odd-nosed Mesopithecus cf. pentelicus -0.16389 -0.11107 0.84751 langurs of Southeast Asia (Jablonski 2002; Pan et al. M. cf. pentelicus 0.16141 1.29404 1.72044 2004), renders the reconstruction of its paleobiology M. cf. pentelicus 0.12701 0.86562 0.89657 essential in the understanding of the evolutionary history M. delsoni/pentelicus 0.79104 -0.02281 1.18712 of these Asian forms. The semiterrestrial adaptations of M. cf. mospessulanus 0.33800 0.15702 0.72806 the genus may have permitted its dispersal eastward M. pentelicus -0.10355 -0.18310 1.07222 across the Asian continent through corridors of habitats M. pentelicus -0.24040 0.93256 1.14511 characterized by the alternation of woodland and open M. pentelicus -0.41486 0.59542 1.24501 environments that can be readily utilized by monkeys that M. pentelicus 0.34134 0.56649 -0.01537 use both arboreal and terrestrial substrates (Pan et al. M. pentelicus 0.48219 0.58126 -0.58891 2004; Sterner et al. 2006). In this context, postcranial Colobus -0.88737 1.01514 1.69982 elements of the recently described?M. sivalensis would Colobus 0.22088 1.07754 1.18461 have been substantial in assessing this trend (Harrison and Colobus 0.02607 1.14939 -0.94818 Delson 2007). Evidence for semiterrestrial ancestry in Colobus -0.05230 -0.70847 -0.08550 these Asian forms may be further reflected in the domi- Colobus -1.59310 0.06064 0.86277 nant semiterrestrial and terrestrial adaptations and habits Colobus -1.34451 0.17416 1.91316 of the northern snub-nosed monkeys (Rhinopithecus spp.), Colobus -2.18737 -0.53425 0.32181 which utilize similarly patchy environments in south Colobus -1.18829 -1.92734 0.85154 China (Davison 1982; Kirkpatrick and Long 1994; Oates et al. 1994; Ren et al. 2001; Pan et al. 2004). On the other Colobus -0.05996 0.22900 -1.62640 hand, the southern odd-nosed forms (Pygathrix, Simias, Nasalis -1.24789 0.85647 0.54686 Nasalis), which are postulated to have evolved from the Nasalis -0.16274 0.58456 0.52960 northern ones (Pan and Oxnard 2001; but see Sterner Nasalis -0.54353 1.34034 0.03955 et al. 2006), may have subsequently diverged from this Nasalis -0.03067 0.33351 -0.69411 habitat and become more arboreal in order to invade and Nasalis -1.00242 0.62964 -0.19986 exploit the rich remnant tropical forests of south and Piliocolobus -0.73793 -1.72153 -0.56705 Southeast Asia. In this context, the detailed analysis of Piliocolobus -0.68614 -0.23996 1.48780 the postcranium of these taxa may shed more light on Piliocolobus -0.35980 -0.63494 1.18069 these phylogenetic and functional adaptations (e.g., Piliocolobus -0.08750 0.23573 1.03673 Wright et al. 2007). Piliocolobus 0.35007 1.26311 -0.57207 Piliocolobus -0.07935 -1.54979 0.19160 Acknowledgments We are greatly indebted to Profs. P. Tassy Piliocolobus 1.23266 -1.18980 0.06339 (Institut de Pale´ontologie, M.N.H.N. Paris), D. Robineau (Laboratoire Presbytis -0.21978 -2.03995 -1.37023 d’Anatomie Compare´e, M.N.H.N. Paris), H. de Lumley (Institut de Pale´ontologie Humaine, M.N.H.N. Paris), Drs. G. Ho¨ck-Daxner and Presbytis -0.32806 0.03941 -0.51272 M. Harzhauser (Naturhistorisches Museum, Wien), Prof. Rabeder Presbytis -1.58057 -0.21006 0.56180 (Institut fu¨r Pala¨ontologie, Universita¨t Wien), and Dr. L. Gordon Presbytis -0.43192 0.47525 -0.75516 (Section of Mammals, Zoology Department, M.N.H., London) who Presbytis -0.55394 -0.10871 -2.30063 provided access to the collections under their care. Excavations in the Axios valley were financially supported by the Revealing Hominoids Presbytis 1.12190 0.73598 -1.08927 Origins Initiative (R.H.O.I.-N.S.F.), the C.N.R.S. (France), and the Presbytis -0.52061 -0.47034 -1.14973 L.S.B. Leakey Foundation. We are thankful to all Greek and French Presbytis 0.20512 0.68739 -1.49311 colleagues and students whose help was invaluable during fieldwork. Research in Vienna and Paris by GDK was supported by SYNTHE- Presbytis 0.32647 0.01064 -0.46906 SYS. Research in Paris by DY was financed by ERASMUS. Finally, Presbytis -0.01332 1.33202 -0.86515 we are particularly grateful to Drs. E. Delson and D.L. Gebo who Presbytis 0.33700 0.47977 -1.72888 provided insightful remarks that greatly improved the manuscript.

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