Geobios 36 (2003) 229–239 www.elsevier.com/locate/geobio

Calcaneal features of the Greek Miocene Mesopithecus pentelicus (Cercopithecoidea: ) Caractères calcanéens du primate du Miocène de Grèce Mesopithecus pentelicus (Cercopithecoidea : Colobinae)

Dionisios Youlatos *

Department of Zoology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece Received 1 June 2001; accepted 21 October 2002

Abstract

This paper investigates substrate preferences of the Greek Colobine Mesopithecus pentelicus WAGNER, from the Miocene of Pikermi, by examining selected functional features of the calcaneus that distinguish between arboreal and terrestrial Cercopithecidae. Mesopithecus possesses a relatively long proximal calcaneal region associated with a slightly low and wide surface for the insertion of m. triceps surae. These features approximate that of semi-terrestrial Cercopithecidae and would suggest terrestrial cursorial activities. On the other hand, the relatively long and narrow proximal calcaneo-astragalar facet, similar to that of most arboreal species, would provide ampler subtalar movements. The mosaic of these features implies a semi-terrestrial way of life and conforms to the savanna-woodland paleoenvironment of Pikermi, Greece. These features appear to be well associated with foot function and change of habitus and are used to examine scenarios of the evolutionary history of the Colobinae. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved.

Résumé

Cet article traite des préférences de support chez le Colobe Grec du Miocène de Pikermi Mesopithecus pentelicus WAGNER à travers l’étude des caractères sélectionnés du calcanéum, capables de distinguer les Cercopithecidae arboricoles de terrestres. Mesopithecus possède une région proximale relativement longue et une surface d’insertion des m. triceps surae assez basse et large. Cette morphologie est proche des formes semi-terrestres et serait associée à des activités quadrupèdes terrestres. En revanche, la facette calcanéo-astragalienne proximale est pareille à celle des espèces arboricoles, en étant longue et relativement étroite, ce qui suggèrerait des mouvements amples de la cheville. Cette combinaison des caractères calcanéens suggèrerait un mode de vie semi-terrestre tout en accord avec l’environnement de Pikermi de savane boisée. En outre, ces caractères étudiés semblent être bien associés à la fonction du pied et aux changements d’habitat et ils sont utilisés à l’examination des scénarios de l’histoire évolutive des Colobinae. © 2003 Éditions scientifiques et médicales Elsevier SAS. Tous droits réservés.

Keywords:Mesopithecus pentelicus; Colobinae; Calcaneus; Functional anatomy; Greece; Miocene

Mots clés : Mesopithecus pentelicus ; Colobinae ; Calcaneum ; Anatomie fonctionnelle ; Grèce ; Miocène

1. Introduction nial, dental, and postcranial specimens from numerous Eur- asian uppermost Miocene to upper Pliocene sites (8.5-3 Ma), The genus Mesopithecus WAGNER, 1839, of the catar- representing three different species (Delson, 1975; Szalay rhine family of Cercopithecidae, is known from several cra- and Delson, 1979; de Bonis et al., 1990). The locality of Pikermi in Greece, dated as end of middle Turolian, has * Corresponding author. yielded the richest material of nearly a hundred individuals E-mail address: [email protected] (D. Youlatos). representing the best-known species, Mesopithecus penteli-

© 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI:10.1016/S0016-6995(03)00008-1 230 D. Youlatos / Geobios 36 (2003) 229–239 cus (Gaudry, 1862–1867; Szalay and Delson, 1979). Based Table 1 on cranial, dental, and postcranial characters, Mesopithecus Substrate preferences of extant Cercopithecidae used in this study is grouped within the subfamily of Colobinae, bearing close Préférences d’habitat des Cercopithecidae récents utilisés dans cette étude COLOBINAE affinities to Asian Colobines (Szalay and Delson, 1979; Ho- ARBOREAL TERRESTRIAL henneger and Zapfe, 1990; Zapfe, 1991; Jablonksi, 1998). SEMI-TERRESTRIAL Colobus spp. i,j Semnopithecus However, given the primitive nature of most of its characters, entellusa it is still classified as a Colobinae incertae sedis (Szalay and Pygathrix nemeaus h Rhinopithecus spp. h Delson, 1979; Strasser and Delson, 1987). Presbytis spp. d The reconstruction of the paleobiology of Mesopithecus is Nasalis larvatush still under debate. Many authors, based on postcranial fea- CERCOPITHECINAE ARBOREAL TERRESTRIAL tures, such as the deep supraradial fossa on the distal hu- SEMI-TERRESTRIAL Cercocebus aterrimusf Cercocebus torquatusb Cercopithecus merus, the shallow radial notch on the ulna, the relatively c short tarsus, and the moderately long phalanges of the foot, aethiops Cercopithecusdianaj Cercopithecus hamlynig Cercopithecus suggest an arboreal way of life for Mesopithecus (Gabis, lhoestie 1960; Szalay and Delson, 1979; Zapfe, 1991). Besides, this Cercopithecus nictitansf Cercopithecus Erythrocebus patasf array of features would further agree with the phylogenetic neglectuse position of the genus as a member of the secondarily arboreal Cercopithecus mitisi Macaca mulattaf Theropithecus subfamily of Colobinae. In contrast, other postcranial char- geladaf e f f acters, such as limb proportions, the posteriomedial direction Cercopithecus talapoin Macaca radiata Papio spp. d f f of the medial epicondyle, the well-developed humeral tro- Macaca fascicularis Macaca maura Mandrillus spp. Macaca sylvanusf chlea, the retroflexed olecranon process, the straight ulnar Macaca nemestrinad shaft, the robustness of the long bones and the phalanges, and a Ripley, 1967; b Jones and Sabatier Pi, 1968; c Rose, 1979; d Fleagle, many tarsal features indicate adaptations to a more terrestrial 1980; e Gautier-Hion, 1988; f Fleagle, 1988; g Thomas, 1991; h Oates et al., way of life (Gaudry, 1862–1867; Gabis, 1960; Szalay and 1994; i Gebo and Chapman, 1995; j McGraw, 1998. Delson, 1979; Zapfe, 1991). Based on this mosaic of differ- ent postcranial features, the paleobiology of Mesopithecus has been mostly paralleled to that of the more terrestrially to be used on the respective bones of Mesopithecus in order adapted and langurs (Szalay and Delson, 1979; to infer substrate preferences of this Greek fossil primate. Youlatos, 1999). Among postcranial material, foot bones are usually con- 2. Material and methods sidered as relatively good indicators of locomotor and pos- tural patterns, because they are in direct contact with the The fossil material for this study consists of five calcanei: preferred substrates of an . Fossil calcanei are fre- PIK-239, PIK-240, PIK-266, PIK-1745, and PIK-1746. The quently well preserved and they have often been used to infer fossil bones belong to Mesopithecus pentelicus and are the locomotor and postural behaviour of many fossil pri- housed in the Institut de Paléontologie of the Muséum Na- mates. In this way, many calcaneal features have been well tional d’Histoire Naturelle (MNHN) in Paris, France. The described and functionally associated with different posi- material was found in the 1850s in the Pikermi locality, near tional patterns. Thus, a relatively long proximal calcaneal Athens in Central Greece by Gaudry (1862–1867). For com- body appears to increase the lever arm of the m. triceps surae, parative purposes, I examined the calcanei of 121 recent thus enhancing foot activity during cursorial habits. On the Cercopithecidae comprising 30 Colobinae and 91 Cercopith- other hand, a relatively long proximal calcaneo-astragalar ecinae. The extant specimens measured belonged to adult facet offers a surface for lower ankle joint mobility, sugges- wild-shot individuals and are housed in the collections of the tive of climbing habits in an arboreal milieu. In contrast, the Laboratoire d’Anatomie Comparée and Laboratoire more square-shaped facet (short and wide) suggests reduced d’Anthropologie Biologique of the MNHN. Based on studies screw-like movements, and provides subtalar stability neces- of ecology and positional behaviour, the different species of sary during terrestrial activities (Szalay and Decker, 1974; the two subfamilies (Table 1) were classified as arboreal Szalay and Langdon, 1986; Langdon, 1986; Strasser, 1988; (almost all active time spent on trees, rarely descending on Gebo, 1989; Lewis, 1989). the ground), semi-terrestrial (activities shared between the In this context, this paper investigates some functional ground and trees, where major behavioural contexts, such as aspects of the calcanei of Mesopithecus pentelicus from the feeding and sleeping may occur), and terrestrial (most active Pikermi locality in Greece. This paper will not describe the time spent on the ground with limited arboreal activity, fossil calcanei of the genus, as this has been done elsewhere mainly resting and sleeping). in detail (i.e., Gaudry, 1862–1867; Zapfe, 1991). In contrast, For the purpose of this paper, I shall only examine calca- its purpose is to identify calcaneal features that would statis- neal features that discriminate well between arboreal and tically distinguish between extant arboreal, semi-terrestrial, terrestrial extant Cercopithecidae. A preliminary qualitative and terrestrial representatives of the family Cercopithecidae, and quantitative assessment demarcated three calcaneal fea- D. Youlatos / Geobios 36 (2003) 229–239 231

Fig. 1. Dorsal (top row) and proximal (bottom row) views of the calcanei of (a) Mesopithecus (PIK-266), (b) a terrestrial Cercopithecine, Theropithecus,and(c) an arboreal Colobine, Presbytis. See Section 2 for the definition of measurements. Fig. 1. Vues dorsale (dessus) et proximale (dessous) des calcanéums de (a) Mesopithecus (PIK-266), (b) Theropithecus, Cercopithèque terrestre, et (c) de Presbytis, Colobe arboricole. Se référer à la section 2. Material and Methods pour la définition des mesures. tures that could safely distinguish between arboreal and ter- The relative form of this insertion is represented by index C1. restrial species: the insertion of m. triceps surae on the Terrestrial Cercopithecidae possess relatively low and wide proximal end of the calcaneus, the proximal calcaneal region, insertions, scoring low values of C1 index (Tables 2–4 and and the proximal calcaneo-astragalar facet. In order to quan- Fig. 2). In contrast, arboreal species differ significantly with tify these characteristics, I used the following measurements high and narrow insertions producing high C1 values (Tables (Fig. 1): (a) height of insertion of m. triceps surae (TSIH), (b) 2–4 and Fig. 2). In terms of subfamilies, the Colobinae and width of insertion of m. triceps surae (TSIW), (c) length of Cercopithecinae differ significantly, the latter showing low proximal calcaneo-astragalar facet (CAFL), (d) width of C1 values (Tables 3 and 4). Within the Colobinae, both proximal calcaneo-astragalar facet (CAFW), (e) length of terrestrial and arboreal representatives bear similar relatively calcaneal heel (=posterior region of calcaneus (CHL)) and (f) high and narrow insertions (Fig. 2 and Tables 2 and 4). On the maximum length of calcaneus (CML). Subsequently, the other hand, semi-terrestrial and arboreal Cercopithecinae measurements were used to calculate four indices. The rela- differ significantly from the terrestrial representatives of the tive shape of the insertion of m. triceps surae is reflected by subfamily, in exhibiting relatively higher insertions, produc- index C1 = (TSIH)/(TSIW). The relative length of the proxi- ing higher C1 values (Fig. 2 and Table 4). Mesopithecus mal (=posterior) region of the calcaneus is reflected by index possesses a relatively intermediate insertion, in between the C2 = (CHL)/(CML). The relative extent of the proximal terrestrial and semi-terrestrial Cercopithecinae (Figs. 1 and calcaneo-astragalar facet (=the proportion of the middle re- 2), with C1 values similar to that of terrestrial Cercopithecus gion of the calcaneus) is reflected by index C3 = species (Tables 2–4 and Fig. 2). Actually, the calcanei of (CAFL)/(CML). Lastly, the relative form of the proximal Mesopithecus bear significantly lower and wider insertions calcaneo-astragalar facet is reflected by index C4 = from that of all Colobinae, both terrestrial and arboreal (CAFW)/(CAFL). All the indices were plotted against log- (Table 4). transformed body weights of the studied species (Smith and The proximal region of the calcaneus, located between the Jungers, 1997) to examine any correlations to body mass. In proximal edge of the proximal calcaneo-astragalar facet and addition, in order to test for significant differences between the proximal end of the bone, is the load arm of m. triceps the different categories, I performed unplanned paired com- surae. Its relative length, as reflected by index C2, is posi- parisons of means with non-parametric Mann-Whitney tively correlated to body size (R = 0.404, F = 24.56, U-tests using a criterion of p < 0.05 (Zar, 1996). p < 0.001). In general, terrestrial Cercopithecidae possess long proximal regions while arboreal forms have signifi- 3. Results cantly shorter ones (Fig. 3 and Tables 2–4). This is also evident for species with similar body sizes, e.g. arboreal The long tendon of the main plantar flexors of the foot, m. Nasalis (BW = 20.4 kg) scores lower than the terrestrial triceps surae, inserts on the proximal end of the calcaneus. Papio spp. (BW ~ 21.0 kg). Moreover, the two subfamilies 232 D. Youlatos / Geobios 36 (2003) 229–239

Table 2 Means and standard deviations (std) of calcaneal indices for Mesopithecus and extant cercopithecids (C1: relative form of the insertion of m. triceps surae; C2: relative length of the posterior (proximal) region of the calcaneus; C3: relative length of the proximal calcaneo-astragalar facet; C4: relative form of the proximal calcaneo-astragalar facet) Valeurs moyennes et écarts types (std) des indices calcanéens chez Mesopithecus et des cercopithecidésrécents (C1 : forme relative de l’insertion des m. triceps surae ; C2 : longueur relative de la partie proximale du calcanéum ; C3 : longueur relative de la facette calcanéo-astragalienne proximale ; C4 : forme relative de la facette calcanéo-astragalienne proximale) C1 C2 C3 C4 Mesopithecus Mean 0.72 0.31 0.32 0.86 (n=4) Std 0.03 0.03 0.02 0.11 ARBOREAL Colobus Mean 0.87 0.29 0.31 0.85 (n=8) Std 0.08 0.02 0.02 0.07 Pygathrix Mean 0.98 0.27 0.32 0.89 (n=3) Std 0.10 0.03 0.02 0.03 Presbytis Mean 0.96 0.29 0.31 0.88 (n=5) Std 0.07 0.02 0.02 0.06 Nasalis Mean 0.93 0.28 0.31 0.88 (n=2) Std 0.04 0.02 0.02 0.01 C. diana Mean 0.71 0.30 0.30 0.88 (n=2) Std 0.06 0.01 0.01 0.10 C. nictitans Mean 0.88 0.26 0.29 0.92 (n=2) Std 0.01 0.03 0.03 0.11 C. mitis Mean 0.85 0.30 0.29 0.92 (n=4) Std 0.06 0.02 0.02 0.04 C. talapoin Mean 0.77 0.26 0.30 0.81 (n=3) Std 0.15 0.03 0.02 0.03 Cercocebus aterrimus Mean 1.02 0.36 0.24 1.06 (n=1) Std –– – – M. fascicularis Mean 0.73 0.33 0.29 0.93 (n=5) Std 0.11 0.02 0.01 0.05 SEMI-TERRESTRIAL C. neglectus Mean 0.86 0.31 0.28 0.88 (n=5) Std 0.11 0.01 0.006 0.04 C. hamlyni Mean 0.79 0.33 0.27 0.93 (n=2) Std 0.14 0.02 0.01 0.07 Cercocebus torquatus Mean 0.87 0.31 0.28 0.94 (n=6) Std 0.11 0.04 0.01 0.05 M. mulatta Mean 0.64 0.34 0.29 0.94 (n=3) Std 0.05 0.04 0.01 0.09 M. radiata Mean 0.76 0.33 0.29 0.94 (n=3) Std 0.05 0.02 0.01 0.04 M. maura Mean 0.74 0.34 0.31 0.88 (n=1) Std –– – – TERRESTRIAL Semnopithecus Mean 0.91 0.33 0.29 0.89 (n=3) Std 0.05 0.05 0.02 0.03 Rhinopithecus Mean 0.93 0.28 0.33 0.85 (n=10) Std 0.11 0.03 0.03 0.09 Theropithecus Mean 0.66 0.37 0.28 0.94 (n=6) Std 0.04 0.01 0.01 0.04 Papio Mean 0.64 0.36 0.29 0.97 (n=16) Std 0.07 0.02 0.02 0.07 Mandrillus Mean 0.71 0.37 0.27 1.07 (n=7) Std 0.09 0.02 0.01 0.11 Erythrocebus Mean 0.73 0.37 0.27 0.91 (n=3) Std 0.03 0.02 0.02 0.02 C. aethiops Mean 0.70 0.31 0.28 0.94 (n=7) Std 0.08 0.02 0.02 0.05 C. lhoesti Mean 0.73 0.31 0.29 0.89 (n=3) Std 0.12 0.01 0.003 0.04 M. nemestrina Mean 0.70 0.32 0.29 0.95 (n=4) Std 0.10 0.02 0.01 0.09 M. sylvanus Mean 0.64 0.34 0.29 0.94 (n=9) Std 0.07 0.02 0.01 0.03 D. Youlatos / Geobios 36 (2003) 229–239 233

Table 3 Means and standard deviations (std) of calcaneal indices of Colobinae, Cercopithecinae, all terrestrial, all semi-terrestrial, and all arboreal Cercopithecidae as defined in Table 1 (C1: relative form of the insertion of m. triceps surae; C2: relative length of the posterior (proximal) region of the calcaneus; C3: relative length of the proximal calcaneo-astragalar facet; C4: relative form of the proximal calcaneo-astragalar facet) Valeurs moyennes et écarts types (std) des indices calcanéens chez les Colobinae, les Cercopithecinae, et tous les Cercopithecidae terrestres, semi-terrestres et arboricoles comme définis au tableau 1 (C1 : forme relative de l’insertion des m. triceps surae ; C2 : longueur relative de la partie proximale du calcanéum ; C3 : longueur relative de la facette calcanéo-astragalienne proximale ; C4 : forme relative de la facette calcanéo-astragalienne proximale) C1 C2 C3 C4 Colobinae Mean 0.92 0.29 0.31 0.86 Std 0.09 0.03 0.03 0.07 Cercopithecinae Mean 0.72 0.33 0.28 0.94 Std 0.12 0.04 0.02 0.08 Terrestrial Cercopithecidae Mean 0.72 0.34 0.29 0.94 Std 0.13 0.04 0.03 0.09 Semi-terrestrial Cercopitheidae Mean 0.80 0.32 0.28 0.91 Std 0.12 0.03 0.01 0.07 Arboreal Cercopithecidae Mean 0.85 0.29 0.30 0.89 Std 0.13 0.03 0.02 0.07 differ significantly (Tables 3 and 4). In effect, arboreal and Tables 2–4). Significant differences are also found between terrestrial Colobinae bear significantly shorter proximal re- the two subfamilies with the Colobinae showing the longer gions than arboreal Cercopithecinae (Fig. 3 and Tables 2–4). facets (Table 2 and 4). In Mesopithecus, the relative length of Mesopithecus possess an intermediate proximal region and the facet approximates that of terrestrial and arboreal Colo- approximate the values obtained for semi-terrestrial Cercop- binae, the facet being significantly longer than those of all ithecinae (Table 2 and Fig. 3). The terrestrial Cercopitheci- locomotor groups of the Cercopithecinae (Tables 2 and 4 and nae possesses by far the longest proximal regions, differing Fig. 4). As a matter of fact, within each subfamily, there are significantly from all other locomotor-taxonomic groups no differences recorded between the different locomotor (Fig. 3 and Table 4). groups (Fig. 4 and Table 4), suggesting that this facet may be strongly outlined by phylogeny. The proximal calcaneo-astragalar facet allows the sliding excursions between calcaneus and talus at the lower ankle The relative form of this facet, as reflected by index C4, joint, responsible for eversion-inversion movements of the further depicts the extent of calcaneo-talar excursions in the foot. Index C3 reflects the relative length of this facet. Ter- lower ankle joint. This character is positively correlated to restrial Cercopithecidae bear relatively short facets, while body size (R = 0.332, F = 15.62, p < 0.001). Terrestrial arboreal ones possess significantly longer ones (Fig. 4 and Cercopithecidae show high values that indicate relatively

Table 4 Mann-Whitney U-test statistics. C1: reflects the relative shape of the insertion of m. triceps surae. C2: reflects the proportion of the posterior (proximal) region of the calcaneus. C3: reflects the relative extent of the proximal calcaneo-astragalar facet. C4: reflects the relative form of the proximal calcaneo-astragalar facet. Significant differences are in bold Tests U de Mann-Whitney. L’indice C1 reflète la forme relative de l’insertion des m. triceps surae. L’indice C2 reflète la proportion de la partie proximale du calcanéum. L’indice C3 reflète la longueur relative de la facette calcanéo-astragalienne proximale. L’indice C4 reflète la forme relative de la facette calcanéo-astragalienne proximale. Les différences significatives sont marquées en gras C1 C2 C3 C4 Colobinae-Cercopithecinae <0.001 0.008 <0.001 <0.001 Colobinae- Mesopithecus 0.002 0.012 0.324 0.500 Cercopithecinae- Mesopithecus 0.804 0.134 0.005 0.030 All terrestrial-all semi-terrestrial 0.004 0.055 0.123 0.196 All terrestrial-all arboreal <0.001 <0.001 0.015 <0.001 All arboreal-all semi-terrestrial 0.109 0.001 <0.001 0.093 Mesopithecus -terr. Colobinae 0.004 0.308 0.909 0.805 Mesopithecus -terr. Cercopithecinae 0.091 0.025 0.006 0.074 Mesopithecus -semi-terr. Cercopithecinae 0.159 0.458 0.006 0.345 Mesopithecus -arbor. Colobinae 0.003 0.147 0.125 0.881 Mesopithecus -arbor. Cercopithecinae 0.117 0.776 0.015 0.512 Terr. Colobinae-arbor. Colobinae 1.000 0.872 0.378 0.471 Terr. Cercopithecinae-arbor. Colobinae <0.001 <0.001 <0.001 <0.001 Terr. Cercopithecinae-arbor. Cercopithecinae <0.001 <0.001 0.103 0.002 Terr. Cercopithecinae-semi-terr. Cercopithecinae <0.001 0.002 0.408 0.023 Arbor. Cercopithecinae-semi-terr. Cercopithecinae 0.836 0.030 0.023 0.313 234 D. Youlatos / Geobios 36 (2003) 229–239

Fig. 2. Mean values (line in box), standard error (box edge), and standard deviation (line off box) of C1 index for terrestrial (TCE), semi-terrestrial (STC),and arboreal (ACE) Cercopithecinae, terrestrial (TCO) and arboreal (ACO) Colobinae, and Mesopithecus. Fig. 2. Valeurs moyennes (ligne à l’intérieur de la boîte), erreur standard (pourtour de la boîte), et écart type (ligne à l’extérieur de la boîte) de l’indice C1 des Cercopithecinae terrestres (TCE), semi-terrestres (STC), et arboricoles (ACE), des Colobinae terrestres (TCO) et arboricoles (ACO) ainsi que de Mesopithecus. short and wide facets and are significantly different from the Colobinae, which as a whole bear relatively long and arboreal forms that bear relatively long and narrow facets narrow facets (Tables 3 and 4). Mesopithecus seems to ex- producing lower values (Tables 2–4 and Fig. 5). Moreover, in hibit a remarkable variation, with C4 values similar to that of terms of subfamilies, the Cercopithecinae score higher than the Colobinae (both arboreal and terrestrial) and arboreal

Fig. 3. Mean values (line in box), standard error (box edge), and standard deviation (line off box) of C2 index for terrestrial (TCE), semi-terrestrial (STC), and arboreal (ACE) Cercopithecinae, terrestrial (TCO) and arboreal (ACO) Colobinae, and Mesopithecus. Fig. 3. Valeurs moyennes (ligne à l’intérieur de la boîte), erreur standard (pourtour de la boîte), et écart type (ligne à l’extérieur de la boîte) de l’indice C2 des Cercopithecinae terrestres (TCE), semi-terrestres (STC), et arboricoles (ACE), des Colobinae terrestres (TCO) et arboricoles (ACO) ainsi que de Mesopithecus. D. Youlatos / Geobios 36 (2003) 229–239 235

Fig. 4. Mean values (line in box), standard error (box edge), and standard deviation (line off box) of C3 index for terrestrial (TCE), semi-terrestrial (STC),and arboreal (ACE) Cercopithecinae, terrestrial (TCO) and arboreal (ACO) Colobinae, and Mesopithecus. Fig. 4. Valeurs moyennes (ligne à l’intérieur de la boîte), erreur standard (pourtour de la boîte), et écart type (ligne à l’extérieur de la boîte) de l’indice C3 des Cercopithecinae terrestres (TCE), semi-terrestres (STC), et arboricoles (ACE), des Colobinae terrestres (TCO) et arboricoles (ACO) ainsi que de Mesopithecus.

Cercopithecinae (Fig. 5). In fact, the form of the facet may terrestrial species bear significantly shorter and wider facets vary from long and narrow (PIK-239) to almost quadrangular than both the semi-terrestrial and arboreal representatives of (PIK-1745). On the other hand, among the Cercopithecinae, the subfamily (Table 4 and Fig. 5).

Fig. 5. Mean values (line in box), standard error (box edge), and standard deviation (line off box) of C4 index for terrestrial (TCE), semi-terrestrial (STC),and arboreal (ACE) Cercopithecinae, terrestrial (TCO) and arboreal (ACO) Colobinae, and Mesopithecus. Fig. 5. Valeurs moyennes (ligne à l’intérieur de la boîte), erreur standard (pourtour de la boîte), et écart type (ligne à l’extérieur de la boîte) de l’indice C4 des Cercopithecinae terrestres (TCE), semi-terrestres (STC), et arboricoles (ACE), des Colobinae terrestres (TCO) et arboricoles (ACO) ainsi que de Mesopithecus. 236 D. Youlatos / Geobios 36 (2003) 229–239

4. Discussion Mesopithecus falls in between, closer to semi-terrestrial spe- cies and more particularly, Cercopithecus neglectus and Cer- The work of inferring the paleobiology of fossil cocebus torquatus (Table 2), which both exploit the ground from selected postcranial elements requires the use of char- and lower forest strata (Jones and Sabatier-Pi, 1968; Gautier- acters that can be relatively safely attributed to different Hion, 1988). This intermediate morphology would provide functions and behaviours. As one of the well-preserved the necessary thrust while contributing to the required con- bones, the calcaneus has been frequently considered in many trolled plantar flexion in locomotors bouts on the ground and studies of functional morphology and reconstruction of the on branches. paleobiology of fossil (Szalay and Decker, 1974; In terrestrial walking and running, the necessary thrust Szalay and Langdon, 1986; Langdon, 1986; Strasser, 1988; would further require more developed foot plantar flexors. Gebo, 1989; Lewis, 1989). In this way, some calcaneal char- Dissections have shown that the Cercopithecinae, and espe- acters, such as the proximal region of the calcaneus, which is cially terrestrial species, possess bulkier m. triceps surae than the load arm of the main foot plantar flexor that inserts on its the Colobinae (Preuschoft, 1970; Strasser, 1988). A more very proximal end, and the relative length and shape of the powerful muscle would most likely be associated with a proximal calcaneo-astragalar facet, which express the extent larger insertion, lower and wider similar to that encountered of calcaneo-talar movements in the lower ankle joint, have on the proximal end of the calcaneus of terrestrial species. been well described and associated to certain functions of the Mesopithecus possesses an insertion that is intermediate be- foot. Previous studies have shown that both the characters tween the terrestrial and semi-terrestrial species (Fig. 2 and exhibit significant differences between arboreal and terres- Table 2). This may imply well-developed m. triceps surae trial species in certain taxonomic groups and have often been that would provide the necessary power for terrestrial activi- used successfully in the reconstruction of the positional be- ties. In contrast, arboreal species, and most particularly the haviour of many fossil mammals (e.g. Szalay and Decker, Colobinae, possess less developed m. triceps surae (Strasser, 1974; Langdon, 1986; Gebo, 1989; Prasad and Godinot, 1988). In their case, the bulky m. flexor digitorum contributes 1994; Szalay, 1994). In this study of the calcanei of the more to the powerful and controlled plantar and conjunct toe Cercopithecidae, both these characters were quantified in the flexion that are necessary in arboreal walking, climbing and form of four indices that resulted from selected measure- foot grasping (Badoux, 1974; Fleagle, 1983). These arboreal ments. All the indices succeeded in distinguishing well be- exhibit long and narrow m. triceps surae insertions; tween terrestrial and arboreal species of the family, and some fairly different from those of their terrestrial relatives (Figs. 1 of them in distinguishing between locomotor groups within and 2 and Table 2). Volkov (1903, 1904) first demonstrated the subfamilies (Tables 2–4 and Figs. 2–5). this difference but restrained it as one of the distinctive In general, the family Cercopithecidae is characterised by characters between the calcanei of Colobinae and Cercopith- relatively long proximal calcaneal regions compared to other ecinae. Indeed, all Colobinae, both terrestrial and arboreal, anthropoids (Strasser, 1988; Gebo, 1989). However, within exhibit the same narrow and high morphology. In contrast, the family, the Cercopithecinae possess significantly longer within the Cercopithecinae, there is a gradient where terres- regions than those of the Colobinae (Volkov, 1903, 1904). In trial species possess low and wide regions, while semi- terms of locomotor groups, this study showed that terrestrial terrestrial and arboreal species (e.g. many Cercopithecus species tend to possess significantly longer regions than both species) possess high and narrow insertion regions (Table 2 semi-terrestrial and arboreal forms; this is particularly evi- and Fig. 2). dent within the Cercopithecinae (Fig. 3). However, this char- With respect to the other calcaneal characters considered acter is positively correlated to body weight and Langdon in this paper, the general morphology of the proximal (1986) suggested caution in any functional interpretations, calcaneo-astragalar facet of the Cercopithecidae is generally but it was shown that even similar-sized Cercopithecidae short, wide and set steeply on the calcaneal body (Langdon, with different positional activities possess different proximal 1986; Strasser, 1988; Gebo, 1989). Furthermore, the two regions. The proximal region of the calcaneus is considered subfamilies are quite distinct, with the Colobinae bearing as the load arm of the foot whereupon acts the force exerted relatively longer and narrower facets than the Cercopitheci- by m. triceps surae, the main plantar flexor of the foot. Thus, nae (Szalay, 1975; Strasser, 1988), a fact supported by the a longer lever arm is associated with a better leverage of foot findings of this study (Table 3). In Mesopithecus, the facet is plantar flexion that provides the necessary rapid propulsion quite long, more reminiscent in form of that of the Colobinae during the accelerating phase of terrestrial cursorial activities to which they belong phylogenetically (Figs. 1 and 4). On the (Badoux, 1974; Fleagle, 1983; Strasser, 1988). In contrast, other hand, Mesopithecus showed a remarkable variation in arboreal species that move within a complex fragile and the form of this facet that ranged from narrow to almost a discontinuous milieu would require more cautious and pre- square-shaped structure (Fig. 5). In functional terms, a long cise movements of the foot on branches. Powerful and con- and narrow proximal facet appears to favour ampler subtalar trolled plantar flexion would be more advantageous in such excursions between the talus and calcaneus. This extended activities and is favoured by shorter proximal calcaneal re- sliding function at the lower ankle joint enhances proximal gions (Badoux, 1974; Fleagle, 1983). The proportion of inversion and eversion of the foot that facilitates its place- D. Youlatos / Geobios 36 (2003) 229–239 237 ment on the branches during arboreal walking and climbing ern species and their adaptations, have paralleled Pikermi (Langdon, 1986; Lewis, 1989). Such excursions are particu- with savanna habitats similar to that of modern East Africa larly pronounced in hominoids and atelines, where the sig- (Gaudry, 1862-1867; Delson, 1975; Mistardis, 1977). How- nificantly long facets permit a helicoid movement (Langdon, ever, the browsing type of ruminants that dominate, may also 1986; Lewis, 1989). This helicoid movement was considered indicate a closer, woodland environment (Solounias and to have been lost within the whole of Cercopithecidae (Sza- Dawson-Saunders, 1988; Solounias et al., 1999). Recent lay, 1975; Szalay and Langdon, 1986; Lewis, 1989), but multivariate analyses of past and recent mammalian commu- apparently still persists in the relatively long and narrow nities have shown that Pikermi usually clusters with more facets of the Colobinae. These ample movements are associ- savanna-like paleoenvironments, following the general dry- ated with the general shift to arboreality that characterises ing of the climate in the Greco-Iranian Province during the many postcranial features of this subfamily (Szalay, 1975; Turolian (de Bonis, 1992, 1999). Thus, the combination of Strasser, 1988).A similar trend is also encountered within the some woodland mammals with more open habitat represen- different species of the Cercopithecinae clade. Both indices tatives might indicate that Pikermi was an open savanna (C3, C4) produced separate locomotor groups with semi- cruised by rivers with gallery forests and ephemeral ponds terrestrial and arboreal representatives of the subfamily ex- surrounded by forested patches. If Pikermi were such a hibiting relatively longer and narrower facets, while terres- habitat, then it would be expected for Mesopithecus to be trial species possess short and relatively wide facets (Figs. 4 well suited for such a patchy habitat, being at ease on the and 5). The latter morphology seems to function as a hinge, trees as on the ground in order to be able to forage and shelter limiting any unnecessary ample calcaneo-talar excursions, between isolated patches of trees. and mainly accommodates a close-packed condition between This way of life may explain the postcranial adaptations to the two bones that would prevent any dislocations under the semi-terrestriality in a genus that belongs to a merely arbo- high stresses of terrestrial cursorial activities (Langdon, real subfamily. In fact, the Colobinae are considered to have 1986). modified the originally semi-terrestrial foot adaptations of The two calcaneal characters examined in this paper show the stem Cercopithecidae (as also seen in the Victoriapith- that the calcanei of Mesopithecus pentelicus present a mosaic ecidae) to an increased supination and a shifting of the morphology that combines features of both subfamilies as functional axis for novel grasp of the foot on arboreal sup- well as features that are functionally associated with terres- ports (Szalay, 1975; Langdon, 1986; Strasser and Delson, trial and arboreal activities. In effect, the relative length and 1987; Strasser, 1988). In the case of the calcaneal characters shape of the proximal calcaneal facet is mostly similar to the examined, the generally short and squared proximal facet form observed in the Colobinae. This feature is functionally and the relatively long proximal region of the Cercopith- associated with increased calcaneo-talar movements that en- ecidae evolved to a more elongate and narrow facet and a hance foot inversion which is necessary for its placement on relatively shortened proximal region, respectively. These fea- arboreal supports. On the other hand, the relative form of the tures promoted more powerful and controlled plantar flexion insertion of m. triceps surae and the relative length of the of the foot as well as ample lower joint mobility, and are proximal calcaneal region approximate those of the semi- presumed to form an integrated unit that evolved simulta- terrestrial representatives of the Cercopithecinae. This set of neously, when the subfamily reinvaded the tree crowns of features is functionally associated with rapid thrust for foot rainforests in Africa some 14 mya (Strasser, 1988; Stewart plantar flexion, habitually occurring in terrestrial running and Disotell, 1998). and walking. Thus, the calcaneal features of M. pentelicus At around 10 mya, a group of Colobinae invaded Eurasia discussed here indicate a foot capable of powerful and rapid (Stewart and Disotell, 1998). This group involves the fossil plantar flexion, combined with lower ankle joint mobility genera Mesopithecus and Dolichopithecus that were spread enhancing inversion and eversion movements. Such findings throughout Europe and western Asia and became extinct by suggest that M. pentelicus could move at ease on arboreal as the end of the Pliocene (Szalay and Delson, 1979; de Bonis et well as terrestrial substrates, implying a semi-terrestrial habi- al., 1990; Gentili et al., 1998; Sen, 1998). Both fossils are tus. This conforms to observations of other postcranial re- found in relatively open habitats and evolved foot features mains, such as limb proportions, the posteromedial direction that favoured rapid foot plantar flexion, while retaining a of the medial epicondyle, the well-developed humeral tro- certain lower ankle joint mobility. These movements are chlea, the retroflexed olecranon process, the straight ulnar associated with the relative elongation of the proximal region shaft, the robustness of the long bones and the phalanges and and the enlargement of m. triceps surae insertion for a second other calcaneal and talar characters (Gaudry, 1862; Gabis, time, while retaining the relatively long and narrow proximal 1960; Szalay and Delson, 1979; Zapfe, 1991; Youlatos, calcaneal facet as an inheritance of the Colobinae. 1999). If Mesopithecus is considered as basal Colobinae and a But can the paleoenvironment of Mesopithecus support sister group to all extant forms (Hohenneger and Zapfe, this semi-terrestrial tendency? The reconstruction of the pa- 1990; Zapfe, 1991), then the shorter proximal calcaneal re- leoenvironment of Pikermi is still in debate. Many research- gion, the high and narrow insertion, and less, the long and ers, based on the analogy of Pikermian mammals with mod- narrow proximal facet of extant Asian Colobinae, the Pres- 238 D. Youlatos / Geobios 36 (2003) 229–239 bytina, would be characters that were inherited from the 1998). More upcoming research in the relationships between arboreally adapted stem group that migrated out of Africa extant and extinct Colobinae, the study of behavioural ecol- and spread throughout Asia. Such a scenario would have ogy and positional activities of recent species, as well as required arboreal pathways towards south-east Asia in a more detailed revisions of the geological events of Miocene- period of general drying and forest decline (Delson, 1975; Pliocene of the eastern Mediterranean region and western Sen, 1998). In this case, the foot features considered here in Asia will undoubtedly shed more light on the evolutionary both African and Asian Colobinae would have been parsimo- history of the subfamily and help establish the polarity of niously inherited from the morphotype of the Colobinae. cranial and postcranial characters in order to reconstruct the On the other hand, if Mesopithecus is considered as ances- biology of extinct forms. tral to extant Presbytina (see Jablonski, 1998), then the shorter proximal region, the high and narrow insertion, and the long and narrow proximal facet of the latter can be Acknowledgements considered as recent acquisitions to a new shift to arboreality when they invaded the still forested southern parts of Asia. In I am greatly indebted to Profs. L. de Bonis (Université de this case, the Colobina would have inherited and probably Poitiers) and J.-P. Gasc (MNHN) for their support and further developed the arboreal habitus of early Colobinae, thoughtful discussions on functional morphology during the while the Presbytina would have independently acquired completion of this work. Profs. L. Ginsburg, D. Robineau, their arboreal adaptations. Differences in foot morphology and H. de Lumley provided access to the collections of the do exist between the two groups but further research is Institut de Paléontologie, the Laboratoire d’Anatomie Com- required to establish the polarity of the characters (Strasser, parée, and the Laboratoire d’Anthropologie Biologique of 1988). This would have further implied that the calcaneal the MNHN. This report is part of an M.Sc. dissertation at the features considered here (especially the m. triceps insertion Université Paris-6. I also wish to thank Prof. G. Koufos and its load arm) exhibit a great evolutionary plasticity with (Aristotle University of Thessaloniki) for constructive re- modifications throughout evolutionary time following marks on the drafts of this paper. Prof. L. de Bonis and an habitat-habitus changes. The plasticity of these features may anonymous reviewer improved this paper. also be supported by the differences observed within the Cercopithecini, which involve terrestrial, semi-terrestrial and arboreal species. The evolutionary history of the tribe is not References well known, but positional adaptations are considered rela- tively novel (Gebo and Sargis, 1994; Stewart and Disotell, Badoux, D.M., 1974.An introduction to biomechanical principles in primate 1998). Semi-terrestrial and arboreal species separated well locomotion and structure. In: Jenkins Jr, F.A. (Ed.), Primate Locomotion. from their terrestrial representatives in almost all indices Academic Press, New York, pp. 1–43. (Figs. 2–5), a fact also observed in other postcranial elements Bonis, L. de, Bouvrain, G., Geraads, D., Koufos, G., 1990. New remains of of the tribe; but details on their positional activities are still Mesopithecus (Primates, Cercopithecoidea) from the late Miocene of far from known to test such hypotheses. Macedonia (Greece), with the description of a new species. Journal of Vertebrate Paleontology 10, 473–483. Bonis, L. de, 1992. Diversity and paleoecology of Greek late Miocene 5. Conclusions mammalian faunas. Palaeogeography Palaeoclimatology Palaeoecology 91, 99–121. The calcaneal features considered in this paper succeeded Bonis, L. de, 1999. Palaeoenvironments of late Miocene primate localities in in distinguishing between terrestrial and semi-terrestrial and Macedonia, Greece. In: Agusti, J., Rook, L., Andrews, P. (Eds.), Homi- arboreal species of Cercopithecidae. Among them, the Piker- noid Evolution and Climatic Change in Europe, vol. 1. 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