The Morphology of Oreopithecus bamboliiPollical Distal Phalanx

Sergio Alm�ecija,1,2,3* Marvin Shrewsbury,4 Lorenzo Rook,5 and Salvador Moy�a-Sol�a6

1Department of Anatomical Sciences, Stony Brook University School of Medicine, Stony Brook, NY 11794-80812Department of Vertebrate Paleontology, American Museum of Natural History and NYCEP, New York, NY 100243Institut Catal�a de Paleontologia Miquel Crusafont, Universitat Aut�onoma de Barcelona, Cerdanyola del Valles,Barcelona 08193, Spain4Wailuku, HI 967935Dipartimento di Scienze della Terra, Universit�a di Firenze, Firenze 50121, Italy6ICREA at Institut Catal�a de Paleontologia Miquel Crusafont and Unitat d’Antropologia Biol�ogica (Dept. BABVE),Universitat Aut�onoma de Barcelona, Cerdanyola del Valles, Barcelona 08193, Spain

KEY WORDS Miocene apes; hominoid hand evolution; thumb morphology; precisiongrasping

ABSTRACT Oreopithecus bambolii is a Late Mioceneape from Italy, first described in the late 19th century.Its interpretation is still highly controversial, especiallyin reference to its hand proportions and thumb morphol-ogy. In this study, the authors provide detailed descrip-tions of the available Oreopithecus pollical distalphalanx (PDP) specimens, as well as bivariate and mul-tivariate morphometric analyses in comparison withhumans, extant apes, selected anthropoid monkeys, andavailable Miocene PDP specimens. The multivariateresults reveal two opposite poles on the hominoid PDPshape spectrum: on one side, a mediolaterally broad anddorsopalmarly short human PDP, and on the other side,the narrow and “conical” PDP of chimpanzees andorangutans. The authors contend that Oreopithecusexhibits intermediate PDP proportions that are largelyprimitive for hominoids because it shares morphological

similarities with Proconsul. Furthermore, Oreopithecusdisplays a mediolaterally wide tuft for a hominoid, aswell as a palmarly elevated attachment for a long ten-don of a flexor muscle that is associated at its proximaledge with a proximal fossa and at its distal edge with anungual fossa. These nonmetrical traits have been associ-ated in humans with their capability to oppose and con-tact the proximal pads of the thumb and fingers, that is,pad-to-pad precision grasping. These traits reinforce pre-vious studies that indicate a human-like thumb-to-handlength ratio compatible with pad-to-pad precision grasp-ing in Oreopithecus. Although specific hand use is stillunresolved in Oreopithecus, the results suggest enhancedmanipulative skills (unrelated to stone tool-making) inthis taxon relative to other (extant or fossil) hominoids.Am J Phys Anthropol 153:582–597, 2014. VC 2014 Wiley

Periodicals, Inc.

Oreopithecus bambolii is a Late Miocene ape (ca. 8.2–6.7 Ma; Rook et al., 2000; Casanovas-Vilar et al., 2011;Rook et al., 2011; Matson et al., 2012) first discovered byCocchi in 1862 in the lignite mines of the Monte Bamboli(Tuscany, Italy), from which the fossil was named (Ger-vais, 1872; H€urzeler, 1958; Berzi, 1973). Since then,more remains have been found in several localities ofthe paleoisland of Tuscany-Sardinia (Rook et al., 2006;Abbazzi et al., 2008). The most complete specimen is apartial skeleton, nicknamed “Sandrone” found in a coal-mine in Baccinello (Grosseto) in 1958 by H€urzeler(Straus, 1958). Over the years, the interpretation ofOreopithecus has been highly controversial, being alter-natively interpreted as a separate anthropoid lineagebelonging to its own family (Oreopithecidae) or fitting inwith cercopithecoids (Schlosser, 1887; Szalay and Delson,1979), hominoids (Schwalbe, 1915; Straus, 1963; Harri-son, 1986; Sarmiento, 1987), or even within early homi-nins (H€urzeler, 1954; Straus, 1957). For a historicalreview of Oreopithecus taxonomy, see the work of Delson(1986). One of the most controversial aspects of Oreopi-thecus has been its hand, especially the thumb, to whichseveral studies have been devoted.

Moy�a-Sol�a et al. (1999, 2005b) proposed that Oreopi-thecus possessed a short hand relative to its body mass,with a thumb-to-finger length ratio similar to modern

humans and baboons. Its pollical distal phalanx (PDP)showed a well-developed fossa on the proximal palmarsurface for an inferred insertion of the flexor pollicis lon-gus (FPL) tendon. This was interpreted by these authorsas indicative of specific adaptations for a “human-likepad-to-pad precision grasping” (see below) in this taxon,which evolved convergently with later hominins as aresult of relaxed forelimb-dominated locomotor behaviorsas well as for efficient harvesting and feeding (K€ohler

Grant sponsor: Generalitat de Catalunya and Fulbright Commis-sion; Grant number: 2009 BFUL 00049, 2009 BP-A 00226; Grantsponsor: Spanish Ministerio de Econom�ıa y Competitividad; Grantnumber: CGL2011-27343, 2009 SGR 754 GRC; Grant sponsor:American Association of Physical Anthropologists, ProfessionalDevelopment Program.

*Correspondence to: Sergio Alm�ecija, Department of AnatomicalSciences, Stony Brook University School of Medicine, Stony Brook,NY 11794, USA. E-mail: sergio.almecija@stonybrook.edu

Received 18 March 2013; accepted 25 November 2013

DOI: 10.1002/ajpa.22458Published online 7 January 2014 in Wiley Online Library

(wileyonlinelibrary.com).

� 2014 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 153:582–597 (2014)

and Moy�a-Sol�a, 1997; Moy�a-Sol�a et al., 1999; Rook et al.,1999).

Susman (2004, 2005) replied to both the above-mentioned communications, proposing that Oreopithecusdisplayed a basic modern-ape hand morphology and thatthe results of Moy�a-Sol�a and coauthors were based onwrongly identified phalangeal specimens. Susman fur-ther stated that a FPL insertion (i.e., the palmar fossadescribed by Moy�a-Sol�a and coauthors) was not identi-fied before by previous studies of the IGF 11778 speci-men. Moy�a-Sol�a et al. (2005b) clarified that the fossawas not visible until more recently when both specimenswere properly prepared and cleaned. A later communica-tion by Marzke and Shrewsbury (2006) pointed out thatthe presence of a proximal fossa in the PDP of Oreopi-thecus as well as in any other primate is not directlyrelated to a FPL insertion. Instead, Shrewsbury et al.(2003) found that the FPL attachment is reflected in agable-shaped ridge, elevated palmarly, which is at thedistal border of the fossa itself [Shrewsbury’s proximalvolar fossa (PVF)]. Although some of these features canbe present in extant primates (Susman, 1998; Shrews-bury et al., 2003), only humans display a complex set ofcharacters on their PDPs (a broad base, sesamoid facet,PVF, gable FPL attachment, ungual fossa, ungualspines, and a mediolaterally wide apical tuft). This com-plex is related to the use of the thumb and the other dig-its in specific types of precision gripping during refinedmanipulation and handling (i.e., pad-to-pad precisiongrasping; see the next section).

WHAT IS HUMAN-LIKE PAD-TO-PAD PRECISIONGRASPING?

The term “precision grasping” is often used in theprimate hand literature with different connotationsbetween primatologists and anthropologists sensu

stricto, and this has led to confusion and unnecessaryarguments. However, “disagreement, as is so often thecase, is largely attributable to a semantic difficulty”(Napier, 1960, p 654). Most primates can contact the tipof their thumb and index finger during different kinds ofprecision grasping in a broad sense. This implies aninteraction between both hand rays (e.g., Christel, 1993;Pouydebat et al., 2008), especially in opposition to“power grasping” where the thumb plays a secondaryrole by securing the grip against the palm and directingthe force being applied (Napier, 1960, 1993). Thus, inthe general sense of precision grasping, even chimpan-zees and orangutans (the great apes that exhibit moredisproportionate thumb-to-hand length proportions;Schultz, 1930), are capable of manipulating objects bymeans of different kinds of hand and index finger“precision grip” interactions (e.g., thumb and index fin-ger tip-to-tip and pad-to-side; Fig. 1). Relevantly, this isnot the specific precision grasping we are addressing inour study.

As discussed by Marzke et al. (2009) and in previousstudies by some of us (Alba et al., 2003; Moy�a-Sol�aet al., 2008; Alm�ecija et al., 2009a, 2010), it is importantto recall that what Napier originally meant by a human“advanced precision grip” (Napier, 1960) was an uniquecapability for holding objects between the thumb andthe index finger, “delicately yet securely between theopposed pulp surfaces” (Napier, 1960, p 652). Amongextant hominoids, however, a pad-to-pad precision grasp-ing (i.e., contact of the proximal portion of the thumband index pulps) is restricted to humans. This type ofgrasping is largely precluded in the other taxa (andespecially Pan and Pongo) due to the disproportionatelength of their Digits II–V relative to the thumb (Fig.1a,b; Napier, 1960; Tuttle, 1967, 1969, 1970; Napier,1993), as well as by restricted passive hyperextension ofthe distal phalanges caused by relatively short flexor

Fig. 1. Human hand (a and c) in comparison with a chimpanzee hand (b and d). Notice the length and robusticity of thehuman thumb in relation to the other fingers. In comparison, chimpanzees show elongated fingers relative to the thumb. A human-like thumb pad to index finger pad precision grip (c) is not possible in great apes due to the disproportion in length between thethumb and the fingers, although other kinds of precision grip are possible (d). Panels (a)–(c) are modified from Figures 24 and 27in Napier (1993), and Panel (d) is modified from Figure 6 in Christel (1993). Images are not to scale.

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 583

American Journal of Physical Anthropology

tendons (Tuttle, 1967; Christel, 1993). As a clarificationto Pouydebat et al. (2008), Marzke et al (2009) notedthat Napier considered only the pad-to-pad contact (Fig.1c) to be the “acme” of human precision grasping (Nap-ier, 1960, p 652), involving “perfect” opposition of pulpsurfaces of the thumb and index finger (Napier, 1993, p55–56). This type of precision grip with its related mor-phology on the pollical distal phalanges was describedby Shrewsbury et al. (2003) and proposed to be exam-ined in Oreopithecus in this relation (Marzke andShrewsbury, 2006).

Two PDPs were figured and described previously forOreopithecus (Moy�a-Sol�a et al., 1999; Moy�a-Sol�a andK€ohler, 2003; Susman, 2004): the specimen that wasassociated with the left hand of the partial skeleton IGF11778 and was assigned to a young adult (with somedamage in the radial side of the base and tuft) andBA#130, found among the collection of Oreopithecusspecimens collected by H€urzeler and housed in Basel(Berzi, 1973). The association of most postcranialremains in these collections is unclear and currentlyunder study (Alm�ecija et al., manuscript in preparation).BA#130 is slightly smaller than IGF 11778 and lacks theproximal base just prior to the epiphysis (Fig. 3). Thus,

its ontogenetic status and side are unknown. AnotherOreopithecus PDP, associated with the juvenile handBA#140 was diagenetically flattened (as the rest of thehand), eliminating evaluation of surface palmar anat-omy. To evaluate and clarify the Oreopithecus thumbmorphology, IGF 11778 and BA#130 are reexamined inthis study, taking into account the pad-to-pad suite offeatures for precision grasping displayed by humans.Furthermore, this study provides a complete morpho-metric analysis of the Oreopithecus PDP from the IGF11778 partial skeleton and available Miocene fossilspecimens.

MATERIALS AND METHODS

Anatomical descriptions are primarily informed by thewell-preserved PDP belonging to the left hand of theIGF 11778 skeleton, supplemented by observations ofthe more partial BA#130 specimen. Most of the anatomi-cal terms used here are described and analyzed else-where (Shrewsbury et al., 2003). Apart from anatomicaldescriptions, the main proportions of the Oreopithecusmore complete PDP specimen (IGF 11778) were com-pared with a modern sample of primates, including

TABLE 1. Pollical distal phalanx measurements and summary statistics (in mm)

L DPT MLT DPMS MLMS DPB MLB

Alouatta (n 5 4) Mean 13.18 2.13 2.35 2.15 2.23 3.05 4.65SD 0.87 0.29 0.17 0.19 0.10 0.44 0.26

Range 12.5–14.4 1.7–2.3 2.2–2.5 1.9–2.3 2.1–2.3 2.5–3.5 4.4–5Nasalis (n 5 9) Mean 8.07 2.26 2.91 2.12 2.51 3.13 5.51

SD 1.08 0.27 0.40 0.38 0.40 0.40 0.77Range 6.7–9.6 1.9–2.7 2.3–3.5 1.6–2.6 2.0–3.0 2.5–3.6 4.5–6.4

Macaca (n 5 5) Mean 7.66 1.72 3.10 1.64 2.98 2.84 5.94SD 0.73 0.18 0.50 0.22 0.37 0.25 0.83

Range 7–8.9 1.5–1.9 2.6–3.9 1.3–1.9 2.5–3.5 2.5–3.2 5–7.1Papio (n 5 29) Mean 9.42 2.31 4.49 2.23 3.32 4.32 7.09

SD 1.03 0.37 0.62 0.26 0.44 0.51 0.72Range 6.7–11.2 1.8–3.3 3.2–6 1.8–2.8 2.5–4.2 3.4–5.4 5.9–8.5

Hylobates (n 5 11) Mean 9.67 1.96 2.93 1.77 3.06 2.90 5.64SD 0.66 0.14 0.27 0.27 0.40 0.19 0.48

Range 8.6–10.5 1.7–2.2 2.6–3.5 1.5–2.4 2.4–3.7 2.6–3.2 4.9–6.5Pongo (n 5 18) Mean 15.21 3.24 4.34 3.50 3.31 6.00 8.68

SD 2.20 0.49 0.95 0.33 0.58 0.88 1.37Range 12.1–19.2 2.5–4.2 3.1–6.7 2.9–4.1 2.2–4.5 4.5–8 7–12.1

Gorilla (n 5 18) Mean 20.86 4.81 7.18 4.20 5.69 7.80 12.94SD 2.62 0.73 0.88 0.50 0.77 0.86 1.58

Range 16.5–25.5 3.3–6.1 5.3–9.1 3.2–5.1 4–6.8 6.1–9.2 9.3–15.3Pan (n 5 33) Mean 18.06 3.69 4.78 3.71 3.54 5.80 8.53

SD 1.81 0.56 0.90 0.51 0.48 0.70 0.84Range 15.3–21 2.8–5.6 2.8–6.7 2.85.3 2.7–4.6 4.6–7.3 7–10.2

H. sapiens (n 5 25) Mean 22.32 3.43 9.28 4.47 7.44 8.22 14.03SD 1.74 0.43 1.12 0.56 0.79 0.68 1.09

Range 19.1–26 2.54.2 7.1–11.1 3.4–5.3 6–8.7 7–9.7 12–16.3Proconsul KPS1-PH96 11.4 2.5 3.5 2.4 3.6 3.3 5.4Pierolapithecus IPS 21350.16 18.8 3.9 4.4 4.6 5.3 – 8.8Oreopithecus IFG 11778 actual (16.5) 3.8 6 3.8 4.3 5 (8.8)Oreopithecus IFG 11778 corrected 16.8 3.8 6 3.8 4.3 5 10Oreopithecus BA#130 – 3.8 4.5 3.8 3.7 – –Orrorin BAR 1901’01 19.2 4.7 7.6 4.9 6.2 6.2 11.1

The extant sample includes the following species: Alouatta seniculus, Macaca nemestrina, Papio cynocephalus, Nasalis larvatus,Pongo pygmaeus and P. abelii, Pan troglodytes and P. paniscus, Gorilla gorilla and G. beringei, Homo sapiens, and Hylobates lar.Parentheses in the actual IGF 11778 specimen represent the preserved measurements. They are marked in bold font to easily com-pare with the inferred measurements from the reconstructed digital model. Midshaft was estimated in BA#130 to take the meas-urements. All measurements are given in maximum lengths.Abbreviations: L, proximodistal length; DPT, dorsopalmar tuft; MLT, maximediolateral tuft; DPMS, dorsopalmar midshaft; MLMS,mediolateral midshaft; DPB, dorsopalmar base; MLB, mediolateral base.

584 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

modern humans, all extant great ape genera, Hylobates,as well as selected platyrrhine and cercopithecoid mon-keys (see Table 1 for sample details). A single Theropi-thecus gelada specimen available was inspected forcomparison but not included in the analyses. The fossilcomparative sample includes the most complete avail-able PDP specimens from the Miocene. The completephalanx (PH 96) associated with the juvenile Proconsulheseloni individual I from the Kaswanga Primate Site(Early Miocene of Rusinga Island, Kenya; Begun et al.,1994), IPS 21350.16, with a slightly damaged base anderoded palmar surface, is attributed to the skeleton ofthe fossil Middle Miocene great ape from Spain Pierola-pithecus catalaunicus (Moy�a-Sol�a et al., 2004; Alm�ecijaet al., 2009b). Another complete phalanx is attributed tothe early hominin Orrorin tugenensis from the Late Mio-cene of Kenya (Gommery and Senut, 2006; Alm�ecijaet al., 2010). A PDP attributed to Afropithecus (KNM-WK 17032) from the early Miocene of Kenya has beenreported (Leakey et al., 1988), although it is actually anon-PDP, probably belonging to one of the lateral rays ofthe foot (Sergio Alm�ecija, personal observation). All fos-sils were measured from the original specimens with theexception of Orrorin, which was measured from a high-quality research cast. Although both Oreopithecus PDPspecimens are incomplete, the main proportions of theactual IGF 11778 can be confidently estimated (i.e.,incompletely preserved maximum length and mediolat-eral width of the base) from a “corrected” digital model.We copied, mirror-imaged, and pasted the ulnar tubercleand tuft onto the radial side and filled in the distal endfollowing the tuft curvature in Geomagic software (ver.2012).

To evaluate the main proportions of IGF 11778 in com-parison with our PDP sample, seven standard measure-

ments (Fig. 2) were collected to the nearest 0.1 mm. ForIGF 11778, both measurements are given for the actualbone (with preserved dimensions) as well as the esti-mated length and base widths. To facilitate shape com-parisons, all PDP specimens were size-adjusted bydividing each original length by the overall PDP size,approximated by the geometric mean (GM) of the avail-able original measurements. Thus, each one of theseratios provides a dimensionless “Mosimann shape varia-ble” of the respective original dimension (Mosimann,1970; Jungers et al., 1995). The mediolateral expansionof the apical or ungual tuft (referenced as tuft, from nowon) relative to the PDP base (expansion index: mediolat-eral tuft width/mediolateral base width 3 100) was foundto be correlated in humans with pulp development (Mit-tra et al., 2007). Thus, to inspect the degree of pulp devel-opment in the Oreopithecus thumb relative to otheranthropoid primates, Mittra’s expansion index was fur-ther examined in IGF 11778. The significance of differen-ces in mean values for this index was tested by means ofanalysis of variance and post hoc multiple comparisons(Bonferroni method). Allometric scaling of the tuft wasalso considered to know if tuft width development cova-ries predictably with overall PDP size. Least squaresregressions of log-transformed (using natural logarithms)mediolateral tuft width versus PDP size (approximatedagain by the GM) were computed independently for eachtaxa. Homogeneity of slopes was tested by means of anal-ysis of covariance (ANCOVA), and post hoc multiple com-parisons (Bonferroni method) were performed onestimated marginal means (generic means adjusted forcovariate effects) to check for differences in the elevationbetween the different taxa examined.

Major trends of shape variation between species in ourprimate PDP sample were summarized by means of aprincipal components analysis (PCA) computed on thecovariance matrix of extant species shape ratios meansand fossil specimens. In addition to the full set of sevenshape variables, this analysis was repeated with the sixavailable lengths in the Pierolapithecus PDP, as a meansof including the latter specimen in the morphometriccomparisons. All analyses were performed using SPSSver. 17 and PAST (Hammer et al., 2001). As a sensitivitytest, all analyses include the actual available measure-ments from the specimen (thus, including incompletelengths), as well as the maximum estimated measure-ments (total length and mediolateral base breadth) fromthe corrected IGF 11778. Both specimens are analyzedas different operational taxonomic units. Detailed closeups to the Oreopithecus PDP specimens are provided inFigure 3, and Figure 4 provides morphological compari-sons with representative specimens of the comparativesample.

RESULTS

Anatomical descriptions

One of the main points that Marzke and Shrewsbury(2006) stressed regarding the Oreopithecus PDP mor-phology was that the attachment for the FPL just distalto the proximal fossa (PVF of Shrewsbury et al., 2003)would be functionally important for inferring precisiongrasping in Oreopithecus rather than the fossa per se. Itis worth mentioning that it is not possible to knowwhether or not the flexor tendon insertion found in fossilPDPs really belongs to an independent FPL or from theradial portion of the flexor digitorium profundus (FDP)

Fig. 2. Measurements used in this study are shown in pal-mar and lateral views of a modern human pollical distal pha-lanx (PDP).

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 585

American Journal of Physical Anthropology

Fig. 3. Pollical distal phalanges of Oreopithecus bambolii. Both individuals have been previously depicted and figured else-where (Moy�a-Sol�a et al., 1999, 2005b). In this figure, we represent them by means of high-resolution surface laser scans to showthe surface detail anatomy discussed in the text. BA#130 is depicted in palmar (a) and oblique lateropalmar (b) views. IGF 11778is depicted in palmar (c), oblique ulnopalmar (d), dorsal (e), and proximal (f) views. A digitally corrected version of IGF 17788shows its main proportions in palmar (g), ulnar (h), and proximal (i) views. Color code is as follows: orange 5 proximal volar fossa;red 5 flexor pollicis longus attachment; green 5 ungual fossa; blue 5 tuft; purple 5 extensor pollicis longus insertion.

Fig. 4. Morphological comparisons. Pollical distal phalanges of the taxa examined are compared with an overall similar size.Color code is as follows orange 5 proximal palmar fossa (PVF of Shrewsbury et al., 2003), referred here as palmar fossa in taxaextending over the whole palmar surface; red 5 flexor tendon attachment; green 5 ungual fossa; blue 5 palmarly protruding distaltuft. Among extant taxa, only humans and Hylobates have a proper flexor pollicis longus (FPL) muscle with a palmarly protrudinginsertion attachment for its tendon (marked in bold red). Only hominins and Oreopithecus exhibit an ungual fossa (green) inbetween the attachment for the FPL (bold red) and a palmarly protruding tuft (blue).

as observed in other primates (Susman, 1998; Diogoet al., 2012) or even to another anomalous muscle ten-don. Thus, in this article, when describing fossils, wewill only denote the presence or absence of a flexor mus-cle tendon.

In palmar view, BA#130 (of uncertain side attribution)shows two elevated tubercles connected by a nonelevatedisthmus (Fig. 3a). The left one is poorly developed,whereas the right one, which is situated slightly distally,is more palmarly raised. By contrast, the proximal baseof IGF 11778 (from the left hand) displays very distinctulnar and radial tubercles on the palmar surface at thedistal margin of the PVF. These two elevated markingsstrongly suggest radial and ulnar attachments of a flexormuscle’s tendinous band. The two sides of the flexorband are connected by a proximodistally narrow andslightly elevated isthmus between the two tubercles forpossible attachment of central slips of the flexor tendon(Fig. 3c). In palmar view, the radial tubercle of IGF11778 is slightly larger than the ulnar, which is situatedslightly more distally than the radial. These tubercleswere discernible in previously published figures of thesespecimens (Moy�a-Sol�a et al., 1999, 2005b); however, theyreceived little deliberation. In both specimens, the twodistinct tubercles on the proximal palmar surface of thePDP delineate a proximal region as a PVF and a distaldepressed area as the ungual fossa over the entire dia-physis of the PDP. IGF 11778 displays a more proximallyconstricted PVF (Fig. 3c,d), whereas BA#130 shows alarger proximodistally extending PVF (Fig. 3a,b). IGF11778 shows no noticeable sesamoid facet at the palmarmidline base of the PDP for an articulation with a sesa-moid bone or cartilage within the palmar plate (Fig. 3c).The base is too incomplete in BA#130 to make such anobservation, regarding the presence or absence of anysesamoid facet. From the palmar surface markings onthese two PDPs, it is not possible to suggest if any satel-lite slips of the flexor tendon attachments were present,as can be observed during dissections for humans or forbaboons (Shrewsbury et al., 2003). There are no noticea-ble ungual spines in either specimen for which satelliteslips of the flexor tendon can be attached. What can beinferred is that a pollical flexor tendon has attachmentsto the two proximal palmar tubercles on the palmar sur-face of the PDP.

Distal to the two tubercles, the diaphysis of thesetwo PDPs contains an ungual fossa (Fig. 3a–d),which extends distally to the base of a slightly pal-marly protruding tuft at the PDP distal end. Eventhough its radial section has been broken off, thetuft of IGF 11778 (Fig. 3c) is more flaring bilaterallyrelative to the shaft than in BA#130 (Fig. 3a). Thefunctional significance of the ungual fossa and tuft isthat the surface area for the distal ungual pulp over-lies and attaches palmarly to the tuft, whereas theproximal ungual pulp overlies and attaches palmarlyto the area over the ungual fossa (Shrewsbury andJohnson, 1975; Shrewsbury et al., 2003). The dorsalside of the base in IGF 11778 shows a marked proxi-mal rim for the attachment of the extensor pollicislongus (Fig. 3e,f). The radial lateral basal tubercle ofIGF 11778 is broken off (Fig. 3c,d,f), and the proxi-mal portion of the base in BA#130 is absent (Fig.3a). Our impression is, however, that the base of theOreopithecus PDP specimens was wide and dorsopal-marly flat (see corrected IGF 11778 specimens inFig. 3g–i).

Shape ratios

Table 1 provides the summary statistics for the sevenmeasurements taken in our sample. The GM and theseven shape variables are represented in Figure 5 asboxplots. Oreopithecus, like Pierolapithecus, has anabsolutely larger PDP than Pan and Pongo, whereasOrrorin, like Gorilla and especially humans, displaylarger PDPs (Fig. 5a). The Proconsul specimen is con-siderably smaller, being in the upper size range of mon-keys (as KPS1 is a subadult specimen, a larger size isexpected for an adult of this taxon). In terms of relativeproximodistal length, Oreopithecus and Proconsul arein the range of humans and Gorilla, whereas Pierolapi-thecus is in the low range of Pongo and Pan, which dis-play long PDPs relative to the other dimensions. Thelatter condition is extreme for Alouatta, an obvious out-lier in this analysis. The catarrhine monkeys andOrrorin display relative shorter PDPs (Fig. 5b). Interms of the dorsopalmar height of the tuft (Fig. 5c), allthe fossils examined display very similar values, in thelow range of extant great apes and Alouatta and theupper range of Hylobates. Cercopithecines have slightlylower values; Nasalis is slightly higher. Modernhumans stand out by having relatively shorter dorso-palmar tuft heights. For values of relative tuft medio-lateral width (Fig. 5d), humans display the better-developed tufts, followed closely by Papio. Pan, Pongo,and Nasalis display lower values, like Proconsul,whereas Macaca, Gorilla, Oreopithecus, and Orrorinare intermediate. Alouatta displays the shortest values,with similarities to Pierolapithecus. Among extant taxa,there is a clear separation between PDPs with a longerdorsopalmar height at the midshaft (Alouatta, Nasalis,Pongo, and Pan) and taxa with shorter dorsopalmarmidshafts, which are relatively wider (Macaca, Papio,Gorilla, H. sapiens, and Hylobates). Oreopithecus, Pro-consul, and Orrorin are in an intermediate positionbetween both groups, whereas Pierolapithecus is in theupper range of Pan and Pongo (Fig. 5e). For the medio-lateral width of the midshaft (Fig. 5f), H. sapiens, Hylo-bates, and Macaca show high values, whereas Alouattaand especially Pongo and Pan show very low degrees ofmidshaft expansion. Papio, Nasalis, and Gorilla are ina more intermediate range. Oreopithecus is in betweenthe mid and low ranges, Orrorin and Pierolapithecusare in the middle to high ranges, and Proconsul is inthe upper range. The analysis of the mediolateral widthof the base (Fig. 5h) shows that Macaca has the rela-tively widest base, whereas Pan and especially Alouattahave the narrowest base. The remaining extant taxashow intermediate values between these extremes. Pro-consul, Pierolapithecus, and Orrorin are in the range ofAlouatta (and lower range of Pan); however, there aredifferences in Oreopithecus depending on the actualand corrected IGF 11778 specimens. The former isbetween Pan and Alouatta, but a much higher valueemerges from the corrected version, which overlapswith most of the taxa of the intermediate group. Theanalysis of the dorsopalmar height of the base (basedon the seven-variable GM and thus not including Piero-lapithecus; Fig. 5g) shows that Pongo has the tallestbase. Nasalis, Macaca, Alouatta, and especially Hylo-bates all have a shorter base. Papio, Gorilla, Pan, andH. sapiens have intermediate values between Pongoand the remaining taxa. All the Miocene fossil taxa dis-play similar values, which are the shortest among thetaxa analyzed.

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 587

American Journal of Physical Anthropology

Tuft expansion

The expansion index (Mittra et al., 2007) shows thatwhen the mediolateral expansion of the tuft is examinedin relation to the base (Fig. 6), Papio and especially H.sapiens exhibit more expanded tufts than the remainingextant taxa (P < 0.008). There are no statistical differen-ces between the remaining extant genera; however,Gorilla on one side and Alouatta and especially Pongoon the other side show a tendency to have slightly moreand less expanded tufts, respectively. Proconsul isbetween the midranges of Papio and modern humans,whereas Orrorin is on the upper human range andPierolapithecus on the low interquartile range of Panand midrange of Pongo. More evident differences existbetween the actual Oreopithecus specimen (in the upper

human range) and the corrected version (intermediatebetween humans-Papio and the remaining taxa).

When covariation of mediolateral tuft expansion andPDP size is inspected through ANCOVA (Fig. 7), homo-geneity of slopes cannot be discarded (F 5 1.644; P 50.143) for all extant taxa with the exception of Pan,which shows a significantly higher slope. Results of theallometric regression analyses are reported in Table 2,showing that isometry cannot be discarded for anyextant genus with the exception of Pan (positive allome-try). Regression of Alouatta was nonstatistically signifi-cant, probably due to its small sample size and wastherefore not reported. Post hoc Bonferroni comparisonson estimated marginal means of genera with similarslopes (i.e., excluding Pan and Alouatta; comparisonsevaluated at lnGM 5 1.66) show that modern humans,

Fig. 5. Boxplots depicting PDP size and shape ratios. Size was approximated by the geometric mean (GM) of six of the originalmeasurements (excluding dorsopalmar base, not available in Pierolapithecus). Shape variables were standardized by the same GMto the exception of the dorsopalmar base, which was adjusted by a GM based on the seven available measures. Box represents 25thand 75th percentiles, respectively, centerline is median, whiskers are nonoutlier range, dots are outliers, and stars representextreme outliers. KPS1-PH96 is Proconsul heseloni; IPS 21350.16 is Pierolapithecus catalaunicus; for Oreopithecus bambolii, theactual (IGF 11778a) and digitally corrected (IGF 11778c) specimens were included; and BAR 1901’01 is Orrorin tugenensis. Thevertical line in every boxplot is meant to facilitate the visual comparison of IGF 11778c to the remaining taxa. [Color figure can beviewed in the online issue, which is available at wileyonlinelibrary.com.]

588 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

Papio, and Macaca display wider tufts relative to overallPDP size than extant great apes (P < 0.001; Papio andGorilla, P 5 0.008). At the same PDP size, Papio alsohas significantly wider tufts than Hylobates and Nasalis(P < 0.001). Hylobates and Nasalis display wider tuftsthan Pongo (P < 0.005). Proconsul, Oreopithecus (bothiterations), and Orrorin are situated in an intermediateposition: Proconsul on the Nasalis–Hylobates regressionline; Oreopithecus on the line of Gorilla (corrected) orslightly above (actual), and both slightly above Pan andPongo; and Orrorin, slightly above the Gorilla regressionline (similarly to the actual IGF 11778 specimen),although fully within this range. Some gorilla specimensfall in the low human range at small sizes, not far fromthe position of Oreopithecus and Orrorin. Pierolapithecusexhibits a low-degree of tuft expansion, being the onlyfossil with significantly (P < 0.001) narrower tufts thansome of the extant taxa (H. sapiens, Hylobates, Papio,Nasalis, and Macaca). These results give a similar met-ric signal to that found in the Mosimann shape ratio oftuft width (Fig. 5d).

Principal components analyses

When all the shape ratios provided in Figure 5 aresummarized by means of a PCA (see Fig. 8a and Table3, Iteration 1), major extant taxonomic groups can beidentified with the first two PCs. The major axis ofshape variation (i.e., PC1, explaining 55.2% of total var-iance) is positively correlated with overall proximodistallength and negatively correlated with mediolateral tuftand midshaft width. The two species of Pan and Pongo,and especially Alouatta show high values along thisaxis, reflecting their overall mediolaterally narrow PDPswith a predominant proximodistal length dimension,resulting in an overall “conical” shape. On the otherextreme of PC1, modern humans, followed by Macacaand Papio are characterized by PDPs with a broaderappearance. Gorilla, Nasalis, Proconsul, and Oreopithe-cus show intermediate values on this axis, with Hylo-bates and Orrorin being intermediate between Miocenehominoids and cercopithecid terrestrial monkeys. PC2(19.1% of variance) is positively correlated with dorso-palmar height of the base and negatively with mediolat-eral shaft width. This axis clearly separates great apes,modern humans, and cercopithecoid monkeys by theirpositive values from Alouatta, Miocene hominoids,Orrorin, and Hylobates, all of which are restricted to thenegative side of the axis.

A second iteration of this same analysis excludes thedorsopalmar height of the base—the variable mosthighly correlated with PC2 in iteration 1—to includePierolapithecus (Fig. 8b and Table 3). PC1 (59.8% of

Fig. 6. Boxplot showing the tuft expansion index. Fossilsand boxplots are as in Figure 5. The vertical line facilitates thevisual comparison of IGF 11778c to the remaining taxa. [Colorfigure can be viewed in the online issue, which is available atwileyonlinelibrary.com.]

Fig. 7. Allometric relationship of mediolateral tuft widthand PDP size. Size was approached by the geometric mean ofsix measurements (as in Fig. 5a). Regression lines for everyextant taxa (except Alouatta) are indicated (dashed lines arePan and Hylobates).

TABLE 2. Results of regression analyses reported in Figure 7

N R SEE P Slope 95% CI Intercept 95% CI

Nasalis 9 0.945 0.127 0.000 0.967 0.668 1.267 20.116 20.482 0.251Macaca 5 0.982 0.139 0.003 1.260 0.819 1.701 20.357 20.876 0.163Papio 29 0.906 0.104 0.000 1.151 0.939 1.363 20.137 20.438 0.165Hylobates 11 0.796 0.280 0.003 1.107 0.473 1.741 20.297 21.081 0.487Pongo 18 0.883 0.194 0.000 1.464 1.052 1.876 20.971 21.652 20.289Gorilla 17 0.659 0.233 0.004 0.790 0.294 1.286 0.354 20.669 1.377Pan 31 0.914 0.141 0.000 1.710 1.421 2.000 21.433 21.933 20.933H. sapiens 25 0.888 0.130 0.000 1.205 0.936 1.473 20.324 20.892 0.244

All regressions show slopes significantly different from zero (P � 0.004).Abbreviations: SEE, standard error of estimate; CI, confident interval.

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 589

American Journal of Physical Anthropology

TABLE 3. Results of the principal components analyses reported in Figure 8

Iteration 1 Iteration 2

PC1 PC2 PC1 PC2

% variance 55.20 19.11 59.80 16.87

Shape variables Factor loadings

Proximodistal length 0.45 20.27 0.46 0.32Dorsopalmar tuft 0.34 20.26 0.35 20.29Mediolateral tuft 20.45 0.06 20.49 20.42Dorsopalmar midshaft 0.34 20.10 0.39 0.00Mediolateral midshaft 20.55 20.48 20.46 0.73Dorsopalmar base 0.11 0.70 – –Mediolateral base 20.22 0.34 20.25 20.34

Variables are shape variables, as each original measurement was divided by the geometric mean (GM) of seven (Iteration 1) or six(Iteration 2) variables. Loadings > 0.40 or < 20.40 are marked in bold. Remaining axes explain less than 12% and 10% of the var-iance, respectively, and do not provide meaningful discrimination.

Fig. 8. Principal components analyses (PCA) based on extant species means and individual fossils. Iteration 1 (a) shows PC1and PC2 including the whole set of seven shape variables depicted in Figure 5. Iteration 2 (b) shows PC1 and PC2, excluding thedorsopalmar height of the base to include Pierolapithecus. Hand-drawn ellipses indicate extant bigger taxonomic groups. [Color fig-ure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

590 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

total variance) is driven by the same shape variables asin the first iteration, but now PC2 is driven positively bymediolateral midshaft and negatively with mediolateraltuft. This more restrictive shape analysis yields a clut-tered morphospace configuration (i.e., more overlapbetween major taxonomic groups) than in the first itera-tion. Pierolapithecus occupies an intermediate positionbetween orangutans and chimpanzees in PC1 and isextreme in PC2 (positive values), resulting from a combi-nation of an overall long PDP with a very narrow tuft.When the dorsopalmar height of the base is excluded,PC2 separates Pierolapithecus, Proconsul, Hylobates,Alouatta and H. sapiens from the remaining taxa. Oreo-pithecus in this iteration is most similar to gorillas andNasalis.

DISCUSSION

PDP proportions and “pad-to-pad” features inOreopithecus

In this study, we reevaluated the PDP morphology ofOreopithecus (based in IGF 11778 and BA#130) in com-parison with other selected anthropoid primates andwith currently available Miocene hominoid fossils. Thepresence of features that have been related to pad-to-pad precision grasping in modern humans (Shrewsburyet al., 2003) is evaluated (Figs. 3 and 4), and morpho-metric affinities of IGF 11778 relative to our compara-tive sample are assessed by means of bivariate (Figs. 5–7) and multivariate (Fig. 8) analyses. A summary of themain metric and nonmetric features of the OreopithecusPDP and our comparative sample is available in Table 4.Our PCA on the covariance matrix of specific means(Fig. 8a) shows that some major taxonomic groups canbe separated by means of the major trends in PDP shapevariation: platyrrhines and catarrhines; cercopithecoids,great apes, and hylobatids. Modern humans are notarranged by phylogenetic proximity to African apes;instead, their overall flat and wide PDPs are more simi-lar to that of terrestrial cercopithecoid monkeys. All Mio-cene taxa considered occupy a similar position in themorphospace, similar to Hylobates, which suggests thatPDP proportions characterized by moderate tuft andmidshaft width and by a dorsopalmarly short base areprobably plesiomorphic for Hominoidea. On the otherhand, the species of Pan and Pongo are more similar toeach other in terms of their overall cylindrical shape[i.e., less mediolaterally expanded at the midshaft andtuft (Fig. 5d,f); and their more dorsopalmarly expansionat the midshaft than other hominoids (Fig. 5e)].Although Oreopithecus shows a PDP with primitive pro-portions (Fig. 8a), it has a mediolaterally well-developedtuft for an ape, similar to the early hominin Orrorin(Figs. 5d and 7), although less so when the correctedversion of IGF 11778 is analyzed by means of the expan-sion index (Fig. 6). The tuft seems to be variable in thistaxon, at least from a qualitative inspection to BA#130(Fig. 3a). A mediolaterally expanded tuft is functionallyrelevant, because in humans, it is also correlated withan expanded digital pulp in pollical (Susman, 1988) andin nonpollical (Mittra et al., 2007) distal phalanges.

A suite of features in the PDP of humans was exten-sively described in relation to a “pad-to-pad” interactionof the thumb and one or more of the remaining digits(Shrewsbury et al., 2003). This suite of characters wasvisually reconstructed in relation to the soft tissue byAlm�ecija et al. (2010, their Fig. 1). Essentially, this mor-

phology is reflected by a proximal palmar fossa (PVF ofShrewsbury et al., 2003) associated with a palmarly pro-truding ridge at the distal border of the PVF for attach-ment of the FPL tendon. The digital pulp distal to theflexor tendon attachment functions to accommodate theshape of the object being manipulated or held. The func-tions of the digital pulp are reflected in the presence ofan ungual fossa, associated with an overlying mobileproximal pulp. The ungual fossa is defined proximally bythe FPL tendon attachment and distally by a relativelywide and palmarly elevated tuft. The tuft itself is associ-ated with a more stable distal ungual pulp (Shrewsburyand Johnson, 1975; Shrewsbury et al., 2003). Finally,ungual spines project proximally from the radial andulnar borders of the tuft. Lateral intraosseous ligamentsare attached to the spines, which sustain the lateral nailbed and support the lateral borders of the proximalungual pulp. These individual morphological featurescan be found in selected specimens of different extantprimates (Susman, 1998); however, among extant taxa,the entire complement of features described can only beconsistently found in modern humans (see Fig. 4;Shrewsbury et al., 2003).

In the PDPs of Oreopithecus, the morphology and spa-tial location of the tubercles just distal to a PVF, projec-ting palmarly, suggest the presence of a strongattachment for the long tendon of a pollical flexor mus-cle. The locations and size for these tendon attachments(i.e., the tubercles) suggest that, as in humans, its func-tion at the interphalangeal joint is for flexion with con-junct rotation, the latter motion reducing the forces offlexion across the joint. Unlike in Plio-Pleistocene andmodern hominin PDPs, there is no noticeable sesamoidfacet in Oreopithecus at the palmar midline base of thePDP for a sesamoid bone or cartilage within the palmarplate to ride up on the facet during flexion and toincrease the torque of the flexor tendon. Furthermore, asin modern humans and fossil hominins (Susman, 1998;Shrewsbury et al., 2003; Alm�ecija et al., 2010), bothOreopithecus PDP specimens display both a PVF and anungual fossa delineated proximally and distally, respec-tively, by the protruding flexor tendon insertion and thetuft (Figs. 3 and 4). The flexor attachment appears dis-tinctive in Oreopithecus by being slightly separatedinstead of a continuous gabled ridge as in hominins.Nevertheless, there is an isthmus ridge connecting thetwo tubercles, which could account tendon attachmentcontinuity. In brief, many of the features present in thehominins PDP that are related to pad-to-pad precisiongrasping are also present in the Oreopithecus specimens,except for the presence of ungual spines and sesamoidfacets. It is noteworthy that ungual spines seem to beonly moderately developed or absent in some later Mio-cene, Pliocene, and Pleistocene hominins (Gommery andSenut, 2006; Lovejoy et al., 2009; Alm�ecija et al., 2010;Ward et al., 2012), whereas a sesamoid facet is not pres-ent in the six-million-year-old BAR 1901’01 (Orrorintugenensis), even though all the remaining features arealready present (Alm�ecija et al., 2010). In that previousanalysis, focusing on available hominins, the dorsopal-mar height of the tuft was not available in our compara-tive sample and thus not measured. The combination ofthe prior and the current analyses offers an interestingpicture: by excluding that single diameter (dorsopalmarheight of tuft), Orrorin falls within the modern humanPDP morphometric variation (Fig. 3 in Alm�ecija et al.,2010), whereas its proportions look less human and

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 591

American Journal of Physical Anthropology

more similar to hylobatids, Proconsul, and Oreopithecuswhen that variable is included in this study. A dorsopal-marly high tuft is most probably plesiomorphic for homi-noids, as it was already pointed out in that previouswork (Alm�ecija et al., 2010). Similarly, and in contrast tomodern humans, high dorsopalmar tuft dimensions havealso been reported for Australopithecus afarensis (Wardet al., 2012) and Australopithecus sediba (Kivell et al.,2011) reinforcing the plesiomorphic status of this charac-ter in these hominins as well. Overall, the presence ofpad-to-pad traits in Oreopithecus and Orrorin, with onlymoderate mediolateral development suggests that thesetraits can evolve prior to modern human PDPproportions.

Relationship between PDP morphology andintrinsic hand length proportions

The implicit assumption of this and previous studiesthat analyze the presence of pad-to-pad precision grasp-ing features in the PDP is that the intrinsic hand pro-portions allowing for such precision grasp are present(Shrewsbury et al., 2003; Alm�ecija et al., 2010), that is,the thumb is long enough so that the proximal pads ofthe thumb and one or more of the remaining digits canoppose each other. However, this argument does not nec-essarily imply that a long thumb relative to digits canbe related only to enhanced precision grasping. Forexample, terrestrial digitigrade monkeys exhibit thumb-to-digit length proportions approaching those of humans(Schultz, 1930; Napier, 1960, 1993), coupled with widePDP tufts (especially Papio; Figs. 4–8). However, themechanism responsible for these hand proportions andthumb morphology in these digitigrade monkeys prob-ably has nothing to do with enhanced manipulation.Conversely, the specific locomotor adaptations are linkedto a high degree of terrestriality, such as Digits II–Vlength reduction (Etter, 1973) and use of tip of thethumb in weight support (e.g., Tuttle, 1967; Whitehead,1993). Explicit analyses of thumb morphology andintrinsic hand length proportions are necessary to testthe former assumption. Therefore, the following discus-sion is intended only to summarize the results in PDPanatomy and proportions in our primate sample takinginto account the available data on intrinsic hand propor-tions and hand use in extant primates to evaluate howour implicit functional assumption stands.

Cercopithecoid monkeys show PDP proportions similarto those of humans (Fig. 8). Instead of a human-likePVF (limited to the proximal palmar portion of the pha-lanx by a marked FPL attachment), cercopithecoids(with the exception of Theropithecus) display a moreextensive fossa, occupying most of the palmar basal anddiaphyseal surface of the PDP while reaching distally tothe proximal edge of the tuft (Fig. 4). A flexor tendonfrom the radial component of the FDP (e.g., Whitehead,1993; Susman, 1998; Diogo et al., 2012) traverses dis-tally to attach to the base or surface of the tuft (Fig. 9 inShrewsbury et al., 2003). Consequently, the complex ofthe PVF, distal protruding flexor muscular attachment,and ungual fossa appears limited to modern and fossilhominins (Susman, 1998; Shrewsbury et al., 2003;Alm�ecija et al., 2010) and Oreopithecus (Fig. 4). Gorilla,Alouatta, and Proconsul exhibit a portion of shaftbetween the flexor insertion and the tuft; however, nei-ther the tendon attachment nor the tuft protrude pal-marly. Thus, a proper ungual fossa is lacking (Fig. 4).

Theropithecus gelada presents a complex similar to thatof hominins: presence of PVF with a conspicuously pro-truding gabled insertion for a long flexor; however, noclear ungual fossa is present (Fig. 4). Etter (1973)described the particular case of the gelada baboons,which displays an especially elongated pollical metacar-pal (but not phalanges) and shortened second ray, as theresult of an extreme reduction of the intermediate pha-lanx, thereby conferring the geladas with a human-likepad-to-pad “precision handling” capability as evaluatedin terms of thumb to index length proportions (Etter,1973, p 343). The special adaptation of the hands ofgeladas is also evident in a special differentiation of theFDP, as well as other thumb muscles (Maier, 1971), thusbeing analogous to a proper FPL. This is explained asspecific feeding adaptations in monkeys that spend 70%of their daily activity collecting grass blades, seeds, andrhizomes (Jolly, 1970). Therefore, other than humans,Theropithecus is the only modern species with reportedpad-to-pad precision grip behaviors, which are furtheraccompanied by intrinsic hand length proportions allow-ing for such grip, as well as a PDP with a flexor attach-ment configuration similar to that of hominins andOreopithecus (Fig. 4). We hypothesized that subtle PDPdifferences in geladas could be related to the use of thethumb for weight bearing and/or the evolution of specifi-cally manipulatory-related features in an already speci-alized terrestrial digitigrade monkey. This evidencehighlights the complexity of the PDP anatomy and howthe evolutionary history of a taxon should be taken intoaccount when analyzing the evolutionary process, espe-cially considering the raw materials originally availablefor natural selection to operate (Gould and Lewontin,1979). Future studies including a more complete sampleof Theropithecus specimens are necessary to properlycharacterize and interpret the PDP of the geladababoons.

Hand manipulation and locomotion are two main (andsometimes opposite) selective pressures shaping thehands of primates (Napier, 1960, 1993). Extant greatapes provide a good example of this: Pan and Pongoshow the shortest thumbs in relation to their elongatedhand, presumably for an efficient below-branch “hookgrasp” during below-branch suspension (Schultz, 1930;Straus, 1942; Tuttle, 1967; Preuschoft, 1973; Preuschoftet al., 1993). Both taxa also share a similar PDP mor-phology with poorly developed tendon insertions on thepalmar aspect and with a narrow tuft (Figs. 4–8 andTable 4). However, the presence or absence of any inser-tion on the palmar aspect of the PDP seems to be widelyvariable in great apes, Pongo being the extreme case,where roughly 95% of the specimens do not exhibit afunctional tendon (Straus, 1942; Diogo et al., 2012). Weargue that similar PDP morphology and intrinsic handproportions in Pan and Pongo could be explained bysuspensory-related homoplasy in great apes (e.g.,Alm�ecija et al., 2013). This argument is reinforced bythe more moderate thumb-to-digit length proportions ingorillas (more terrestrial than Pan and Pongo), andespecially the highly terrestrial mountain gorillas(Schultz, 1930; Tuttle, 1967; Sarmiento, 1994) as well astheir more moderate PDP proportions (Figs. 4 and 8).Even with the short thumb relative to digits and thelack of a proper FPL, extant great apes exhibit well-developed thenar muscles (but not to the degree ofhumans) and use their hands for a variety of power andprecision grips (Napier, 1960; Tuttle, 1967, 1969, 1970;

592 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

TA

BL

E4.

Ma

inm

orp

hol

ogic

al

fea

ture

sof

the

pol

lica

ld

ista

lp

ha

lan

ges

an

aly

zed

inth

isw

ork

Base

Mid

shaft

Tu

ftP

alm

ar

Fle

xor

inse

rtio

nU

ngu

al

Un

gu

al

Dor

sop

alm

ar

Med

iola

tera

lD

orso

palm

ar

Med

iola

tera

lD

orso

palm

ar

Med

iola

tera

lF

ossa

Exp

ress

ion

Pla

ceM

usc

leF

ossa

Sp

ines

Alo

ua

tta

Sh

ort

Ver

yn

arr

owT

all

Narr

owT

all

Ver

yn

arr

owL

arg

e,sh

all

owF

ain

tD

ista

lsh

aft

FD

PA

bse

nt

Abse

nt

Na

sali

sS

hor

tIn

term

edia

teT

all

Inte

rmed

iate

Tall

Narr

owL

arg

e,d

eep

Fain

tT

uft

FD

PA

bse

nt

Abse

nt

Ma

caca

Sh

ort

Ver

yw

ide

Sh

ort

Wid

eS

hor

tIn

term

edia

teL

arg

e,d

eep

Fain

tT

uft

FD

PA

bse

nt

Vari

ably

pre

sen

tP

ap

ioT

all

Wid

eS

hor

tIn

term

edia

te/

wid

eS

hor

tW

ide

Larg

e,d

eep

Fain

tT

uft

FD

PA

bse

nt

Vari

ably

pre

sen

tH

ylob

ate

sS

hor

tIn

term

edia

teS

hor

tW

ide

Sh

ort

Narr

owL

arg

e,d

eep

Vari

able

Dis

tals

haft

FP

LA

bse

nt

Abse

nt

Pon

go

Ver

yta

llW

ide

Tall

Narr

owT

all

Narr

owF

ain

tif

pre

sen

tF

ain

tS

haft

FD

PA

bse

nt

Abse

nt

Gor

illa

Tall

Wid

eS

hor

tIn

term

edia

teT

all

Inte

rmed

iate

Larg

e,sh

all

owF

ain

tS

haft

FD

PA

bse

nt

Abse

nt

Pa

nT

all

Narr

owT

all

Narr

owT

all

Narr

owF

ain

tif

pre

sen

tF

ain

tS

haft

FD

PA

bse

nt

Abse

nt

H.

sap

ien

sT

all

Wid

eS

hor

tW

ide

Ver

ysh

ort

Wid

eP

VF

Mark

edS

haft

FP

LL

arg

e,d

eep

Pre

sen

t

KP

S1-

PH

96

Pro

con

sul

Sh

ort

Ver

yn

arr

owIn

term

edia

teW

ide

Tall

Inte

rmed

iate

PV

FF

ain

tS

haft

?A

bse

nt

Abse

nt

IPS

21350.1

6P

iero

lap

ith

ecu

s?

Narr

owT

all

Wid

eT

all

Ver

yn

arr

owP

VF

??

?A

bse

nt

Abse

nt

IGF

11778

Ore

opit

hec

us

Sh

ort

Inte

rmed

iate

Inte

rmed

iate

Narr

ow/

inte

rmed

iate

Tall

Inte

rmed

iate

PV

FM

ark

edS

haft

?L

arg

e,d

eep

Abse

nt

BA

#130

Ore

opit

hec

us

??

Inte

rmed

iate

?In

term

edia

te?

Tall

?N

arr

ow?

PV

FM

ark

edS

haft

?S

mall

,d

eep

Abse

nt

BA

R1901’0

1O

rror

inS

hor

tN

arr

owIn

term

edia

teW

ide

Tall

Inte

rmed

iate

PV

FM

ark

edS

haft

?S

mall

,d

eep

Mod

erate

Abbre

via

tion

s:P

VF

,p

roxim

al

vol

ar

(5p

alm

ar)

foss

a;

FD

P,

flex

ord

igit

oriu

mp

rofu

nd

us;

FP

L,

flex

orp

olli

cis

lon

gu

s.

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 593

American Journal of Physical Anthropology

Christel, 1993; Napier, 1993; Pouydebat et al., 2008).However, a human-like pad-to-pad contact is precludedby the disproportionate length of their Digits II–V rela-tive to the thumb (see Discussion section in Alba et al.,2003; Alm�ecija et al., 2009a; Marzke et al., 2009;Alm�ecija et al., 2010), as well as the shortness of thecommon flexor tendons (Christel, 1993).

Hylobatids provide an alternative anatomical solution,reconciling highly specialized suspensory behaviors andwell-developed thumbs. Even though they are the mostsuspensory of the modern hominoids, hylobatids stillexhibit moderate thumb-to-hand length proportions(Schultz, 1930), moderate PDP proportions (Fig. 8), andan insertion marking on the palmar side (Fig. 4) for aproper FPL (Straus, 1942; Diogo et al., 2012). Further-more, hylobatids exhibit a deep cleft that separates thethumb from the palm at the metacarpal level (Fig. 10 inStraus, 1942) to enable the hand for secure grips—assisted by the thumb—during arboreal locomotion aswell as to allow the thumb to be “bent across the proxi-mal palm, where it is of no hindrance in brachiation”(Straus, 1942, p 239). Hylobatids suggest that a properFPL can be present in some Miocene apes due to evolu-tionary history but unrelated to enhance manipulativebehaviors. If this suggestion holds true, then the posses-sion of a FPL would not be a hominin synapomorphy,but rather the plesiomorphic status for Hominoidea.Extant great apes might have lost a proper FPL in rela-tion to thumb shortening relative to hand length(Straus, 1942; Lovejoy et al., 2009; Alm�ecija et al., 2012).Until more specific analyses relating to PDP morphologyand intrinsic hand proportions are available, the obser-vations discussed above support the hypothesis that thepresence of pad-to-pad traits on the PDP palmar sidecan only evolve in hands with long thumbs relative todigit(s). We argue that this was the case of Oreopithecus.

Oreopithecus as part of the bigger picture

The complete, although juvenile, PDP specimen ofProconsul (KPS1-PH96) has been described as possess-ing a “deep pit” on its palmar side, indicating the inser-tion for a long flexor tendon (Begun et al., 1994). Ashallow PVF is present in this specimen, followed dis-tally by a rugose surface, suggesting an insertion for thelong pollical flexor tendon (Fig. 4). However, this inser-tion does not protrude palmarly as in hominins or inOreopithecus (Table 4), although its subadult statusshould caution our speculations. The KPS1 specimenshows similar overall PDP proportions with Oreopithe-cus (Fig. 8a), although with less-developed mediolateraltuft (Figs. 5d and 7; although uncertain for expansionindex, Fig. 6), which has been related to distal pulpdevelopment (Mittra et al., 2007). As previously observed(Alm�ecija et al., 2009b), the Pierolapithecus PDP speci-men appears to have a faint proximal depression on itspalmar side (slight abrasion of the palmar side hindersany detailed anatomical description; Fig. 4) and aweakly developed tuft (Figs. 5d–8). The case is similarfor the more partial IPS 4333 specimen from Castell deBarber�a where the base is absent (Alm�ecija et al., 2012).This might suggest similar thumb morphology in Span-ish Miocene apes (i.e., long PDP with reduced tuft).There is a general agreement that most Miocene apeswould have better developed thumbs than their extantrelatives, which were used to assist in power graspingduring above-branch quadrupedalism and, possibly, in

climbing (Pilbeam et al., 1980; Begun et al., 1994; Madaret al., 2002; Nakatsukasa et al., 2003; Ward, 2007;Alm�ecija et al., 2009b, 2012). Thus, a moderately longthumb could actually be the plesiomorphic state forgreat apes, as suggested by these previous analyses onproximal pollical phalanx length relative to body mass(Alm�ecija et al., 2012). Furthermore, with the exceptionof the European Late Miocene Hispanopithecus/Rudapi-thecus suspensory group (Begun, 1993; Moy�a-Sol�a andK€ohler, 1996; Alm�ecija et al., 2007), with disputed phy-letic affinities (e.g., Alba, 2012; Begun et al., 2012), stemhominoids and great apes have been discussed as exhib-iting only moderate hand lengths, certainly shorter thanmodern suspensory forms (e.g., Napier and Davis, 1959;Moy�a-Sol�a et al., 2005a; Alm�ecija et al., 2009b). Accord-ingly, moderate thumb-to-hand length proportions allow-ing (although not necessarily selected) for a better pad-to-pad contact than that observed on extant apes couldactually be plesiomorphic for hominoids and originallyrelated to above-branch palmigrady assisted by thethumb (Alm�ecija et al., 2007, 2009b, 2012). Hence,human hand length proportions (i.e., long thumb rela-tive to hand) could have evolved without the drasticchanges that starting from a “chimp-like” ancestor wouldimply (Ashley-Montagu, 1931; Harrison, 1991; Lovejoyet al., 2009).

The overall picture of our morphometric analyses showsthat the PDP of Oreopithecus is not modern-human-likebut rather primitive. However, it shows on its palmar sidea combination of features present in fossil hominins (tothe exception of OH 7; Fig. 4 and Table 4): a PVF, apalmarly-protruding flexor insertion marking, an ungualfossa, and a palmarly protruding and slightly wide tuft(Susman, 1988; Gommery and Senut, 2006; Alm�ecijaet al., 2010; Kivell et al., 2011; Ward et al., 2012). Thesetraits suggest a better-developed flexor apparatus for thePDP of Oreopithecus than in extinct and in extant greatapes. In Oreopithecus, these qualitative features are fur-ther accompanied with better-developed tufts than in pre-vious Miocene apes, especially in comparison withPierolapithecus. Some of these fossil PDPs are attributedto hominin species with inferred human-like intrinsichand length proportions, predating the establishment of asystematic stone-tool culture (Alba et al., 2003; Green andGordon, 2008). Recently, and for the first time in the Aus-tralopithecus fossil record, a virtually complete associatedhand was found for Australopithecus sediba (ca. 2 Ma),indicating long thumb relative to third digit (slightlyabove humans) but unassociated with stone tools (Kivellet al., 2011). This evidence indicates that enhanced manip-ulative skills allowed by more efficient pad-to-pad contactcould have evolved in early hominins from Miocene-ape-like (moderate) hand length proportions once selectivepressures posed by forelimb locomotor behaviors becamerelaxed with the advent of terrestrial bipedalism (Albaet al., 2003; Alm�ecija et al., 2010). Thus, among the vastarray of traits characterizing the human hand (Napier,1956, 1960, 1993), intrinsic length proportions would nothave necessarily evolved originally in relation to stonetool-making specifically. They probably were exapted forthe latter in hominins with advanced cognitive capabilitiesand, as a consequence, “purposive actions” (Napier, 1956,1962; Alba et al., 2003).

Oreopithecus has been alternatively reconstructed asbeing a slow-moving (Schultz, 1960), an agile suspen-sory/climber (e.g., Szalay and Delson, 1979; Jungers,1984; Harrison, 1986; Jungers, 1987; Sarmiento, 1987;

594 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

Harrison, 1991), or even a bipedal ape (Straus, 1963;K€ohler and Moy�a-Sol�a, 1997; Rook et al., 1999).Although the proportions of its postcranial long bonesindicate the pattern of an extant ape-like forelimb(Jungers, 1987), neither its hand proportions are of asuspensory type of ape nor is their morphology compati-ble with a pronograde monkey-like creature (Moy�a-Sol�aet al., 1999, 2005b), although different interpretationshave been presented (Susman, 2004, 2005). The phalan-geal curvature in Oreopithecus (36�, using the includedangle technique) estimated by Susman (2004) fallswithin the low range of African apes, but interestingly,also within range of early hominins (Susman, 1988;Stern et al., 1995; Richmond and Jungers, 2008) andwell below the range of any other available Miocene ape(Alba et al., 2010). We believe that this low degree ofmanual phalangeal curvature in Oreopithecus is a com-pelling argument for low degree of suspensorylocomotion.

The origins of Oreopithecus are still obscure (see intro-ductory paragraph of this work and references therein);however, previous studies have established that Oreopi-thecus evolved and lived in the insular paleoecosystemof Tuscany and Sardinia (e.g., Moy�a-Sol�a and K€ohler,2003; Rook et al., 2006; Abbazzi et al., 2008). A com-monly observed thesis is that animals develop very par-ticular adaptations under insular conditions, withseveral different physiological and morphological adapt-ive processes being described for mammals of the Medi-terranean islands (e.g., Bover et al., 2008; Palomboet al., 2008; van der Made, 2008; K€ohler and Moy�a-Sol�a,2009; Quintana et al., 2011). Most of the insular adapta-tions involve enhanced energy processing that includeimproved harvesting and reduction of energy expensivelocomotor behaviors (Moy�a-Sol�a and K€ohler, 2003;K€ohler et al., 2007). In this resource-limited insular eco-system, enhanced manipulative capabilities in Oreopi-thecus relative to modern apes would have improved itsharvesting capabilities and, thus, its fitness (K€ohler andMoy�a-Sol�a, 1997; Moy�a-Sol�a et al., 1999; Rook et al.,1999; Moy�a-Sol�a and K€ohler, 2003; Moy�a-Sol�a et al.,2005b). This evolutionary scenario would explain whyOreopithecus displays a bizarre combination of featuresincluding modern ape-like limb long-bone proportions(Jungers, 1987), which we suggest are part of its recentevolutionary history, in combination with a short hand(Moy�a-Sol�a et al., 1999, 2005b). Moderate hand lengthin Oreopithecus could, however, be interpreted largelyas plesiomorphic (evolved from more moderate handlength proportions inferred for stem hominoids andstem great apes) or secondarily derived in this taxonfrom a long-handed suspensory ancestor (which wouldimply a larger amount of change). Only the finding ofcomplete associated thumb and median digital bones inOreopithecus will allow us to actually test its “real”intrinsic hand proportions and thus the functional sig-nificance of its PDP anatomy. Suspensory adaptationshave evolved several times independently between someplatyrrhines and hominoids (Erikson, 1963) and alsowithin hominoids (Larson, 1998; Moy�a-Sol�a et al., 2004;Alm�ecija et al., 2007; Ward, 2007; Alba, 2012; Albaet al., 2012), probably by different means (Straus, 1942).We further propose that pad-to-pad precision graspingevolved independently at least three times in catar-rhines: during the Late Miocene of Europe (Oreopithe-cus), of Africa (early hominins) and again inTheropithecus during the Pliocene (Jablonski, 1986).

CONCLUSIONS

Our morphometric analyses indicate that Oreopithecusdisplays a pollical distal phalanx (PDP) of intermediateproportions between the overall wide and flat PDP ofhumans and some cercopithecoid monkeys and the coni-cal PDPs of Pierolapithecus, chimpanzees, orangutans,and especially Alouatta. Thus, Oreopithecus shows aPDP with overall similar morphometric affinities toHylobates, Gorilla, and Nasalis, as well as to Proconsuland the Late Miocene Orrorin, and are interpreted asplesiomorphic. In addition, the Oreopithecus PDP pal-mar surface exhibits protruding tubercles for insertionof a long pollical flexor tendon associated with proximaland distal (ungual) fossae, respectively. This arrange-ment has only been found in humans and fossil relativesand has been associated with the presence of a properflexor pollicis longus (FPL) as well as differentiated pulpregions. These traits have been previously linked withenhanced pad-to-pad precision grasping in humans andare compatible with previous studies reporting human-like thumb-to-fingers length proportions in Oreopithecus.Moderate length relationships, however, have beeninferred in the past for other more “generalized” Mioceneapes. Our results support the interpretation that theintrinsic hand proportions of Oreopithecus are more sim-ilar to those of humans and other primates with a mod-erate thumb-to-hand length ratio (in opposition to thehomoplastically derived proportions displayed by suspen-sory extant hominoids). We conclude that the total mor-phological pattern of the Oreopithecus hand and thumbis compatible with enhanced manipulative skills (unre-lated to stone tool-making) in this species, relative tomodern hominoids. Those adaptations are compatiblewith the insular ecosystem contextual background previ-ously reported for this taxon, improving its harvestingfeeding capabilities in a resource-limited environment.Only future finding of more complete and associatedhand bones of Oreopithecus would allow testing theintrinsic hand proportions of this puzzling fossil taxon.

ACKNOWLEDGMENTS

The authors are grateful to Elisabetta Cioppi (Museodi Storia Naturale dell’Universit�a di Firenze), BurkartEngesser and Lo€ıc Costeur (Basel NaturhistorischesMuseum), Emma Mbua (National Museums of Kenya),Eileen Westwig (American Museum of Natural History),and William Jungers (Stony Brook University) for allow-ing to access the specimens under their care. Theauthors thank Esteban Sarmiento for providing some ofthe measurements on great apes. Biren Patel facilitatedthe 3D models of the Nasalis, Theropithecus, and Hylo-bates PDPs displayed in Figure 4. Data collection fromthe Museum of Comparative Zoology specimens (Macaca,Nasalis, and Hylobates) was facilitated through a loan tothe Stony Brook University by Biren Patel and CaleyOrr and their funding from The Leakey and theWenner-Gren Foundations, respectively. This work wasenriched by the edits of Ashley Hammond and WilliamJungers and with the constructive comments of the asso-ciate editor and two anonymous reviewers. This isNYCEP morphometrics contribution number 76.

LITERATURE CITED

Abbazzi L, Delfino M, Gallai G, Trebini L, Rook L. 2008. Newdata on the vertebrate assemblage of Fiume Santo (north-

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 595

American Journal of Physical Anthropology

western Sardinia, Italy), and overview on the Late MioceneTusco-sardinian paleobioprovince. Palaeontology 51:425–451.

Alba DM. 2012. Fossil apes from the Valles-Penedes Basin. EvolAnthropol 21:254–269.

Alba DM, Alm�ecija S, Casanovas-Vilar I, M�endez JM, Moy�a-Sol�a S. 2012. A partial skeleton of the fossil great ape Hispa-nopithecus laietanus from Can Feu and the mosaic evolutionof crown-hominoid positional behaviors. PLoS ONE 7:e39617.

Alba DM, Alm�ecija S, Moy�a-Sol�a S. 2010. Locomotor inferencesin Pierolapithecus and Hispanopithecus: reply to Deane andBegun (2008). J Hum Evol 59:143–149.

Alba DM, Moy�a-Sol�a S, K€ohler M. 2003. Morphological affinitiesof the Australopithecus afarensis hand on the basis of manualproportions and relative thumb length. J Hum Evol 44:225–254.

Alm�ecija S, Alba DM, Moy�a-Sol�a S. 2009a. OH 7, the curiouscase of the original handy man? Paleolusitana 1:85–92.

Alm�ecija S, Alba DM, Moy�a-Sol�a S. 2009b. Pierolapithecus andthe functional morphology of Miocene ape hand phalanges:paleobiological and evolutionary implications. J Hum Evol 57:284–297.

Alm�ecija S, Alba DM, Moy�a-Sol�a S. 2012. The thumb of Mioceneapes: new insights from Castell de Barber�a (Catalonia,Spain). Am J Phys Anthropol 148:436–450.

Alm�ecija S, Alba DM, Moy�a-Sol�a S, K€ohler M. 2007. Orang-likemanual adaptations in the fossil hominoid Hispanopithecuslaietanus: first steps towards great ape suspensory behav-iours. Proc R Soc B 274:2375–2384.

Alm�ecija S, Moy�a-Sol�a S, Alba DM. 2010. Early origin forhuman-like precision grasping: a comparative study of pollicaldistal phalanges in fossil hominins. PLoS ONE 5:e11727.

Alm�ecija S, Tallman M, Alba DM, Pina M, Moy�a-Sol�a S, andJungers WL. 2013. The femur of Orrorin tugenensis exhibitsmorphometric affinities with both Miocene apes and laterhominins. Nat Commun 4:2888.

Ashley-Montagu FM. 1931. On the primate thumb. Am J PhysAnthropol 25:291–314.

Begun DR. 1993. New catarrhine phalanges from Rudab�anya(northeastern Hungary) and the problem of parallelism andconvergence in hominoid postcranial morphology. J Hum Evol24:373–402.

Begun DR, Nargolwalla MC, Kordos L. 2012. European Miocenehominids and the origin of the African ape and human clade.Evol Anthropol 21:10–23.

Begun DR, Teaford MF, Walker A. 1994. Comparative and func-tional anatomy of Proconsul phalanges from the KaswangaPrimate Site, Rusinga Island, Kenya. J Hum Evol 26:89–165.

Berzi A. 1973. The Oreopithecus bambolii. J Hum Evol 2:25.Bover P, Quintana J, Alcover JA. 2008. Three islands, three

worlds: paleogeography and evolution of the vertebrate faunafrom the Balearic Islands. Quat Int 182:135–144.

Casanovas-Vilar I, Alba DM, Garc�es M, Robles JM, Moy�a-Sol�aS. 2011. Updated chronology for the Miocene hominoid radia-tion in Western Eurasia. Proc Natl Acad Sci USA 108:5554–5559.

Christel M. 1993. Grasping techniques and hand preferences inHominoidea. In: Preuschoft H, Chivers DJ, editors. Hands ofprimates. Vienna: Springer. p 91–108.

Delson E. 1986. An anthropoid enigma: historical introductionto the study of Oreopithecus bambolii. J Hum Evol 15:523–531.

Diogo R, Richmond BG, Wood B. 2012. Evolution and homolo-gies of primate and modern human hand and forearmmuscles, with notes on thumb movements and tool use. JHum Evol 63:64–78.

Erikson GE. 1963. Brachiation in New World monkeys and inanthropoid apes. Symp Zool Soc Lond 10:135–163.

Etter HF. 1973. Terrestrial adaptations in the hands of Cercopi-thecinae. Folia Primatol 20:331–350.

Gervais P. 1872. Sur un singe fossile, d’espece non encored�ecrite, qui a �et�e d�ecouvert au Monte Bamboli. C R Acad SciParis 74:1217–1223.

Gommery D, Senut B. 2006. La phalange distale du pouced’Orrorin tugenensis (Miocene sup�erieur du Kenya). Geobios39:372–284.

Gould SJ, Lewontin RC. 1979. The spandrels of San Marco andthe panglossian paradigm. Proc R Soc Lond B 205:581–598.

Green DJ, Gordon A. 2008. Metacarpal proportions in Australo-pithecus africanus. J Hum Evol 54:705–719.

Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: paleontologicalstatistics software package for education and data analysis.Palaeo Electronica 4:1–9.

Harrison T. 1986. A reassessment of the phylogenetic relation-ships of Oreopithecus bambolii Gervais. J Hum Evol 15:541–583.

Harrison T. 1991. The implications of Oreopithecus bambolii forthe origins of bipedalism. In: Coppens Y, Senut B, editors.Origine(s) de la bip�edie chez les hominid�es. Paris: Editions duCNRS. p 235–244.

H€urzeler J. 1954. Zur systematischen Stellung von Oreopithe-cus. Verh Naturf Gesellsch (Basel) 65:88–95.

H€urzeler J. 1958. Oreopithecus bambolii Gervais. A preliminaryreport. Verh Naturf Gesellsch (Basel) 69:1–48.

Jablonski NG. 1986. The hand of Theropithecus brumpti. In:Else JG, Lee PC, editors. Primate evolution. Cambridge:Cambridge University Press. p 173–182.

Jolly CJ. 1970. The seed-eaters: a new model of hominid differ-entiation based on a baboon analogy. Man 5:5–26.

Jungers WL. 1984. Aspects of size and scaling in primate biol-ogy with special reference to the locomotor skeleton. YearbPhys Anthropol 27:73–97.

Jungers WL. 1987. Body size and morphometric affinities of theappendicular skeleton in Oreopithecus bambolii (IGF 11778).J Hum Evol 16:445–456.

Jungers WL, Falsetti AB, Wall CE. 1995. Shape, relative size,and size-adjustments in morphometrics. Yearb Phys Anthro-pol 38:137–161.

Kivell TL, Kibii JM, Churchill SE, Schmid P, Berger LR. 2011.Australopithecus sediba hand demonstrates mosaic evolutionof locomotor and manipulative abilities. Science 333:1411–1417.

K€ohler M, Moy�a-Sol�a S. 1997. Ape-like or hominid-like? Thepositional behavior of Oreopithecus bambolii reconsidered.Proc Natl Acad Sci USA 94:11747–11750.

K€ohler M, Moy�a-Sol�a S. 2009. Physiological and life historystrategies of a fossil large mammal in a resource-limited envi-ronment. Proc Natl Acad Sci USA 106:20354–20358.

K€ohler M, Moy�a-Sol�a S, Wrangham RW. 2007. Island rules can-not be broken. Trends Ecol Evol 23:6–7.

Larson SG. 1998. Parallel evolution in the hominoid trunk andforelimb. Evol Anthropol 6:87–99.

Leakey REF, Leakey MG, Walker AC. 1988. Morphology of Afro-pithecus turkanensis from Kenya. Am J Phys Anthropol 76:289–307.

Lovejoy CO, Simpson SW, White TD, Asfaw B, Suwa G. 2009.Careful climbing in the Miocene: The forelimbs of Ardipithe-cus ramidus and humans are primitive. Science 326:70–708.

Madar SI, Rose MD, Kelley J, MacLatchy L, Pilbeam D. 2002.New Sivapithecus postcranial specimens from the Siwaliks ofPakistan. J Hum Evol 42:705–752.

Maier W. 1971. Vergleichend–und funktionell–anatomischeUntersuchungen an der Vorderextremitaet von Theropithecusgelada (Rueppell 1835): Abh Senckenb naturforsch Ges. 527:1–284.

Marzke MW, Pouydebat E, Laurin M, Gorce P, Bels V. 2009. Aclarification of Pouydebat et al., 2008, evolution of graspingamong anthropoids. J Evol Biol 22:2554–2557.

Marzke MW, Shrewsbury MM. 2006. The Oreopithecus thumb:pitfalls in reconstructing muscle and ligament attachmentsfrom fossil bones. J Hum Evol 51:213–215.

Matson SD, Rook L, Oms O, Fox DL. 2012. Carbon isotopicrecord of terrestrial ecosystems spanning the Late Mioceneextinction of Oreopithecus bambolii, Baccinello Basin (Tus-cany, Italy). J Hum Evol 63:127–139.

596 S. ALM�ECIJA ET AL.

American Journal of Physical Anthropology

Mittra ES, Smith HF, Lemelin P, Jungers WL. 2007. Compara-tive morphometrics of the primate apical tuft. Am J PhysAnthropol 134:449–459.

Mosimann JE. 1970. Size allometry: size and shape variableswith characterizations of the lognormal and generalizedgamma distributions. J Am Stat Assoc 65:930–945.

Moy�a-Sol�a S, K€ohler M. 1996. A Dryopithecus skeleton and theorigins of great-ape locomotion. Nature 379:156–159.

Moy�a-Sol�a S, K€ohler M. 2003. La evoluci�on de Oreopithecusbambolii Gervais, 1872 (Primates, Anthropoidea) y la con-dici�on de insularidad. Coloquios de Paleontolog�ıa 1:443–458.

Moy�a-Sol�a S, K€ohler M, Alba DM, Alm�ecija S. 2008. Taxonomicattribution of the Olduvai Hominid 7 manual remains andthe functional interpretation of hand morphology in robustaustralopithecines. Folia Primatol 79:215–250.

Moy�a-Sol�a S, K€ohler M, Alba DM, Casanovas-Vilar I, Galindo J.2004. Pierolapithecus catalaunicus, a new Middle Miocenegreat ape from Spain. Science 306:1339–1344.

Moy�a-Sol�a S, K€ohler M, Alba DM, Casanovas-Vilar I, Galindo J.2005a. Response to comment on “Pierolapithecus catalauni-cus, a new Middle Miocene great ape from Spain”. Science308:203d.

Moy�a-Sol�a S, K€ohler M, Rook L. 1999. Evidence of hominid-likeprecision grip capability in the hand of the Miocene ape Oreo-pithecus. Proc Natl Acad Sci USA 96:313–317.

Moy�a-Sol�a S, K€ohler M, Rook L. 2005b. The Oreopithecusthumb: a strange case in hominoid evolution. J Hum Evol 49:395–404.

Nakatsukasa M, Kunimatsu Y, Nakano Y, Takano T, Ishida H.2003. Comparative and functional anatomy of phalanges inNacholapithecus kerioi, a Middle Miocene hominoid fromnorthern Kenya. Primates 44:371–412.

Napier J. 1962. Fossil hand bones from Olduvai Gorge. Nature196:409–411.

Napier J. 1993. Hands (Revised by Russell H. Tuttle). Prince-ton, NJ: Princeton University Press.

Napier JR. 1956. The prehensile movements of the humanhand. J Bone Joint Surg Am 38:902–913.

Napier JR. 1960. Studies of the hands of living primates. ProcZool Soc Lond 134:647–657.

Napier JR, Davis PR. 1959. The fore-limb skeleton and associ-ated remains of Proconsul africanus. Foss Mamm Afr 16:1–69.

Palombo MR, K€ohler M, Moy�a-Sol�a S, Giovinazzo C. 2008.Brain versus body mass in endemic ruminant artiodactyls: acase studied of Myotragus balearicus and smallest Candiacer-vus species from Mediterranean islands. Quat Int 182:160–183.

Pilbeam DR, Rose MD, Badgley C, Lipschutz B. 1980. Miocenehominoids from Pakistan. Postilla 181:1–94.

Pouydebat E, Laurin M, Gorce P, Bels V. 2008. Evolution ofgrasping among anthropoids. J Evol Biol 21:1732–1743.

Preuschoft H. 1973. Functional anatomy of the upper extremity.Chimpanzee 6:34–120.

Preuschoft H, Godinot M, Beard C, Nieschalk U, Jouffroy KK.1993. Biomechanical considerations to explain important mor-phological characters of primate hands. In: Preuschoft H,Chivers DJ, editors. Hands of primates. Vienna: Springer-Ver-lag. p 245–256.

Quintana J, K€ohler M, Moy�a-Sol�a S. 2011. Nuralagus Rex, gen.et sp. nov., an endemic insular giant rabbit from the Neogeneof Minorca (Balearic Islands, Spain). J Vertebr Paleontol 31:231–240.

Richmond BG, Jungers WL. 2008. Orrorin tugenensis femoralmorphology and the evolution of hominin bipedalism. Science319:1662–1665.

Rook L, Bondioli L, K€ohler M, Moy�a-Sol�a S, Macchiarelli R.1999. Oreopithecus was a bipedal ape after all: evidence fromthe iliac cancellous architecture. Proc Natl Acad Sci USA 96:8795–8799.

Rook L, Gallai G, Torre D. 2006. Lands and endemic mammalsin the Late Miocene of Italy: constraints for paleogeographicoutlines of Tyrrhenian area. Palaeogeogr Palaeocl 238:263–269.

Rook L, Oms O, Benvenuti MG, Papini M. 2011. Magnetostra-tigraphy of the Late Miocene Baccinello-Cinigiano basin (Tus-cany, Italy) and the age of Oreopithecus bambolii faunalassemblages. Palaeogeogr Palaeocl 305:286–294.

Rook L, Renne P, Benvenuti M, Papini M. 2000. Geochronologyof Oreopithecus-bearing succession at Baccinello (Italy) andthe extinction pattern of European Miocene hominoids. JHum Evol 39:577–582.

Sarmiento EE. 1987. The phylogenetic position of Oreopithecusand its significance in the origin of the Hominoidea. Am MusNovitates 2881:1–44.

Sarmiento EE. 1994. Terrestrial traits in the hands and feet ofgorillas. Am Mus Novitates 3091:1–56.

Schlosser M. 1887. Die Affen, Lemuren, Chiropteren usw. ausdem europaischen Terti€ar. Beitr Palaont Geol €Ost 6:1–162.

Schultz AH. 1930. The skeleton of the trunk and limbs ofhigher primates. Hum Biol 2:303–438.

Schultz AH. 1960. Einige beobachtungen und maße am skelettvon Oreopithecus: im vergleich mit anderen catarrhinen pri-maten. Z Morphol Anthropol 50:136–149.

Schwalbe G. 1915. €Uber den fossilen affen Oreopithecus bambo-lii. Zugleich ein beitrag zur morphologie der Z€ahne der pri-maten. Z Morphol Anthropol 19:149–254.

Shrewsbury M, Johnson RK. 1975. The fascia of the distal pha-lanx. J Bone Joint Surg Am 57:784–788.

Shrewsbury MM, Marzke MW, Linscheid RL, Reece SP. 2003.Comparative morphology of the pollical distal phalanx. Am JPhys Anthropol 121:30–47.

Stern JT, Jungers WL, Susman R. 1995. Quantifying phalan-geal curvature: an empirical comparison of alternative meth-ods. Am J Phys Anthropol 97:1–10.

Straus WL Jr. 1942. Rudimentary digits in primates. Q RevBiol 17:228–243.

Straus WL Jr. 1957. Oreopithecus bambolii. Science 126:345–346.

Straus WL Jr. 1958. A new Oreopithecus skeleton. Science 128:523.

Straus WL Jr. 1963. The classification of Oreopithecus. In:Washburn SL, editor. Classification and human evolution.Chicago: Aldine. p 146–177.

Susman RL. 1988. Hand of Paranthopus robustus from member1, Swartkrans: fossil evidence for tool behavior. Science 240:781–784.

Susman RL. 1998. Hand function and tool behavior in earlyhominids. J Hum Evol 35:23–46.

Susman RL. 2004. Oreopithecus bambolii: an unlikely case ofhominid like grip capability in a Miocene ape. J Hum Evol46:105–117.

Susman RL. 2005. Oreopithecus: still apelike after all theseyears. J Hum Evol 49:405–411.

Szalay FS, Delson E. 1979. Evolutionary history of the prima-tes. New York: Academic Press.

Tuttle RH. 1967. Knuckle-walking and the evolution of homi-noid hands. Am J Phys Anthropol 26:171–206.

Tuttle RH. 1969. Quantitative and functional studies on thehands of the Anthropoidea. J Morphol 128:309–364.

Tuttle RH. 1970. Postural, propulsive, and prehensile capabil-ities in the cheiridia of chimpanzees and other great apes.Chimpanzee 2:167–253.

van der Made J. 2008. New endemic large mammals from theLower Miocene of Oschiri (Sardinia): observations on evolu-tion in insular environment. Quat Int 182:116–134.

Ward C. 2007. Postcranial and locomotor adaptations of hom-inoids. In: Henke W, Tattersall I, editors. Handbook ofpaleoanthropology. Heidelberg: Springer Verlag. p 1011–1030.

Ward CV, Kimbel WH, Harmon EH, Johanson DC. 2012. Newpostcranial fossils of Australopithecus afarensis from Hadar,Ethiopia (1990–2007). J Hum Evol 63:1–51.

Whitehead PF. 1993. Aspects of the anthropoid wrist andhand. In: Gebo DL, editor. Postcranial adaptation in nonhu-man primates. DeKalb: Northern Illinois University Press.p 96–120.

THE OREOPITHECUS BAMBOLII POLLICAL DISTAL PHALANX 597

American Journal of Physical Anthropology