New evidence for canine dietary function in Afropithecus turkanensis

Journal of Human Evolution 62 (2012) 707e719

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New evidence for canine dietary function in Afropithecus turkanensis Andrew S. Deane Department of Anatomy and Neurobiology, University of Kentucky, MN 224 UK Medical Centre, Lexington, KY 40514, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 3 May 2011 Accepted 21 March 2012 Available online 1 May 2012

Despite considerable post-cranial and cranial morphological overlap with Proconsul, Afropithecus turkanensis is distinguished from that taxon by a suite of anterior dental and gnathic characters shared in common with extant pitheciin monkeys (i.e. low crowned, robust and laterally splayed canines, procumbent incisors, prognathic premaxilla, powerful temporalis muscles, reduced or absent maxillary sinuses, and deep mandibular corpora). Pitheciins are unique among living anthropoids because their canines serve a habitual dietary function and are not strictly influenced by inter-male competition. Given the functional association between pitheciin canine morphological specializations and sclerocarp foraging, a feeding strategy where the hard pericarps of unripe fruit are mechanically deformed by the canines, it has been suggested that Afropithecus may also have used its canines in a dietary context. This is confirmed by quantitative morphometric analyses of Afropithecus canine curvature and basal dimensions demonstrating that Afropithecus and extant pitheciins (Chiropotes, Cacajao) are distinguished from all other anthropoids by pronounced and evenly distributed mesial canine crown contours as well as greater resistance to canine bending in both the mesiodistal and labiolingual axes. In addition, Afropithecus, Chiropotes and Cacajao are also shown to have significantly longer and more curved premaxillae with greater incisor procumbency that effectively isolates the incisor and canine functional complexes. These morphological similarities are a result of convergence and not a shared derived ancestry. Despite their considerable morphological overlap, it is unlikely that Afropithecus and extant pitheciin diets are identical given significant dissimilarities in their post-canine morphology, maximum angular gape and body size. Nevertheless, Afropithecus canine dietary function is unique among hominoids and may have been a key component for the expansion of hominoids into Eurasia at the end of the early Miocene. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Afropithecus Diet Miocene Hominoid Canine Sclerocarp foraging

Introduction Afropithecus turkanensis is a large-bodied hominoid (w36 kg) from the early Miocene fossil record of East Africa (Leakey et al., 1988, 1991; Leakey and Walker, 1997). Fossils attributed to Afropithecus have historically been restricted to Kenya (w16.8e17.5 Ma), although that taxon may be congeneric with Heliopithecus leakeyi from Ad Dabtiyah, Saudi Arabia (w17.0 Ma) (Andrews and Martin, 1987; WhyBrow et al., 1982; Boschetto et al., 1992; Begun, 2007). Despite considerable cranial and post-cranial overlap with Proconsul, Afropithecus is characterized by a suite of derived craniofacial and anterior dental features morphologically similar to extant pitheciin seed-predators (i.e. Chiropotes, Cacajao) (Table 1). These similarities have been previously cited as evidence of a functional convergence between Afropithecus and extant pitheciins and are key components in dietary reconstructions of the former

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suggesting a diet which included a significant sclerocarp foraging component (Leakey et al., 1988, 1991; Leakey and Walker, 1997). This dietary strategy is consistent with models of hominoid dispersals out of Africa between 19 and 17 Ma. Begun et al. (2003) propose that the shift to thicker occlusal enamel and robust jaws would have allowed hominoids to exploit a wider variety of less preferred food resources, ultimately allowing them to extend their ranges into more northern latitudes (see also van der Made, 1999; Heizmann and Begun, 2001; Begun, 2002; Begun and Nargolwalla, 2004). Sclerocarp foraging Chiropotes and Cacajao are sclerocarp foragers that habitually exploit unripe fruits with hard outer pericarps. These taxa use their specialized anterior dentition to gain access to immature seeds that, prior to ripening, are a significant source of dietary protein that is low in secondary toxic compounds. Chiropotes regularly exploits fruit resources up to fifteen times harder than those eaten

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Table 1 Dentognathic similarities of Afropithecus turkanensis, Chiropotes satanas and Cacajao calvus, indicative of independently acquired adaptations for sclerocarp foraging and seed predation (Leakey and Walker, 1997). Sclerocarp foraging adaptations 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.

Root of the maxillary zygomatic process positioned anteriorly at M1 Canine jugum prominent and post-canine fossa strongly developed Strongly heteromorphic I1 and I2 C1 robust, tusk-like and externally rotated Upper premolar occlusal area enlarged (relative to area of M1) Strongly proclined symphyseal axis, moderately-developed inferior transverse torus, robust corpus Mesiodistally narrow I1 and I2, labiolingually thick, high crowned, strongly procumbent and styliform Molar cusps low, rounded Reduced or absent maxillary sinus Large diastema between C1 and I2 C1 lingual crest Extensive canine wear, horizontal wear plane Deep mandibular corpora and well-developed temporalis muscle Strong markings for the labial depressors

by sympatric primates by using its low crowned and robust canines to mechanically fracture hard fruit pericarps (van Roosmalen et al., 1988; Ayres, 1989; Kinzey and Norconk, 1990; Kinzey, 1992; Anapol and Lee, 1994). Pitheciin canines are wedge shaped which creates well-developed cutting edges on the mesial and distal surfaces of the maxillary and mandibular crowns respectively. The splayed orientation and medial rotation of pitheciin canines positions these cutting surfaces outside the contour of the dental arcade and, in combination with the large diastema separating each canine from the lateral incisor, functionally isolates the canines from incisors making it possible for them to puncture hard-objects with considerable force (Kinzey, 1992; Anapol and Lee, 1994). Once the canines have been used to mechanically fracture the hard outer pericarp, the procumbent and horizontally inclined incisors, which form an efficient nipping and cropping device, are used to remove the relatively soft and pliable seed within (Kinzey and Norconk, 1990; Kinzey, 1992; Anapol and Lee, 1994). This strategy is thought to be an adaptive mechanism for dealing with intense competition, particularly from sympatric primates who prefer ripe fruit with softer pericarps. Although seeds are the most important dietary component for Chiropotes and Cacajao year round, there is seasonal fluctuation in seed consumption and seeds are identified as a fallback resource eaten more frequently during annual periods of resource scarcity (van Roosmalen et al., 1988; Ayres, 1989; Kinzey and Norconk, 1990). Afropithecus diet Despite anterior dental and gnathic characters shared in common by both Afropithecus and extant pitheciins, which may indicate some degree of functional convergence in feeding biomechanics, there are also significant anatomical differences suggesting these taxa might have had dissimilar diets. Both Chiropotes and Afropithecus have relatively bunodont molars, although the former has thin enamel and well-developed crenulations while the latter is thickly enameled with little to no enamel crenulation (Leakey et al., 1988, 1991; Leakey and Walker, 1997; Martin et al., 2003; Smith et al., 2003). Likewise, the ratio of height over jaw length for Afropithecus falls within the range for Papio implying that it had an extremely large angular gape relative to extant pitheciins (Lucas, 1981). Although this is not uncommon in taxa with high crowned canines used in yawning displays, it is unexpected in a primate with low crowned, tusk-like canines that potentially serve a dietary function. It has been suggested that the large maximum gape in Afropithecus may be related to stripping bark

from trees or perhaps the processing of extremely large fruits (Leakey and Walker, 1997). Most significantly, Afropithecus is up to ten times larger than either Chiropotes or Cacajao, meaning that, while overlapping in a number of derived anterior dental characters, the feeding energetics associated with the divergent body sizes of these taxa are almost certainly dissimilar. Formal dietary analyses of Afropithecus dental morphology and dental wear, while broadly consistent with a sclerocarp foraging dietary model (Leakey et al., 1988), have yet to conclusively identify a canine dietary function for that taxon. Analyses of relative molar cusp proportions identify Afropithecus maxillary and mandibular molar cusp morphology as evenly split between extant soft object frugivores (i.e. Pan troglodytes ssp.) and dedicated folivores (i.e. Gorilla beringei beringei) (Smith, 1999). This discrepancy has been explained as either a consequence of elongated third molars, a trait also observed in Proconsul and one that is associated with extant folivores, or as an indication of a novel dietary adaptation involving unique combinations and proportions of food textures not represented by extant hominoids (Smith, 1999). Low magnification analyses of early and middle Miocene hominoid molar microwear including Afropithecus identify that taxon as a hard-object frugivore (Grossman, 2008, 2009). These wear patterns are consistent with enamel thickness measurements for Afropithecus that are broadly similar to other thickly enameled Miocene apes and Pliocene hominins (i.e. Griphopithecus, Sivapithecus, Australopithecus) (Martin, 1985; Smith et al., 2003). More recently, morphometric analysis of early Miocene fossil catarrhine incisor curvature has shown that Afropithecus has more pronounced incisor heteromorphy, and I1 and I2 mesiodistal and labial curvature, than all other early Miocene East African catarrhines, a morphological pattern associated with an increased reliance on hard-object frugivory (Deane, 2007, 2009a, 2009b). Additionally, the I1 crowns for that taxon are considerably less curved and labiolingually broader than all other large-bodied early Miocene taxa and are superficially similar to the styliform pitheciin condition (Kinzey, 1992; Leakey and Walker, 1997). This is consistent with the interpretation that Afropithecus may have used these flattened, procumbent and mesiodistally narrow mandibular incisors to extract seeds from unripened fruits in a manner similar to Chiropotes and Cacajao (Kinzey, 1992; Anapol and Lee, 1994; Deane, 2007, 2009b). Although analyses of incisor dimensions and curvature identify a significant overlap in Afropithecus, Chiropotes and Cacajao dental morphology consistent with a sclerocarp foraging dietary model (Deane et al., 2005, 2009a, 2009b, in press; Kiser et al., 2010), a similar treatment of the canine dentition and premaxilla is presently lacking. Given that canine dietary function is arguably the defining component of sclerocarp foraging adaptations, a functional analysis of canine and premaxillary morphology is necessary to determine if Afropithecus had such a feeding adaptation. The present study is intended to address this shortcoming by examining canine curvature and bending strength and premaxillary morphology in an attempt to identify the degree to which Afropithecus and extant pitheciin canines are functionally convergent. Methods Sample High resolution images of extant hominoid and ceboid (n ¼ 160) maxillary and mandibular canines were collected from individuals housed at the American Museum of Natural History (AMNH; New York, USA), The Smithsonian Institution (NMNH; Washington D.C., USA), The Royal Ontario Museum (ROM; Toronto, Canada), and the Royal Museum for Central Africa (RMCA; Tervuren, Belgium). Digital images of the skull in lateral view and in occlusal view were

A.S. Deane / Journal of Human Evolution 62 (2012) 707e719

also collected for each individual. Nine genera (three hominoid, six ceboid) representing eleven species were sampled (Table 2). Afropithecus turkanensis, Proconsul heseloni and Proconsul nyanzae specimens with preserved canines and premaxillae were examined at the National Museum of Kenya (NMK) (Nairobi, Kenya). A high resolution cast of an as of yet undescribed canine (Nabwal, Kenya) attributed to Afropithecus was included in the canine bending strength analysis but was excluded from all canine crown curvature analyses. Specimens belonging to the genus Proconsul were allocated to species as per the taxonomic identifications reported by Walker et al. (1993). A complete list of the fossil taxa and individual specimen numbers is presented in Table 3.

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Table 3 Fossil catarrhines. Maxillary canine Proconsul sp.

KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU KNM-RU

1677 1982 16764 7290 1684 1960 1688 1769 2049 1942 5938

Afropithecus turkanenis

KNM-WK 16999 KNM-WS 11599 undescribed Nabwal caninea

Data collection Extant and fossil individuals were selected for inclusion in the study sample if they had unworn or only moderately worn canines. Digital images were generated in a series of standardized planes for all upper and lower canine crowns. Canine orientation and splay may vary considerably across taxa and even within a given species. Canine orientation was normalized by positioning the mesiodistal and labiolingual crown axes perpendicular to the camera lens. All canines were photographed in lateral profile to represent the maximum mesial crown curvature and again in anterior view to represent the maximum labial crown curvature (Fig. 1). Only the mesial and labial crown curvatures were selected for study owing to the minimal wear these surfaces receive relative to the distal and lingual surfaces. Maximum mesiodistal length (MD) and labiolingual breadth (LL) was recorded for each crown using Mitutoyo digital calipers. Each linear measurement was repeated three times and an averaged value was used in the final analysis. A ratio of MD length/LL breadth was used to represent basal crown shape. Mesial and labial canine crown curvature was quantified using high resolution polynomial curve fitting (HR-PCF) (Deane et al., 2005; Deane, 2007). Each curve (represented as the line extending between the crown apex and the enamel-dentin junction) was modeled as a 2nd order polynomial function with three coefficients (Y ¼ Ax2 þ Bx þ C). The first coefficient (A) expresses the nature and degree of the longitudinal curvature whereas the second (B) and third (C) reflect aspects of the orientation of that curve with respect to the rest of the element (i.e. element rotation, element position in 2D space). High resolution digital images of hominoid and ceboid skulls in lateral and occlusal view (Fig. 2) were generated for 2D morphometric analyses of incisor procumbency angle, premaxilla length and premaxilla curvature. Incisor orientation angles and premaxilla length measurements were calculated using ImageJ 2D morphometric software. Premaxilla curvature was quantified using HR-PCF. Incisor procumbency angles (Fig. 2D) were calculated as the angle formed by the intersection of a line through the long axis of the upper central incisor (i.e. a line drawn from the anterior

Mandibular canine KNM-RU 1698 KNM-RU 1717 KNM-RU 1769 KNM-RU 1791 KNM-RU 1889 KNM-RU 1914 KNM-RU 1960 KNM-RU 1999 KNM-RU 2034 KNM-RU 2036 KNM-RU 2087 KNM-RU 7290 KNM-RU 1674 KNM-WS 11599

a Due to poor preservation, the undescribed Nabwal canine was only included in the maxillary canine bending strength analysis.

intersection of the enamel-dentin junction to the crown apex) and a line drawn through the most posterior intersection of the M3 and its alveolus and the most posterior intersection of the maxillary canine and its alveolus. Premaxilla length (Fig. 2A) was measured as the linear distance from the most anterior point of the premaxilla to a perpendicular line spanning the distance between the most distal points of the maxillary canines (bi-canine breadth). Premaxilla curvature (Fig. 2C) was quantified for a curved arc extending from the anterior intersection of the right maxillary canine root and its alveolus to the same point on the left side. Between these points the arc of curvature was defined by the mesial and distal intersections of the central and lateral incisor roots and their alveoli that mirror the anterior most projection of the premaxilla. Premaxillary curvatures were modeled as 2nd order polynomial functions using HR-PCF. Data analysis All metric and curvature data were standardized for scale. Although the component coefficients of the polynomial functions defining canine curvature, shape and angle measurements are by

Table 2 Extant anthropoids.

Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta

Maxillary canine

Mandibular canine

Palate length

Palate curvature

Incisor procumbency

20 25 20 21 10 5 6 5 10

28 54 28 11 10 5 6 5 10

29 52 0 13 10 5 6 5 10

29 51 7 13 10 5 6 5 10

29 51 0 13 10 5 6 5 10 Figure 1. Canine crown curvature; A. mesial curvature B. labial curvature.

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Figure 2. Premaxilla dimensions and incisor orientation measurements. A. premaxilla length; B. bi-canine breadth; C. arc of premaxilla curvature; D. incisor orientation angle in.

definition scale-independent (Deane et al., 2005; Deane, 2007), metric variables are potentially subject to the effects of isometric size-related scaling. Premaxilla length measurements were adjusted by dividing raw measurements by M2 length. The length of the second upper molar was used as an indicator of body size both because: a) the linear dimensions of primate check teeth, including the second maxillary molar, exhibit relatively low variability and are therefore a suitable proxy for body size (Kay, 1973;

Gingerich and Schoeninger, 1979); and b): the use of molar dimensions increases the probability that the resulting dataset can be employed in future applications to the fossil record where preservation is a limiting factor. Morphometric analysis of canine curvature was used to determine how patterns of canine curvature vary with respect to diet and phylogeny. Mandibular and maxillary canine samples were analyzed separately. Given that the 2nd (B) and 3rd (C) coefficients

Table 4 Maxillary canine one-way ANOVA results with Bonferroni significance values for mesial curvature. A1 ¼ analysis of entire sample. A2 and A3 represent supplemental analyses excluding non-pitheciin platyrrhines and hominoids respectively; B. the ratio of MD length/LL breadth. A1. Mesial (A) Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta Proconsul

Pan

Gorilla

.018

.008 .05

2

A . Mesial (A) Pan Gorilla Pongo Chiropotes Cacajao Proconsul 3

A . Mesial (A) Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta B. MD/LL Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Alouatta Proconsul

Pongo

Chiropotes

Cacajao

.018

.05

Callicebus

Cebus

Lagothrix

Alouatta

.003 .02

Pan

Gorilla

Pongo

.013 .047

.006 .031

.002 .013

Chiropotes

Cacajao

.002 .001 .010 .000

.002 .001 .010 .000

Pan

Gorilla

Pongo

.014 .012

.002 .000 .001

.027 .019

.002

.008

.001

Chiropotes

Cacajao

.012

.033

Callicebus

Cebus

Lagothrix

Chiropotes

Cacajao

Callicebus

Cebus

.000

.000

.000

.000

Alouatta

.000

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Figure 3. Maxillary canine; boxplots showing the range and mean values for A. mesial crown curvature (measured as the 1st coefficient of the 2nd order polynomial defining curvature) for extant ceboids and extant and fossil hominoids; B. the ratio of mesiodistal length (ML)/labiolingual breadth (LL) for extant ceboids and extant and fossil hominoids; C. labial crown curvature (measured as the 1st coefficient of the 2nd order polynomial defining curvature) for extant ceboids and extant and fossil hominoids.

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Figure 4. Comparison of maxillary canine mesial contour curvature; A. Pan B. Gorilla C. Chiropotes D. Cacajao E. Afropithecus.

of a 2nd order polynomial function represent characteristics unrelated to curvature magnitude (i.e. element rotation, element position in 2-dimensional space), the 1st polynomial coefficient (A) was used as a proxy for curvature magnitude. Boxplots representing the median, range and 50% confidence interval of the first polynomial coefficient (A) defining mesial and labial canine curvatures and the ratio of linear canine crown dimensions (MD length/LL breadth) were generated for all extant and fossil taxa. Similar boxplots were also generated for premaxilla length, premaxilla curvature, and incisor procumbency angle. A one-way ANOVA with post-hoc multiple comparison tests (i.e. Bonferonni) was carried out for each study variable to identify statistically significant variation among the group means of a subset of the study sample (i.e. all extant taxa and Proconsul) to determine if sclerocarp foraging ceboids are morphologically distinct from nonsclerocarp foraging hominoids and ceboids. Canine bending strength values were also calculated for a sample (n ¼ 3) of Afropithecus maxillary canines (Table 4) for comparison with published average maxillary canine bending strength values for 114 extant anthropoid taxa (Plavcan and Ruff, 2008). Canine bending strength was calculated from raw metric data (i.e. crown height, MD length, LL breadth) using the formulas in van Valkenburgh and Ruff (1987) (see also Plavcan and Ruff, 2008). This method quantifies resistance to bending at the base of the crown and models the canine crown as a beam. Maximum bending strength was calculated separately about the MD and BL axes, and log normalized bending strength values were plotted against log normal average body mass values in Plavcan and Ruff (2008). Results Maxillary canine Mesial maxillary canine curvature and basal canine crown dimensions differentiate extant pitheciins and Afropithecus from all other hominoid and ceboid taxa (Fig. 3). Pitheciin and Afropithecus maxillary canines have more pronounced mesial curvatures that are evenly distributed along their length between the enameldentin junction (EDJ) and the crown apex. The mesial borders of the maxillary canines of all other taxa are characterized by a sharply angled curvature near the base of the crown that is followed by a posteriorly sloping yet relatively uncurved mesial margin. This gives the maxillary canines in non-sclerocarp foraging taxa a characteristically ‘swept back’ appearance where the crown apex is posteriorly deflected (i.e. the crown apex is positioned closer to the distal crown border than to the mesial border). This posterior deflection is absent in Afropithecus and extant pitheciin maxillary

canines and the position of the crown apex is intermediate between the mesial and distal crown margins (Fig. 4). Unlike mesial curvature, labial curvature does not discriminate among sample taxa, however Afropithecus mean sample labial curvature considerably exceeds all other taxa (i.e. the mean 1st coefficient [A] value for Afropithecus ¼ .15 whereas similar values for all other sample taxa range between .06 and .11). Similarly, the ratio of basal crown dimensions (MD/LL) does not effectively segregate pitheciins from non-pitheciins, but instead broadly separates the labiolingually-compressed canines of Alouatta, Proconsul and extant hominoids from the labiolingually broader pitheciin, Callicebus, Cebus and Afropithecus canines. The Afropithecus maxillary canine sample is small (n ¼ 2; KNMWT 16999; KNM-WS 11599) and therefore not suitable for parametric testing. Bonferroni post-hoc test values from a one-way ANOVA of a sample subset, excluding Afropithecus, demonstrates that Chiropotes and Cacajao mesial curvature (A) sample means are significantly different from all extant hominoids and Proconsul but are not statistically different from non-pitheciin platyrrhines or one another (Table 4A1). When extant hominoids and Proconsul are excluded from the analysis (Table 4A3) Bonferroni post-hoc tests values indicate that the pitheciins, Cacajao and Chiropotes, are significantly different from all other platyrrhines. Likewise, when non-pitheciin platyrrhines are excluded, there is a complete and total separation of pitheciin and hominoid taxa (Table 4A2). The failure of the initial one-way ANOVA including all taxa to identify statistically significant differences among pitheciin and nonpitheciin platyrrhines is almost certainly a consequence of the reduced power and resolution of the ANOVA resulting from unequal sample variances and sample sizes among study taxa. The Cebus (n ¼ 6), Callicebus (n ¼ 5) and Lagothrix (n ¼ 5) samples, in particular, are notably smaller than the samples representing all other taxa (i.e. n ¼ 10e25 individuals). Regardless, the collective results of the initial ANOVA and supplemental ANOVA’s demonstrate that pitheciins are significantly different from all other taxa included in the present study. There were no statistically significant differences reported for interspecific comparisons of labial maxillary canine curvature. Bonferroni values reported for mean sample ratios of canine basal dimensions (MD/LL) indicate that there is a statistically significant difference between living hominoids and the grouping of pitheciins and Callicebus, although there was no significant distinction between Chiropotes and Pan or Pongo. Alouatta has the most labiolingually-compressed canines and is distinct from all other study taxa. Maxillary canine bending strength was calculated separately about the MD and LL axis for three specimens of A. turkanensis

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(KNM-WT 16999; KNM-WS 11599; undescribed Nabwal canine) with sufficient preservation of the canine crown. Leakey and Walker’s (1997) estimate of 36 kg was used as the body mass value for Afropithecus. These results were then compared with published average maxillary canine bending strength values for 114 extant anthropoid taxa (Plavcan and Ruff, 2008). Similar to the canines of sclerocarp foraging pitheciins, Afropithecus canines exhibit increased resistance to bending at the base of the crown when modeled as a beam. Fig. 5 represents bivariate plots of log

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normalized body mass values against log normalized canine bending strength values for both the MD (Smd) and LL (Sbl) axes. Afropithecus and pitheciin sclerocarp foragers are positioned well above the line of best fit. Non-pitheciin anthropoids cluster around the line of best fit indicating that they have lower maxillary canine bending strength in both dimensions (MD and LL) relative to Afropithecus and extant pitheciins. Mandibular canine Unlike the results reported for the maxillary canine sample, the ratio of basal crown dimensions (MD length/LL breadth) and the mesial and labial curvature of the mandibular canine failed to effectively discriminate between sclerocarp foraging pitheciins and non-sclerocarp foraging sample taxa. The lone Afropithecus mandibular canine specimen (KNM-WS 11599) has mesial and labial curvatures that are more pronounced than the sample mean for any other taxon. Likewise, with the exception of Callicebus, the ratio of basal dimensions is greatest for Afropithecus. KNM-WS 11599 is more labiolingually-compressed than any other taxon sample mean except Callicebus and has a MD length that is almost 1.5 greater than that specimen’s LL breadth (Fig. 6). Among extant taxa, Pongo has the most pronounced mesial and labial crown curvature. Bonferroni post-hoc test values from oneway ANOVA’s of sample subsets excluding Afropithecus demonstrate that, while not significantly different from one another, the mean labial curvature values reported for Pongo and Proconsul are significantly different from Pan, Gorilla, Cacajao, Cebus, Callicebus, and Alouatta. Alouatta is also significantly different from Chiropotes. Likewise, while Chiropotes and Cacajao have the lowest mean mesial curvature values, Bonferroni post-hoc tests identify statistically significant differences between both pitheciins and Pongo in addition to differences between Chiropotes and Pan, Pongo, Alouatta and Proconsul. Bonferroni post-hoc test values from a one-way ANOVA of the ratio of basal mandibular canine dimensions demonstrate that Callicebus and Alouatta have longer MD basal dimensions relative to LL breadth and are significantly different from all other extant anthropoids, although Alouatta is not significantly different from Cebus. Proconsul is significantly different from Pan, Gorilla and Callicebus (Table 5). Premaxilla length Premaxilla length measurements differentiate extant pitheciins and Afropithecus from all other hominoid and ceboid taxa (Fig. 7a) and demonstrate that the former have relatively longer premaxillae relative to M2 length (Fig. 8). Bonferroni post-hoc tests values from a one-way ANOVA of M2 size adjusted premaxilla length measurements for a sample subset excluding Afropithecus identify statistically significant differences between sclerocarp foragers (Chiropotes, Cacajao) and non-sclerocarp foragers (Pan, Gorilla, Alouatta, Callicebus, Cebus, Lagothrix) and among members of the non-sclerocarp foraging group (Table 6A). The Pan and Gorilla sample means are significantly different from one another and Pan premaxilla length approaches observed values for Cebus. Although premaxilla length values for Cebus exceed all other non-pitheciin platyrrhines, values for that taxon are intermediate between pitheciins and all other platyrrhines and statistically distinct from all study taxa except Pan (Table 6A). Premaxilla curvature

Figure 5. Bivariate plots of MD and LL maxillary canine bending strength against body mass.

Similar to premaxilla length, premaxilla curvature differentiates extant pitheciins and Afropithecus from all other sample taxa. Afropithcus, Chiropotes and Cacajao have premaxillae that narrow

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Figure 6. Mandibular canine; boxplots showing the range and mean values for A. mesial crown curvature (measured as the 1st coefficient of the 2nd order polynomial defining curvature) for extant ceboids and extant and fossil hominoids; B. the ratio of mesiodistal length (ML)/labiolingual breadth (LL) for extant ceboids and extant and fossil hominoids; C. labial crown curvature (measured as the 1st coefficient of the 2nd order polynomial defining curvature) for extant ceboids and extant and fossil hominoids.

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Table 5 Mandibular canine one-way ANOVA results with Bonferroni significance values for A. mesial curvature; B. the ratio of MD length/LL breadth; C. Labial curvature. A. Mesial (A) Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta Proconsul B. MD/LL Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Alouatta Proconsul C. Labial (A) Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta Proconsul

Pan

Gorilla

Pongo

Chiropotes

Cacajao

Callicebus

Cebus

Lagothrix

Alouatta

.001 .016

.000 .052

.045 .000

.021 Pan

Gorilla

.000

.000

.000 .009

.000 .001

Pan

Gorilla

.000

.000

Pongo

Pongo

Chiropotes

Cacajao

.000

.000

.000

.007

.016

.006

Chiropotes

Cacajao

Callicebus

Cebus

Alouatta

.000 .004 .000 Callicebus

Cebus

Lagothrix

Alouatta

.001 .001 .000 .002

.45

.000

anteriorly and that have a higher radius of curvature than do nonsclerocarp foragers (Fig. 7b; Fig. 8). This results in a characteristically ‘beaked’ appearance that effectively staggers the incisors such that the lateral incisors are positioned lateral and posterior to the central incisors. As in the Afropithecus type (KNM-WK 16999) it is common for Chiropotes and Cacajao to have mesially oriented lateral incisors that overlap slightly with the central incisors. Bonferroni post-hoc tests values from a one-way ANOVA of premaxilla curvature for a sample subset excluding Afropithecus identify statistically significant differences between extant pitheciins and all other taxa but not among individual taxa within the pitheciin and non-sclerocarp foraging groups (Table 6B). Incisor procumbency The results of the analysis of incisor procumbency mirror the results for analyses of premaxilla length and curvature. The angle formed by the intersection of a line through the long axis of the upper central incisor and a line drawn through the most posterior intersection of the M3 and its alveolus and the most posterior intersection of the maxillary canine and its alveolus was highest in Chiropotes and Cacajao indicating that these taxa have incisors that are more procumbent (i.e. horizontally oriented). All other nonpitheciin taxa are noticeably less procumbent, although Alouatta, Lagothrix and Gorilla are intermediate between the pitheciins group and a cluster including Pan, Cebus and Callicebus. Afropithecus, while not as procumbent as extant pitheciins, is intermediate between that group and the Gorilla, Lagothrix and Alouatta group (Fig. 7c). Bonferroni post-hoc tests values from a one-way ANOVA of procumbency angle values for a sample subset excluding Afropithecus identify statistically significant differences between extant pitheciins and all other taxa (Table 6C).

.034

.035

.000

Discussion The results of the present study identify a clear distinction between the canine and premaxillary morphology of sclerocarp foraging pitheciins (Chiropotes, Cacajao) and non-sclerocarp foraging hominoids and ceboids (Pan, Gorilla, Pongo, Alouatta, Cebus, Callicebus, Lagothrix, Proconsul). This distinction demonstrates that sclerocarp foragers are characterized by a suite of anterior dental and gnathic characters including an elongated and highly curved premaxilla, a greater degree of incisor procumbency, and maxillary canines with more pronounced and evenly distributed mesial crown curvature and greater bending strength relative to non-sclerocarp foragers. Although only distantly related to extant pitheciins, Afropithecus premaxillary and canine morphology converges on the pitheciin condition for each of these traits. These similarities are consistent with prior suggestions that, like pitheciins, Afropithecus canines may have served an habitual dietary function (Leakey et al., 1988, 1991; Leakey and Walker, 1997) and with more recent reconstructions of a hard-object diet for Afropithecus based on incisor crown curvature and shape (Deane, 2007, 2009a, 2009b). This is significant because variation in anthropoid canine shape and size is almost exclusively associated with inter-male competition, and habitual canine dietary function is unique to Afropithecus and the pitheciins (Roosmalen et al., 1988; Ayres, 1989; Plavcan, 1993; Anapol and Lee, 1994). Given that the use of the maxillary canines to mechanically fracture the hard outer pericarps of unripened fruit is the defining characteristic of the pitheciin sclerocarp foraging adaptation, it is reasonable to predict that aspects of maxillary canine morphology will be a response to the role of that tooth in dietary function. Morphometric analyses of basal canine dimensions and mesial and labial crown curvature demonstrate that pitheciin and Afropithecus

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Figure 7. Boxplots showing the range and mean values for A. premaxilla length; B. premaxilla curvature; C. incisor procumbency for extant ceboids and extant and fossil hominoids.

A.S. Deane / Journal of Human Evolution 62 (2012) 707e719

717

Figure 8. Comparison of premaxilla curvature and length; A. Pan; B. Gorilla; C. Alouatta; D. Chiropotes; E. Cacajao; F. Afropithecus.

maxillary canines are distinguished from all other hominoids and ceboids by an evenly distributed and highly curved mesial crown margin. In contrast, taxa with canines that are used less frequently in a dietary context have a sharply angled curve near the base of the crown followed by a posteriorly sloping yet relatively uncurved mesial contour (Fig. 4). It is possible that the more anteriorly positioned maxillary canine crown apex and evenly distributed and gently curved mesial border observed in pitheciins and Afropithecus may act to increase crown bending strength when force is directed anteriorly from a posterior position. Likewise, when canine loading is directed posteriorly from a position anterior to the crown, as it is most often in pitheciins (Kinzey and Norconk, 1990), the object being consumed contacts only a limited segment of that contour and is therefore subjected to greater localized stresses at that specific and limited point of contact which is mechanically beneficial in the deformation and crushing of hard-objects. Afropithecus canine dietary function, or at least the increased mechanical loading of the canines, is confirmed by the results of the maxillary canine bending analysis in the present study which demonstrate that the estimated canine bending strength for that taxon is comparable to that in Chiropotes and Cacajao. Canine morphology is almost certainly the cornerstone of the pitheciin sclerocarp foraging model, however, that adaptation is also represented by specialized incisor (Deane, 2007, 2009a; 2009b, in press) and premaxillary morphology. The results of

separate analyses of premaxilla length, curvature and incisor procumbency all identify Afropithecus as most similar to extant pitheciins and provide further evidence of dietary canine use in that taxon. Observations of feeding behavior identify separate and unique functional roles for pitheciin canines and incisors. Pitheciin canines are used to mechanically fracture unripened fruit pericarps whereas incisors perform a separate nipping and cropping function and are most often engaged to extract fruit pulp and seeds once the pericarp has been opened (van Roosmalen et al., 1988; Ayres, 1989; Kinzey and Norconk, 1990; Kinzey, 1992; Anapol and Lee, 1994). The increased length and curvature of the anterior premaxilla physically separates the incisors from the canines, effectively isolating the incisor and canine functional complexes. In addition, the pronounced curvature of the anterior premaxilla effectively staggers the incisors such that the incisal margins of the central incisors are anteriorly positioned relative to the incisal margins of the lateral incisors and are therefore better able to act independently of the lateral incisors. This staggered incisor position results in mesially positioned lateral incisors with crowns that overlap the central incisors giving pitheciin and Afropithecus anterior premaxillae a characteristically ‘beaked’ appearance. Similarly, procumbent incisors further isolate the incisor and canine functional complexes and more appropriately position the incisors for the removal of fruit pulp from the inner surface of the pericarp.

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Table 6 Palate measurement one-way ANOVA results with Bonferroni significance values for A. palate length; B. palate curvature; C. incisor procumbency. A. Premaxilla length Pan Gorilla Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta B. Premaxilla curvature Pan Gorilla Pongo Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta C. Incisor angle Pan Gorilla Chiropotes Cacajao Callicebus Cebus Lagothrix Alouatta

Pan

Gorilla

.000 .000 .000 .007

.000 .000 .000

.002 .000

.022

Pan

Gorilla

Pongo

.000 .000

.000 .000

.000 .000

Pan

.014 .000 .000

.019

Gorilla

.000 .000 .005

Chiropotes

Cacajao

Callicebus

Cebus

.000 .000 .000 .000

.000 .000 .000 .000

.004 .001 .000

.001

Chiropotes

Cacajao

.000 .000 .000 .000

.000 .000 .000 .000

Chiropotes

Cacajao

.000 .000 .000 .000

.000 .000 .000 .000

The weight of the morphometric evidence presented here supports the identification of habitual canine dietary function in Afropithecus, however, it is unlikely that Afropithecus and extant pitheciin diets are identical given significant dissimilarities in molar morphology, molar enamel thickness, and estimates of maximum angular gape and body size. Although overlapping with extant pitheciins for an extensive suite of derived anterior dental and premaxillary characters, Afropithecus would most likely have had a more diverse dietary strategy, of which sclerocarp foraging was only a single component. Regardless, Afropithecus canine dietary function, in and of itself, is significant given the existing fossil record for that taxon and its biogeographical implications. Afropithecus canine dietary function and a greater reliance on hard-object feeding are consistent with models of hominoid dispersals out of Africa between 19 and 17 Ma. It has been suggested that an increased reliance on hard-object feeding and an adaptive shift to thicker occlusal enamel and robust jaws would have made it possible for fossil hominoids to exploit a wider variety of lesser quality foods and that this may ultimately have allowed hominoids to expand their range outside of East Africa (van der Made, 1999; Heizmann and Begun, 2001; Begun, 2002; Begun et al., 2003; Begun and Nargolwalla, 2004). Afropithecus represents the earliest appearance of such an adaptation, and if it is in fact congeneric with Heliopithecus then it also represents the first hominoid to significantly extend its range beyond East Africa. Within a million years of the first appearance of that taxon there are hominoids with hardobject feeding adaptations extending as far north as Germany and as far south as Namibia. Although post-canine adaptations associated with hard-object feeding are common among middle Miocene hominoids, none of these possess a comparable suite of derived anterior dental and gnathic characters suggesting a similar type of canine dietary function (although see McCrossin and Benefit, 1997; Benefit et al., 2005 for a contra opinion). This suggests that

Callicebus

Callicebus

Cebus

Cebus

Lagothrix

Lagothrix

Lagothrix

.001

Afropithecus may be too derived to have been a direct ancestor of middle Miocene hard-object feeding hominoids and that canine dietary function in that taxon likely represents a specialized dietary adaptation that is unique among hominoids. Conclusion The specialized suite of anterior and dental gnathic characters identified in this study as shared between Afropithecus and extant pitheciin sclerocarp foragers provides new evidence to support the identification of canine dietary function in the former. Although an elongated and highly curved premaxilla, a greater degree of incisor procumbency, and maxillary canines with more pronounced and evenly distributed mesial crown curvature and greater bending strength distinguish Afropithecus and extant pitheciins from all other anthropoid primates, these similarities are a result of convergence and not a shared derived ancestry. Despite considerable similarities in their anterior dental and gnathic anatomy, it is unlikely that Afropithecus and extant pitheciin diets are identical given significant dissimilarities in their post-canine morphology, maximum angular gape and body size. Regardless, the identification of Afropithecus canine dietary function is significant for our understanding of early Miocene hominoid biogeography and the role that hard-object feeding may have played in allowing hominioids to expand into Eurasia. Acknowledgements Thanks to Linda Gordon (Smithsonian), Wim Van Neer (RMCA), Bill Stanley (FMNH) and Ema Mbua (NMK) for access to collections under their care. Michael Plavcan and Magdalena Muchlinski provided technical advice and/or helpful discussions that greatly improved this manuscript. A special thanks to John Fleagle for the

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