Given the central adaptive role of diet, paleodietary inference is essential for understanding the relationship between evolutionary and paleoenvironmental change. Here we rely on dental microwear analysis to investigate the role of dietary specialization in the diversification and extinction of Miocene hominoids from Western Eurasian between 14 and 7 Ma. New microwear results for five extinct taxa are analyzed together with previous data for other Western Eurasian genera. Except Pierolapithecus (that resembles hard-object feeders) and Oreopithecus (a soft-frugivore probably foraging opportunistically on other foods), most of the extinct taxa lack clear extant dietary analogues. They display some degee of sclerocarpy, which is most clearly expressed in Griphopithecus and Ouranopithecus (adapted to more open and arid environments), whereas Anoiapithecus, Dryopithecus and, especially, Hispanopithecus species apparently relied more strongly on soft-frugivory. Thus, contrasting with the prevailing sclerocarpic condition at the beginning of the Eurasian hominoid radiation, soft- and mixed-frugivory coexisted with hard-object feeding in the Late Miocene. Therefore, despite a climatic trend towards cooling and increased seasonality, a progressive dietary diversification would have occurred (probably due to competitive exclusion and increased environmental heterogeneity), although strict folivory did not evolve. Overall, our analyses support the view that the same dietary specializations that enabled Western Eurasian hominoids to face progressive climatic deterioration were the main factor ultimately leading to their extinction when more drastic paleoenvironmental changes took place.
Citation: DeMiguel D, Alba DM, Moyà-Solà S (2014) Dietary Specialization during the Evolution of Western Eurasian Hominoids and the Extinction of European Great Apes. PLoS ONE 9(5): e97442. doi:10.1371/journal.pone.0097442
Editor: Lorenzo Rook, University of Florence, Italy
Received: March 21, 2014; Accepted: April 14, 2014; Published: May 21, 2014
Copyright: © 2014 DeMiguel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. Our data may be found within the manuscript and in the supporting information Tables.
Funding: This work was funded by the Spanish Ministerio de EconomÍa y Competitividad (CGL2011-28681/BTE, CGL2011-27343, JCI-2011-11697 (to DDM), and RYC-2009-04533 (to DMA)) and the Generalitat de Catalunya (2009 SGR 754 GRC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Dietary Adaptation and the Hominoid Radiation in Western Eurasia
After an initial radiation in Africa during the Early to Middle Miocene , hominoids dispersed into Eurasia, where they diversified into multiple great ape genera from ca. 14 Ma onwards –. Available data suggest that vicariance and parallel evolution played a significant role in the Eurasian hominoid radiation, with dryopithecines diversifying in Europe, pongines in Asia, and maybe hominines in Africa , . Dietary adaptations have long been regarded as very significant for understanding the dispersal of hominoids from Africa into Eurasia and their subsequent radiation , –. Paleodietary inference is thus paramount for understanding how fossil great apes adapted to changing environmental conditions through time. Unlike in hominins, however, comparatively little dietary research has focused on fossil great apes from Eurasia –. Previous results suggest that a considerable dietary diversity was present in the Late Miocene, and that such diversification might have taken place during the Middle and Late Miocene .
Previous dental microwear analyses were based on a wide array of extinct hominoids from the Miocene of Western Eurasia –: Griphopithecus alpani ,  from the early Middle Miocene (MN6, ca. 14.9–13.7 Ma)  of Turkey; Hispanopithecus (Rudapithecus) hungaricus ,  from the Late Miocene (MN9, ca. 10.0–9.8 Ma)  of Hungary; Ouranopithecus macedoniensis – from the Late Miocene (MN10, ca. 9.7–9.0 Ma)  of Greece; Oreopithecus bambolii – from the Late Miocene (MN12, ca. 8.3–6.7 Ma)  of Italy; and Hispanopithecus crusafonti (MN9, ca. 10.4–10.0 Ma) and Hispanopithecus laietanus (MN9, ca. 11.1–9.5 Ma)  from Spain . Results based on these taxa – suggested that, from the hard-object feeding plesiomorphic condition displayed by G. alpani , a progressive dietary diversification and specialization would have taken place through time—with Hispanopithecus spp. being inferred as a frugivore , , Ou. macedoniensis as a hard-object specialist , and O. bambolii as an extreme folivore .
These analyses had, however, a significant gap, because late Middle Miocene taxa were not included due to the scarcity of fossil specimens from this time span. This situation, however, drastically changed during the last decade thanks to continued and extensive fieldwork in the late Middle Miocene local stratigraphic series of Abocador de Can Mata in els Hostalets de Pierola (Vallès-Penedès Basin) , , . The material recovered there has shown an unprecedented diversity of Middle Miocene dryopithecines in Western Europe , , with two new genera and species (Pierolapithecus catalaunicus  and Anoiapithecus brevirostris ) being described, and new material of Dryopithecus fontani  being recovered. Similarly, excavations at several Late Miocene localities of the same basin have led to the recovery of new dental remains of Hispanopithecus laietanus, which further confirm the distinction of this species from Hispanopithecus crusafonti, recorded at slightly older localities . Additional paleodietary data are therefore required for these taxa in order to better understand the hominoid radiation in Western Eurasia from a dietary viewpoint.
Here we report new dental microwear analyses for five hominoids from the Iberian Peninsula (Figure 1), ranging in age from 12.3–12.2 to 9.7 Ma , . Together with previous results for other Miocene hominoids from elsewhere in Europe and Turkey – (see Table S1), these data allow us to re-evaluate dietary diversification during great-ape evolution in Western Eurasia (ca. 14 to 7 Ma) in the light of paleoenvironmental changes.
Among the various methods of paleodietary inference in primates, dental gross morphology and ultrastructure are useful because teeth are adapted for food processing . Occlusal morphology, which can be quantified by means of shearing crest analysis , , , offers some clues because folivorous apes possess longer shearing crests on molars than frugivorous ones. However, shearing crest quotients are highly dependent on the particular group being analyzed and the baseline used as a reference for comparison , , so that they might be potentially biased when applied to extinct taxa . Enamel thickness is also generally considered to reflect dietary adaptations to some degree, given the relationship between hard-object feeding and thick enamel , , –. However, enamel thickness is heavily influenced by phylogenetic constraints  and there is no threshold value for distinguishing hard-object feeders on this basis alone , , so that overall there is no direct relationship between enamel thickness and diet. All these morphology-based approaches reflect dietary adaptation as well as phylogenetic constraints, and hence probably are more informative about what extinct taxa were able to eat than about what they actually ate .
Non-morphological methods of paleodietary reconstruction, based on either dental microwear or stable isotope geochemistry, provide more direct information on the properties of the foods consumed independently from adaptation , . Geochemical methods, such as stable carbon isotope ratios derived from fossil tooth enamel, are based on the fact that hominoids that consumed grasses and sedges have higher 13C levels than those that fed on fruits and other plants –. These methods are based on the carbon isotopic distinction between C3 and C4 photosynthetic pathways. However, C4 plants (grasses) did not globally expand until the Late Miocene (ca. 8-6 Ma) , , being present in Eurasia only from 9.4 Ma onwards —i.e., after the extinction of most of the Western Eurasian hominoids studied in this paper. Moreover, isotopic analysis of tooth enamel implies invasive sampling techniques, which are not advisable given the small available dental samples for most of the studied taxa. Dental microwear analysis similarly provides direct evidence on the type of food items consumed by a particular fossil individual, but unlike isotopic methods it is a non-invasive technique, which relies on the microscopic traces left by foods on the enamel surface , , .
Dental microwear analysis is thus one of the most powerful methods for inferring dietary behavior in extinct taxa, being based on the strong and consistent association between dental microscopic patterns and the physical properties of the chewed foods , . While both occlusal morphology and enamel thickness might provide important clues as to what types of food a particular taxon was adapted to consume, microwear features directly reflect what an animal actually ate just prior to death . Hence, since the early 1980s dental microwear analysis has been extensively applied to early hominins and other fossil primates in order to try to determinate their dietary behavior (and seasonal changes thereof), as well as tooth use and masticatory jaw movements . Dental microwear provides direct information on the type of food items consumed shortly prior to an individual's death (days, weeks or months, depending on the nature of the foods being masticated)—a phenomenon referred to as the “Last Supper effect” . The physical properties of both the food items (especially phytoliths from plant taxa) and of exogenous grit (abrasive dirt) being ingested during feeding influence dental microwear patterns. Based on both research in the wild  and experimental studies , , some authors have contended that exogenous grit plays an important (or even a primary) role in dental microwear genesis—which might explain why some species have broadly-similar microwear patterns in spite of marked dietary differences . Further experimental research is undoubtedly necessary to better understand the mechanisms responsible of microwear formation, and particularly to determine the role of exogenous grit as a causative agent. However, various studies support the view that food item properties are the main factor determining microwear genesis –. Thus, work on primates and other mammals has shown a strong relationship between dental microwear features and the types of food consumed, as indicated by different taxa from comparable sites, which exhibit microwear differences that are consistent with their contrasting diets –.
Dental microwear texture analysis – was recently introduced as an alternative technique to more traditional methods of microwear analysis, being based on 3D surface data and scale-sensitive fractal analysis. Unlike the traditional method, texture analysis does not require the identification of individual features and the analysis is automated—thus being less affected by interobserver error and much less time consuming , . Contrary to such advantages, microwear texture analysis is a much more costly alternative, because it relies on white-light scanning confocal microscope instead of 2D micrographs taken with a standard Scanning Electron Microscope (SEM). Texture analysis was introduced to increase repeatability and avoid interobserver error , but error studies of traditional microwear quantification techniques show that high errors are found only when different methodologies are employed . As long as a consistent technique is employed, such as that offered by the Microware software package, a common microwear database derived by different researchers can be consistently employed . In this sense, using the traditional microwear analysis approach offers the advantage that our new results can be analyzed together with those derived by previous researches for both the extant comparative sample and other extinct hominoids. Whereas traditional microwear data are available for some Western Eurasian hominoids , , no microwear texture data have been thus far published for Miocene apes. As a result, the more traditional approach to microwear analysis followed in this work is still currently used by various researchers , , .
Methods and Materials
Micrographs of the occlusal enamel surfaces of the investigated teeth were taken with an environmental SEM (FEI Quanta 200) at the Serveis Cientificotècnics of the Universitat de Barcelona (Spain), on “Phase II” crushing/grinding facets (9, 10n and x) , . The standard procedure described in ref.  was employed, including 500× magnification and 200 dpi micrograph resolution, in secondary emissions mode and a 20 kV voltage. To avoid interobserver error, an area of 0.02 mm2 ,  was analyzed with Microware 4.02© software by a single author (DDM). Some of the examined specimens showed extensive microscopic damage and were therefore discarded.
Two main microwear features (pits and striations) were distinguished , , . Pits are microwear scars that are circular or subcircular in outline. Scratches, in turn, are elongated microfeatures with straight, parallel sides. In this study, pits and scratches were directly categorized by following an arbitrarily-set length to width ratio of 4:1 . The three standard variables customarily quantified in dental microwear analyses were employed , , : (1) Percentage of pits (%), i.e., the proportion of pits relative to the total number of microwear features; (2) breadth of striations (in µm); and (3) breadth of pits (in µm). Previous studies have shown that the relative proportion between pits and scratches enables the distinction between frugivores, folivores and hard-object feeders , , , , , . Thus, although this is a continuous variable across dietary categories, there is a strong and significant positive correlation between the prevalence of pits and the consumption of hard, brittle foods (such as nuts), as well as between higher scratch frequencies and the consumption of tough items (such as leaves and softer fruits). Microwear feature size is also valuable for further characterizing diets, especially when combined with pitting incidence in multivariate analyses . Moreover, striation breadth has been related to the ratio of exogenous grit versus phytoliths consumed in incisors , although this relationship remains to be tested in molar microwear.
We studied 15 upper and lower molars of the following Miocene hominoids (Table 1 and 2): Pierolapithecus catalaunicus from ACM/BCV1 (IPS21350) , Anoiapithecus brevirostris from ACM/C3-Aj (IPS41712 and IPS43000)  and ACM/C1-E* (IPS35027) , Dryopithecus fontani from ACM/C3-Ae (IPS35026) ; Hispanopithecus (Hispanopithecus) crusafonti from CP1 (IPS1820, IPS1818, IPS1812 and IPS1821) and TF (MGSB25314) , ; and Hispanopithecus (Hispanopithecus) laietanus from CF (IPS34753)  and CLL1 (IPS1763, IPS1788, IPS1797 and IPS1800) , , . The taxonomy employed for hominoids follows ref. . All specimens studied in this paper are housed at the Institut Català de Paleontologia Miquel Crusafont (Sabadell, Spain) and the Museu Geològic del Seminari de Barcelona (Barcelona, Spain). No permits were required for the described study. The ACM specimens come from the late Middle Miocene (MN7+8), whereas those from the remaining localities are Late Miocene (MN9) in age , . To fully assess the available information and compensate for the small number of individuals in some cases, specimens of a single species from various localities were also analyzed together by using their average values for microwear variables. In particular, we combined specimens of A. brevirostris from ACM/C1-E* and ACM/C3-Aj, specimens from H. crusafonti from TF and CP1, and specimens of H. laietanus from CF and CLL1. This procedure is justified by the close geographic situation and age of these localities (Table 1, see also Figure 1, and Table S1).
Our results were compared with those derived from previous authors , ,  for a sample of 11 extant anthropoid primates with well-known diets (extant species samples consisting of 10 specimens, except that of Papio cynocephalus, which consists of 16). These studies were selected because they used a sufficiently similar technique to allow comparison with our results. As mentioned above, we analyzed our microwear results together with those previously published for other Western Eurasian Miocene hominoids, including: Griphopithecus alpani from Paşalar (MN6) , ; Hispanopithecus hungaricus from Rudabánya (MN9) , ; Ouranopithecus macedoniensis from Ravin de la Pluie, Xirochori and Nikiti (MN10) ; and Oreopithecus bambolii from Baccinello, Monte Bamboli and Ribolla (MN12) .
Three extant dietary categories were employed by attributing each of the extant species to one of these groups defined a priori on the basis of published behavioral data : (1) folivores (FOL); (2) frugivores/mixed feeders (FMF); and (3) hard-object feeders (HOF). Several species were subsumed into a single category of “frugivores/mixed feeders” , , because periods of fruit scarcity may impel many frugivorous primates to exploit alternative, non-preferred food sources (fallback foods), thereby resulting in a somewhat eclectic foraging strategy . It should be also taken into account that the HOF category not only includes specialized hard-object feeders (Lophocebus albigena and Cebus apella) , , but also orangutans (Pongo pygmaeus), which are less specialized hard-object feeders but are not frugivores in a strict sense. All extant hominoids have a preference for ripe fruit, but the emphasis on leaves, soft fruits and hard food items various among the various species —with orangutans consuming on average harder and unripe fruits more often than other great apes , , especially as fallback foods .
In order to offer insights into the dietary habits of species, hierarchical, complete-linkage (farthest neighbor method) cluster analyses based on Euclidean distances, and discriminant Canonical Variates Analyses (CVA) were used to analyse the extant and fossil data sets. Cluster analysis was intended to explore the similarities in microwear patterns between extant primates and extinct hominoids by using the above-mentioned three microwear variables. CVA, in turn, was intended to evaluate the reliability of these microwear variables for distinguishing between the various dietary categories defined for extant taxa, as well as to classify fossils to these categories. Extant taxa were thus included a priori in one of the three dietary categories described above, whereas the extinct hominoids were left unclassified and classified a posteriory on the basis of the classification probabilities derived by the analysis from Mahalanobis squared distances to extant group centroids. All statistical analyses were performed using the SPSS v. 11 statistical package.
Like every paleobiological approach, dental microwear analysis has its particular drawbacks and limitations. When data derived from different researchers are combined into a single analysis, interobserver error in microwear features is a major concern that can complicate the interpretation of the results , . This caveat applies to this study and should be borne in mind when interpreting our results. However, it is worth mentioning that several methodological precautions were adopted by us to minimize the error introduced. Thus, all the employed data were obtained through SEM imaging, which is less prone to error bias than other techniques such as light microscopy . Moreover, the data used are based on procedures that, although not identical, are highly comparable because: (1) they were obtained using the same quantitative SEM-based technique; (2) microwear features were analyzed with a semiautomated image analysis procedures (primarily Microware 4.0), which results in lesser error rates —with the exception of data taken from ref. , which employed traditional digitizer-based measurements; and (3) all the procedures employed followed standard methodological details, i.e., same wear facets selected for analysis, same instrumental settings (voltage, magnification and specimen detector), same micrograph resolution and analyzed surface, same measured microwear variables, etc. Finally, all the data measured in this analysis or taken from the literature were derived by experienced and highly trained microwear researchers, which diminishes the magnitude of error in microwear measurements , . Although the use of these methodological precautions cannot fully remove the error bias, they provide a reasonable degree of interobserver consistency, thereby ensuring the comparability of the data employed.
Among the three analyzed variables (Table 1 and 2, and Figure 2 and S1), pitting incidence best distinguishes among dietary categories , , whereas microwear feature (especially striation) breadth allows to further refine paleodietary inferences . With regard to pitting incidence, only Pierolapithecus catalaunicus and Dryopithecus fontani (represented by a single individual each) resemble extant HOF such as Pongo pygmaeus and Lophocebus albigena, which habitually consume hard and brittle items. Most of the remaining taxa are somewhat intermediate between P. pygmaeus and extant FMF such as Pan troglodytes and Papio cynocephalus. Although some differences between taxa/localities must partly reflect interindividual variation (Table 1 and 2, and Figure S1), the pitting incidences of all the hominoids from Spain suggest some degree of sclerocarpy. This is most clear in P. catalaunicus, which further displays wider striations—consistent with a preference for hard foods —than in other extinct taxa, in the range of extant HOF and most closely resembling L. albigena (Figure 2 A). The remaining taxa (including Hispanopithecus crusafonti and Hispanopithecus laietanus) are intermediate between extant HOF and FMF when both pitting incidence and striation breadth are considered simultaneously (Figure 2 A). In contrast, none of the taxa overlaps with extant FOL for any of the studied variables.
(A) Striation breadth and (B) pit breadth vs. pitting incidence based on species/locality means (Table 1). Fossil taxa abbreviations: Ab, Anoiapithecus brevirostris; Df, Dryopithecus fontani; Ga, Griphopithecus alpani; Hc, Hispanopithecus crusafonti; Hh, Hispanopithecus hungaricus; Hl, Hispanopithecus laietanus; Ob, Oreopithecus bambolii; Om, Ouranopithecus macedoniensis; Pc, Pierolapithecus catalaunicus. Different symbols are employed to distinguish each species. For species from multiple localities, only average values are shown (see individual values in Figure S1). The results derived in this study are depicted in red, whereas those taken from previous studies are shown in yellow. The polygons showing the variability of extant dietary categories are depicted in blue (folivores), green (mixed feeders/frugivores) and magenta (hard-object feeders).
Compared with other hominoids from Western Eurasia (Figure 2, Figure S1), only Griphopithecus alpani and Ouranopithecus macedoniensis surpass the pitting incidences of the hominoids from the Iberian Peninsula (and even that of extant HOF in some instances). The former, however, display much narrower microwear features than extant HOF and P. catalaunicus, thus overlapping with the remaining studied taxa (Figure 2 A, B). Hispanopithecus hungaricus overlaps to a large extent with other species of Hispanopithecus in the various microwear variables, thus being rather intermediate between FMF and HOF, whereas Oreopithecus bambolii uniquely falls within the range of extant FMF for most individuals.
A cluster analysis based on microwear fabrics (Figure 3) yields two main clusters separating FOL and FMF (cluster A) from HOF (cluster B). Among extinct hominoids, the average values of A. brevirostris and H. laietanus are grouped with the mixed feeder P. cynocephalus and the soft-fruit eater P. troglodytes in subcluster A1. The average of O. bambolii is in turn included in subcluster A2, together with the remaining extant frugivores and all FOL, which are characterized by lower pitting incidences. The remaining fossil hominoids clump together with HOF in cluster B, displaying higher pit percentages. Average values of P. catalaunicus, D. fontani, H. crusafonti and H. hungaricus are grouped with P. pygmaeus and C. apella in subcluster B1, whereas G. alpani and Ou. macedoniensis cluster with L. albigena in subcluster B2 (see Figure S3 for individual variation). Overall, the analyses indicate a hard-object feeding component for many of the fossil hominoids, with the exception of A. brevirostris, H. laietanus and O. bambolii, which show greater affinities with FMF. None of the taxa clusters with extant FOL.
The CVA (Figure 4 and Table 3; see also Table S2) confirms that the investigated variables provide a satisfactory dietary discrimination (100% of extant taxa correctly classified, 64% in cross-validation). CV1 separates HOF (positive values) from FMF and FOL (negative values) mostly on the basis of pitting incidence, whereas CV2, more influenced by scratch and pit breadths, does not enable a clear distinction among dietary categories. The discriminant analysis (Table S3) based on the CVA classifies most of the taxa as HOF, except the average values of A. brevirostris, H. laietanus and O. bambolii, which are classified as FMF (Figure 4 A). When individual classifications for extinct taxa are analyzed, A. brevirostris, H. laietanus and H. crusafonti display some variation in individual classifications between HOF and FMF, whereas several individuals of O. bambolii are classified as FOL or HOF instead of FMF (Figure 4 B, Tables 4 and S4). This fact reflects dietary diversity in some of the taxa, which indicates that caution is required when interpreting species (P. catalaunicus and D. fontani) represented by a single individual. However, based on classification probabilities (Table S4), P. catalaunicus falls within the variation of extant HOF, unlike D. fontani, G. alpani and Ou. macedoniensis (p<0.05). Anoiapithecus brevirostris and most individuals of O. bambolii similarly fit well with extant FMF. In contrast, the classification of Hispanopithecus species as either HOF or FMF is not consistent among individuals and not well supported for most of them, suggesting that they were truly intermediate between these categories.
(A) Results based on mean/species locality data and (B) on individuals. Colored ellipses denote the morphospace defined by each extant group, black symbols extant taxa (group centroids by larger symbols). Symbols and colors in a as in Figure 2, whereas in B symbols and colors are different to show variability within fossil species.
Miocene Hard-Object Feeders
Only the single individual of P. catalaunicus fits well with extant HOF, as shown by its high pitting incidence and broad scratches, thus resembling L. albigena and, especially, P. pygmaeus. The latter resemble other extant apes in preferring ripe fruits , but display thicker enamel as an adaptation to consume harder or unripe fruits, especially as fallback foods . L. albigena is also a thick-enameled HOF that consumes fleshy fruits but seasonally forages on hard, brittle objects such as nuts and seeds , . Although the small sample size precludes a definitive conclusion, our results are consistent with P. catalaunicus being a HOF, as previously suggested based on its relatively thick enamel  and further confirmed by our multivariate analyses.
Our results also confirm previous inferences, based on pitting incidence, that Ou. macedoniensis was a hard-object specialist ,  and that G. alpani consumed hard fruits at least as often as orangutans , . These taxa are very similar in microwear features to one another, but differ from P. catalaunicus and extant HOF by displaying narrower microwear features. This condition of P. catalaunicus is more consistent with being a HOF, which compared to FMF and FOL have wider microwear striations (due to higher occlusal forces)  as well as larger pits (due to the higher amount of grit routinely ingested by these taxa) , –. Differences in microwear feature size among extinct HOF might reflect their divergent habitats and ecological niches. Thus, the orthograde bodyplan with adaptations for vertical climbing and above-branch palmigrady of P. catalaunicus , , ,  suggests a strong arboreal commitment, as in orangutans and the other extant HOF (L. albigena and C. apella) , . In contrast, the postcranials of G. alpani suggest a pronograde bodyplan more suitable for semi-terrestrial quadrupedalism , , . Similarly, the relatively large body mass  and open, pure C3 environments inferred for Ou. macedoniensis based on the associated fauna ,  also agree with a semi-terrestrial locomotion. Microwear differences between P. catalaunicus and other extinct HOF might be thus attributable to differences in the mechanical properties of the food items found in the canopy as opposed to closer to the ground , , in agreement with previous microwear inferences of a diet primarily based on hard, abrasive items (roots, tubers and/or grasses) for Ou. macedoniensis . Alternatively, microwear differences among these taxa might be related to differences in the content of exogenous grit versus phytoliths in the foods consumed, as previously shown for incisor microwear . Abrasive dust particles are more abundant but smaller on average in dry compared to humid environments , suggesting that the higher pitting incidences and lower striation breadths of G. alpani and Ou. macedoniensis might merely reflect their more open and drier habitats compared to both P. catalaunicus and extant HOF. Thus, these former taxa might have been predominantly (semi-)terrestrial hard-object feeders, whereas P. catalaunicus is best interpreted as an arboreal hard-fruit forager.
Miocene Soft-Fruit Eaters
Among the taxa analyzed, only O. bambolii is best interpreted as a soft frugivore, thus contradicting previous interpretations of a specialized folivorous diet , . Both pitting percentage and striation breadth suggest some dietary diversity (a few individuals show closer microwear resemblances to either FOL and HOF), as further confirmed by the multivariate analyses. Cebus nigrivittatus—a mainly frugivorous primate that further consumes a significant proportion of leaves —might be a good analogue of O. bambolii, as shown by their almost identical pitting percentages (16.20% and 16.96%). However, the wide range of pitting incidence displayed by O. bambolii does point towards a high dietary flexibility, sporadically including leaves and hard fruits alike, instead of specialized folivory. Although the marked development of molar shearing crests in this taxon was interpreted as a folivorous specialization , its pronounced dental relief (with multiple accessory cusps, crests and cingula) more closely resembles that of omnivorous suoids rather than folivores , , in agreement with our microwear results and its moderately thick enamel . O. bambolii is thus best interpreted as an eclectic FMF, more clearly relying on soft fruits than other hominoids from Western Eurasia, but further exploiting other resources, possibly due to the trophic restrictions characteristic of insular environments , .
Miocene Mixed Soft/Hard-Fruit Feeders
The remaining hominoids from Western Eurasia do not comfortably fall into any of the extant dietary categories, being somewhat intermediate between FMF and HOF. On average, A. brevirostris and H. laietanus are classified as FMF, whereas D. fontani, H. crusafonti and H. hungaricus display closer affinities with HOF. Individual values, however, are classified as both FMF and HOF, except for the two individuals of H. hungaricus and the single specimen of D. fontani. The restricted samples for the latter taxa do not enable to ascertain whether they significantly differed from H. laietanus and/or H. crusafonti. However, when pitting incidence and striation breadth are considered simultaneously, most of the analyzed individuals are intermediate between extant FMF and HOF, not overlapping with other extinct hominoids here interpreted as HOF. Our analyses therefore suggest that the diet of these taxa might have been intermediate between FMF and HOF (by including both soft and hard fruits to a large proportion), thus lacking an appropriate analog among the comparative sample. Such interpretation differs from previous inferences, based on microwear and shearing crest analyses –, of a mainly frugivorous diet for Hispanopithecus species, and clearly discounts a folivorous diet for H. laietanus based on buccal microwear .
In these taxa, emphasis on hard-object feeding might have varied depending on the species and/or fluctuated depending on environments. Available samples are too small to adequately test whether hard-food items were consumed as fallback foods, depending on seasonal factors influencing resource availability , or whether these species displayed an eclectic foraging strategy on a regular, non-seasonal basis. For species of Hispanopithecus, paleoenvironmental reconstructions tend to favor the former hypothesis, since these taxa inhabited humid and subtropical to warm-temperate environments , , , . Such environments would have provided soft fruits at least during part of the year. However, the linear enamel hypoplasias frequently displayed by species of Hispanopithecus ,  indicate repeated episodes of malnutrition due to seasonal fluctuations in resource abundance (due to fruiting cycles) , , , thus suggesting that they might have consumed hard-food items as fallback foods during the unfavorable season. Whereas postcranial remains are unknown for A. brevirostris and very restricted for D. fontani , the more complete postcranial remains of H. laietanus and H. hungaricus clearly evidence a high arboreal commitment and more derived suspensory adaptations than in P. catalaunicus , , , , –. Species of Hispanopithecus are thus best interpreted as arboreal feeders, with their enhanced suspensory capabilities enabling a more efficient foraging on terminal branches , .
Although hominoids are first recorded in Eurasia ca. 17 Ma, coinciding with the beginning of the Miocene Climatic Optimum , , , additional hominoid dispersal events between Africa and Europe probably took place afterwards , , . Kenyapithecines ,  extended their range into Eurasia before 14 Ma—G. alpani and Kenyapithecus kizili , —and apparently gave rise to the Eurasian hominoid radiation , , . Besides their likely semi-terrestrial locomotion , the dispersal of kenyapithecines was apparently facilitated by their HOF adaptations , , , enabling them to occupy subtropical and highly seasonal, single-canopied woodland/forest with abundant ground vegetation and more open areas . This agrees with our results, suggesting that G. alpani mainly relied on hard food items. Available evidence suggests that kenyapithecines rapidly spread throughout Eurasia and vicariantly diversified into different clades , , with pongines being recorded in Asia and dryopithecines in the Iberian Peninsula by ca. 12.5 Ma .
The European dryopithecines are alternatively interpreted as stem hominids , , hominines , , or the sister-taxon of Asian pongines , . Between 12.5 and 7 Ma, and despite a climatic trend towards cooling and increased seasonality , , they experienced an adaptive radiation from both taxonomic and ecological viewpoints , . This radiation, including the acquisition of new locomotor and dietary adaptations, was probably related to the new selection pressures posed by the different biotopes present in Europe during the Middle and Late Miocene, coupled with regional paleoenvironmental differences and changes through time , . Both the habitat and diet of G. alpani from Turkey most closely resemble those of their Middle Miocene relatives from Africa , , . In contrast, the habitats encountered by subsequent hominoids in both NE Spain and Central Europe were more humid, less seasonal, and more densely-forested –. Our results suggest that P. catalaunicus retained the ancestral HOF strategy while specializing for arboreal foraging. In contrast, D. fontani and A. brevirostris apparently displayed a somewhat more frugivorous diet (albeit with some sclerocarpic component), which might be interpreted as an early adaptive response to the new environmental conditions. Competitive exclusion coupled with increased environmental heterogeneity of the plant communities—which favors increased paleobiodiversity by multiplying the number of available ecological niches —would have played a role in the dietary diversification of dryopithecines.
The dietary diversification of hominoids in Western Eurasia was further accentuated during the Late Miocene—as shown by the mixed soft-hard frugivorous condition of Hispanopithecus, the more frugivorous but versatile diet of O. bambolii, and the specialized hard-object feeding of Ou. macedoniensis. The adaptive trend towards increased soft frugivory in Hispanopithecus is at odds with concomitant climatic changes toward increased seasonality and lower temperatures. These environmental changes prompted the substitution of evergreen by deciduous trees  as well as the fragmentation of habitats suitable for frugivorous hominoids . For some time, Hispanopithecus overcame such a paleoenvironmental deterioration thanks to new locomotor adaptations—presumably enabling a more efficient foraging on the canopy , —instead of exploiting a greater proportion of leafy material and/or foraging on the ground.
The extinction of hominoids in Europe was ultimately related to an increase in environmental uniformity and the resulting loss of suitable habitats . In Western and Central Europe, it has been related to the substitution of (sub)tropical plants by deciduous trees . At least in the Vallès-Penedès, however, this process was gradual, implying the generation of mosaic environments in which (sub)tropical elements became progressively restricted to lowland humid areas , . Hispanopithecus probably had to seasonally recourse to hard food items as fallback foods, until the reduction of its preferred habitat ultimately caused its extinction in Spain and elsewhere in Europe , , .
In Eastern Europe, Ou. macedoniensis survived longer than Hispanopithecus (ca. 8.0-7.5 vs. 9.5 Ma), probably thanks to a specialized terrestrial HOF diet adapted to open and arid habitats with a predominantly herbaceous vegetation with abundant C3 grasses, bushes and herbs . Although its extinction did not coincide with any major climatic shift, it was similarly related to strong seasonal variations . The paleoenvironmental changes leading to the extinction of Ou. macedoniensis were apparently opposite to those experienced by Hispanopithecus, since in Eastern Europe bushy vegetation expanded over areas previously occupied by grasslands , whereas in Western and Central Europe it was rather accompanied by the substitution of (sub)tropical plants by deciduous trees .
O. bambolii survived much longer in the Tusco-Sardinian insular ecosystems by displaying a more frugivorous but highly versatile diet, allowing it to opportunistically exploit more fibrous plant materials and harder fruits alike. Its extinction does not offer much insight with regard to that of other apes from mainland Europe, since it is not related to any environmental change , but rather to the connection of its insular habitat to the mainland ca. 7 Ma—and the substitution of the endemic associated fauna , .
Contrary to previous interpretations, our microwear analyses show that leaves and stems were not a primary dietary component for any hominoid from Western Eurasia, which are interpreted instead as frugivores (O. bambolii) and/or hard-object feeders (e.g., P. catalaunicus). Whereas some of the studied taxa fall comfortably within these two dietary categories, many of them (such as Hispanopithecus species) seem to be intermediate, suggesting that they have no extant dietary analog in the comparative sample.
From a evolutionary perspective, our results indicate that hominoids from Western Eurasia experienced a progressive dietary diversification between 14 and 7 Ma, from the presumably ancestral condition of (semi-)terrestrial hard-object feeding shown by G. alpani. In Western and Central Europe, this diversification might have been triggered by changes in habitat structure (more densely-forested environments), coupled with competitive exclusion and new locomotor adaptations related to arboreal feeding (as shown by P. catalaunicus). Other taxa from this area (especially the species of Hispanopithecus) apparently combined soft and hard fruits in their diets. The high behavioral plasticity of extant great apes allows them to survive in front of a marked environmental instability (resulting in spatial/temporal uncertainty of preferred fruit resources) , . Similarly, the suspensory adaptations of Hispanopithecus species (enabling a more efficient foraging on terminal branches), coupled with the exploitation of harder food items during the unfavorable season, might have allowed them to temporarily overcome the progressive environmental deterioration. Ultimately, however, the restriction and fragmentation of their preferred habitats would have led to their extinction from Western and Central Europe. In contrast, Ou. macedoniensis survived longer in the more open and arid landscapes of Eastern Europe by displaying a more terrestrial trophic niche based on hard food items, whereas O. bambolii persisted even longer in the Tusco-Sardinian Paleobioprovince by displaying a versatile frugivorous diet, until its insular ecosystem was connected to the mainland.
The failure by any of these taxa to adapt to folivory in the face of environmental changes towards increased seasonality might be attributable to their specialized (although diverging) trophic niches. The contrasting environmental changes experienced by the respective habitats of Hispanopithecus (more deciduous and open forests) and Ou. macedoniensis (less open and more bushy habitats), coupled with their strikingly divergent trophic niches, suggest that great-ape vulnerability to environmental change is not attributable to a frugivorous bias per se , but rather to the adaptation to whatever hyperspecialized trophic niche.
Bivariate plots of microwear feature breadth vs. pitting incidence. (A) Striation breadth and (B) pit breadth vs. pitting incidence based on individual values reported in Table 2. See Figure 2 for the equivalent plots based on mean species/locality values reported in Table 1. Abbreviations as in Figure 2 (note that symbols and colors are different to show variability within fossil species).
Results of the cluster analysis based on dental microwear features for individual values. Note that symbols and colors are different to those of Figure 2 to show variability within fossil species. See Figure 3 for the results based on mean species/locality data.
Sample sizes for the studied extinct species.
Results of the CVA based on microwear features.
Scores for the two canonical variates in extant and extinct taxa derived by the CVA.
Individual results of the discriminant analysis based on the CVA.
We thank Isaac Casanovas-Vilar for the map of Figure 1, and Sebastià Calzada for the loan of the TF specimen.
Conceived and designed the experiments: DDM DMA SMS. Performed the experiments: DDM. Analyzed the data: DDM DMA. Contributed to the writing of the manuscript: DDM DMA. Generated the figures: DDM.
- 1. Harrison T (2010) Dendropithecoidea, Proconsuloidea and Hominoidea (Catarrhini, Primates). In: Werdelin L, Sanders WJ, editors. Cenozoic mammals of Africa. Berkeley, University of California Press. pp. 429–469.
- 2. Andrews P, Kelley J (2007) Middle Miocene dispersals of apes. Folia Primatol 78: 328–343.
- 3. Casanovas-Vilar I, Alba DM, Garcés M, Robles JM, Moyà-Solà S (2011) Updated chronology for the Miocene hominoid radiation in Western Eurasia. Proc Natl Acad Sci USA 108: 5554–5559.
- 4. Alba DM (2012) Fossil apes from the Vallès-Penedès Basin. Evol Anthropol 21: 254–269.
- 5. Begun DR (2002) European hominoids. In: Hartwig WC, editor. The primate fossil record. Cambridge, Cambridge University Press. pp. 339–368.
- 6. Begun DR, Nargolwalla MC, Kordos L (2012) European Miocene hominids and the origin of the African ape and human clade. Evol Anthropol 21: 10–23.
- 7. Andrews P, Martin L (1991) Hominoid dietary evolution. Phil Trans R Soc B 334: 199–209.
- 8. Alba DM, Fortuny J, Moyà-Solà S (2010) Enamel thickness in Middle Miocene great apes Anoiapithecus, Pierolapithecus and Dryopithecus. Proc R Soc B 277: 2237–2245.
- 9. Ungar PS, Kay RF (1995) The dietary adaptations of European Miocene catarrhines. Proc Natl Acad Sci USA 92: 5479–5481.
- 10. Ungar PS (1996) Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J Hum Evol 31: 335–366.
- 11. Ungar PS (2005) Dental evidence for the diets of fossil primates from Rudabánya northeastern Hungary with comments on extant primate analogs and “noncompetitive” sympatry. Palaeontograph Ital 90: 97–111.
- 12. King T, Aiello LC, Andrews P (1999) Dental microwear of Griphopithecus alpani. J Hum Evol 36: 3–31.
- 13. King T (2001) Dental microwear and diet in Eurasian Miocene catarrhines. In: de Bonis L, Koufos GD, Andrews P, editors. Hominoid Evolution and Climatic Change in Europe, Vol. 2. Phylogeny of the Neogene Hominoid Primates of Eurasia. Cambridge, Cambridge University Press pp. 102–117.
- 14. Merceron G, Blondel C, de Bonis L, Koufos GD, Viriot L (2005) A new method of dental microwear analysis: Application to extant primates and Ouranopithecus macedoniensis (Late Miocene of Greece). Palaios 20: 551–561.
- 15. Teaford MF, Walker A (1984) Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus. Am J Phys Anthropol 64: 191–200.
- 16. Alpagut B, Andrews P, Martin L (1990) New hominoid specimens from the Middle Miocene site at Pasalar, Turkey. J Hum Evol 19: 397–422.
- 17. Kelley J, Andrews P, Alpagut B (2008) A new hominoid species from the middle Miocene site of Paşalar, Turkey. J Hum Evol 54: 455–479.
- 18. Begun DR, Kordos L (1993) Revision of Dryopithecus brancoi Schlosser, 1901, based on the fossil hominoid material from Rudábanya. J Hum Evol 25: 271–285.
- 19. Kordos L, Begun DR (2001) Primates from Rudabánya: allocation of specimens to individuals, sex and age categories. J Hum Evol 40: 17–39.
- 20. de Bonis L, Koufos GD (1993) The face and the mandible of Ouranopithecus macedoniensis: description of new specimens and comparisons. J Hum Evol 24: 469–491.
- 21. de Bonis L, Koufos GD (1994) Our ancestors' ancestor: Ouranopithecus is a Greek link in human ancestry. Evol Anthropol 3: 75–83.
- 22. de Bonis L, Koufos GD (1997) The phylogenetic and functional implications of Ouranopithecus macedoniensis. In: Begun DR, Ward CV, Rose MD, editors. Function, phylogeny and fossils: Miocene hominoid evolution and adaptation. New York: Plenum Press. pp. 317–326.
- 23. Rook L, Harrison T, Engesser B (1996) The taxonomic status and biochronological implications of new finds of Oreopithecus from Baccinello (Tuscany, Italy). J Hum Evol 30: 3–27.
- 24. Harrison T, Rook L (1997) Enigmatic anthropoid or misunderstood ape? The phylogenetic status of Oreopithecus bambolii reconsidered. In: Begun DR, Ward CV, Rose MD, editors. Function, phylogeny and fossils: Miocene hominoid evolution and adaptation. New York: Plenum Press. pp. 327–362.
- 25. Moyà-Solà S, Köhler M (1997) The phylogenetic relationships of Oreopithecus bambolii Gervais, 1872. C R Acad Sci Paris (IIa) 324: 141–148.
- 26. Rook L, Oms O, Benvenuti M, Papini M (2011) Magnetostratigraphy of the Late Miocene Baccinello–Cinigiano basin (Tuscany, Italy) and the age of Oreopithecus bambolii faunal assemblages. Palaeogeogr Palaeoclimatol Palaeoecol 305: 286–294.
- 27. Alba DM, Moyà-Solà S, Casanovas-Vilar S, Galindo J, Robles JM, et al. (2006) Los vertebrados fósiles del Abocador de Can Mata (els Hostalets de Pierola, l’Anoia, Cataluña), una sucesión de localidades del Aragoniense superior (MN6 y MN7+8) de la cuenca del Vallès-Penedès. Campañas 2002-2003, 2004 y 2005. Est Geol 62: 295–312.
- 28. Alba DM, Casanovas-Vilar I, Robles JM, Moyà-Solà S (2011) Parada 3. El Aragoniense superior y la transición con el Vallesiense: Can Mata y la exposición paleontological de els Hostalets de Pierola. Paleontol Evol Mem. esp 6: 95–109.
- 29. Moyà-Solà S, Köhler M, Alba DM, Casanovas-Vilar I, Galindo J (2004) Pierolapithecus catalaunicus, a new Middle Miocene great ape from Spain. Science 306: 1339–1344.
- 30. Moyà-Solà S, Alba DM, Almécija S, Casanovas-Vilar I, Köhler M, et al. (2009) A unique Middle Miocene European hominoid and the origins of the great ape and human clade. Proc Natl Acad Sci USA 106: 9601–9606.
- 31. Moyà-Solà S, Köhler M, Alba DM, Casanovas-Vilar I, Galindo J, et al. (2009) First partial face and upper dentition of the Middle Miocene hominoid Dryopithecus fontani from Abocador de Can Mata (Vallès-Penedès Basin, Catalonia, NE Spain): Taxonomic and phylogenetic implications. Am J Phys Anthropol 139: 126–145.
- 32. Ungar PS (1992) Dental evidence for diet in primates. Anthrop Közl 34: 141–155.
- 33. Kay RF, Ungar PS (1997) Dental evidence for diet in some Miocene catarrhines with comments on the effects of phylogeny on the interpretation of adaptation. In: Begun DR, Ward CV, Rose MD, editors. Function, phylogeny and fossils: Miocene hominoid evolution and adaptation. New York: Plenum Press. pp. 131–151.
- 34. DeMiguel D, Alba DM, Moyà-Solà S (2013) European pliopithecid diets revised in the light of dental microwear in Pliopithecus canmatensis and Barberapithecus huerzeleri. Am J Phys Anthropol 151: 573–582.
- 35. Schwartz GT (2000) Taxonomic and functional aspects of the patterning of enamel thickness distribution in extant large-bodied hominoids. Am J Phys Anthropol 111: 221–244.
- 36. Lucas P, Constantino P, Wood B, Lawn B (2008) Dental enamel as a dietary indicator. BioEssays 30: 374–385.
- 37. Vogel ER, van Woerden JT, Lucas PW, Utami Atmoko SS, van Schaik CP, et al. 2008 Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J Hum Evol 55: 60–74.
- 38. Olejniczak AJ, Tafforeau P, Feeney RNM, Martin LB (2008) Three-dimensional primate molar enamel thickness. J Hum Evol 54: 187–195.
- 39. Dumont ER (1995) Enamel thickness and dietary adaptation among extant primates and chiropterans. J Mammal 76: 1127–1136.
- 40. Maas MC, Dumont ER (1999) Built to last: the structure, function, and evolution of primate dental enamel. Evol Anthropol 8: 133–152.
- 41. Grine FE, Sponheimer M, Ungar PS, Lee-Thorp J, Teaford MF (2012) Dental microwear and stable isotopes inform the paleoecology of extinct hominins. Am J Phys Anthropol 148: 285–317.
- 42. Ungar PS, Sponheimer M (2013) Hominin diets. In: Begun DR, editor. A companion to paleoanthropology. Chichester, Blackwell Publishing. pp. 165–182.
- 43. Sponheimer M, Lee-Thorp JA (2007) Hominin paleodiets: the contribution of stable isotopes. In: Henke W, Tattersall I, editors. Handbook of Paleoanthropology. Heidelberg, Springer Verlag. pp. 555–586.
- 44. Lee-Thorp J, Sponheimer M (2006) Contributions of biogeochemistry to understanding hominin dietary ecology. Yrbk Phys Anthropol 49: 131–148.
- 45. Lee-Thorp J, Sponheimer M, Passey BH, de Ruiter DJ, Cerling TE (2010) Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene. Phil Trans Roy Soc B 365: 3389–3396.
- 46. Sponheimer M, et al. 2013 Isotopic evidence of early hominin diets. Proc Natl Acad Sci USA 110: 10513–10518.
- 47. Cerling TE, Wang Y, Quade J (1993) Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361: 344–345.
- 48. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, et al. 1997 Global vegetation change through the Miocene/Pliocene boundary. Nature 389: 153–158.
- 49. Morgan ME, Kingston JD, Marino BD (1994) Carbon isotope evidence for the emergence of C4 plants in the Neogene from Pakistan and Kenya. Nature 367: 162–165.
- 50. Teaford MF (1988) A review of dental microwear and diet in modern mammals. Scanning Microsc 2: 1149–1166.
- 51. Ungar PS, Grine FE, Teaford MF (2008) Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS ONE 3: e2044.
- 52. Grine FE (1986) Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15: 783–822.
- 53. Daegling DJ, Grine FE (1999) Terrestrial foraging and dental microwear in Papio ursinus. Primates 40: 559–572.
- 54. Teaford MF, Lytle JD (1996) Diet-induced changes in rates of human tooth microwear: a case study involving stone-ground maize. Am J Phys Anthropol 100: 143–147.
- 55. Lucas PW, Omar R, Al-Fadhalah K, Almusallam AS, Henry AG, et al. (2013) Mechanisms and causes of wear in tooth enamel: implications for hominin diets. J R Soc Interface 10: 20120923.
- 56. Strait DS, Weber GW, Constantino P, Lucas PW, Richmond BG, et al. (2012) Microwear, mechanics and the feeding adaptations of Australopithecus africanus. J Hum Evol 62: 165–168.
- 57. Lucas PW, Teaford MF (1995) Significance of silica in leaves eaten by long-tailed macaques (Macaca fascicularis). Folia Primatol 64: 30–36.
- 58. Gügel IL, Gruppe G, Kunzelmann KH (2001) Simulation of dental microwear: characteristic traces by opal phytoliths give clues to ancient human dietary behavior. Am J Phys Anthropol 114: 124–138.
- 59. Merceron G, Schulz E, Kordos L, Kaiser TM (2007) Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: evidence from dental meso- and micro-wear analyses of large vegetarian mammals. J Hum Evol 53: 331–349.
- 60. Teaford MF (1985) Molar microwear and diet in the genus Cebus. Am J Phys Anthropol 66: 363–370.
- 61. Ungar PS, Grine FE, Teaford MF, El Zaatari S (2006) Dental microwear and diets of African early Homo. J Hum Evol 50: 78–95.
- 62. Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, et al. (2005) Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436: 693–695.
- 63. Scott RS, Teaford MF, Ungar PS (2012) Dental microwear texture and anthropoid diets. Am J Phys Anthropol 147: 551–579.
- 64. Ungar PS, Krueger KL, Blumenschine RJ, Njau JK, Scott RS (2012) Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. J Hum Evol 63: 429–437.
- 65. Merceron G, Scott J, Scott RS, Geraads D, Spassov N, et al. (2009) Folivory or fruit/seed predation for Mesopithecus, an earliest colobine from the late Miocene of Eurasia? J Hum Evol 57: 732–738.
- 66. Grine FE, Ungar PS, Teaford MF (2002) Error rates in dental microwear quantification using scanning electron microscopy. Scanning 24: 144–153.
- 67. Merceron G, Koufos GD, Valentin X (2009) Feeding habits of the first European colobine, Mesopithecus (Mammalia, Primates): evidence from a comparative dental microwear analysis with modern cercopithecids. Geodiv 31: 865–878.
- 68. Merceron G, Tafforeau P, Marivaux L (2010) Dietary reconstruction of the Amphipithecidae (Primates, Anthropoidea) from the Paleogene of South Asia and paleoecological implications. J Hum Evol 59: 96–108.
- 69. Kay RF (1977) The evolution of molar occlusion in the Cercopithecidae and Early Catarrhines. Am J Phys Anthropol 46: 327–352.
- 70. Grine FE, Ungar PS, Teaford MF, El-Zaatari S (2006) Molar microwear in Praeanthropus afarensis: Evidence for dietary stasis through time and under diverse palaeoecological conditions. J Hum Evol 51: 297–319.
- 71. El-Zaatari S, Grine FE, Teaford MF, Smith AH (2005) Molar microwear and dietary reconstructions of fossil Cercopithecoidea from the Plio-Pleistocene deposits of South Africa. J Hum Evol 49: 180–205.
- 72. Teaford MF (1985) Molar microwear and diet in the genus Cebus. Am J Phys Anthropol 66: 363–370.
- 73. Ungar PS (1994) Incisor microwear of Sumatran anthropoid primates. Am J Phys Anthropol 94: 339–363.
- 74. Alba DM, Fortuny J, Perez de los Ríos M, Zanolli C, Almécija S, et al. (2013) New dental remains of Anoiapithecus and the first appearance datum of hominoids in the Iberian Peninsula. J Hum Evol 65: 573–584.
- 75. Begun DR (1992) Dryopithecus crusafonti sp. nov., a new Miocene hominoid species from Can Ponsic (Northeastern Spain). Am J Phys Anthropol 87: 291–309.
- 76. Golpe Posse JM (1993) Los Hispanopitecos (Primates, Pongidae) de los yacimientos del Vallès-Penedès (Cataluña, España). II: Descripción del material existente en el Instituto de Paleontología de Sabadell. Paleontol Evol 26–27: 151–224.
- 77. Alba DM, Almécija S, Casanovas-Vilar I, Méndez JM, Moyà-Solà S (2012) A partial skeleton of Hispanopithecus laietanus from Can Feu and the mosaic evolution of crown-hominoid positional behaviors. PLoS ONE 7: e39617.
- 78. Begun DR, Moyá-Sola S, Köhler M (1990) New Miocene hominoid specimens from Can Llobateres (Vallès Penedès, Spain) and their geological and paleoecological context. J Hum Evol 19: 255–268.
- 79. Alba DM, Casanovas-Vilar I, Almécija S, Robles JM, Arias-Martorell J, et al. (2012) New dental remains of Hispanopithecus laietanus (Primates: Hominidae) from Can Llobateres 1 and the taxonomy of Late Miocene hominoids from the Vallès-Penedès Basin (NE Iberian Peninsula). J Hum Evol 63: 231–246.
- 80. Teaford MF, Maas MC, Simons EL (1996) Dental microwear and microstructure in Early Oligocene Primates from the Fayum, Egypt: Implications for diet. Am J Phys Anthropol 101: 527–543.
- 81. McGraw WS, Pampush JD, Daegling DJ (2012) Brief communication: Enamel thickness and durophagy in mangabeys revisited. Am J Phys Anthropol 147: 326–333.
- 82. Mihlbachler MC, Beatty BL, Caldera-Siu A, Chan D, Lee R (2012) Error rates in dental microwear analysis using light microscopy. Palaeontol Electron 15: 22p.
- 83. Scott R, Schubert B, Grine FE, Teaford MF (2008) Low magnification microwear: Questions of precision and repeatability. J Hum Evol 28: 139A.
- 84. Purnell MA, Hart PJB, Baines DC, Bell MA (2006) Quantitative analysis of dental microwear in threespine stickleback: a new approach to analysis of trophic ecology in aquatic vertebrates. J Anim Ecol 75: 967–977.
- 85. Poulsen JR, Clark CJ, Smith TB (2001) Seasonal variation in the feeding ecology of the grey-cheeked mangabey (Lophocebus albigena) in Cameroon. Am J Primatol 54: 91–105.
- 86. Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL (2004) Hardness of cercopithecine foods: Implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125: 363–368.
- 87. Teaford MF, Oyen OJ (1989) Differences in the rate of molar wear between monkeys raised on different diets. J Dental Res 68: 1513–1518.
- 88. Ungar PS, Teaford MF, Glander KE, Pastor RF (1995) Dust accumulation in the canopy: A potential cause of dental microwear in primates. Am J Phys Anthropol 97: 93–99.
- 89. Daegling DJ, McGraw WS, Ungar PS, Pampush JD, Vick AE, et al. (2011) Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology. PLoS ONE 6: e23095.
- 90. Alba DM, Almécija S, Moyà-Solà S (2010) Locomotor inferences in Pierolapithecus and Hispanopithecus: Reply to Deane and Begun (2008). J Hum Evol 59: 143–149.
- 91. Almécija S, Alba DM, Moyà-Solà S (2009) Pierolapithecus and the functional morphology of Miocene ape hand phalanges: paleobiological and evolutionary implications. J Hum Evol 57: 284–297.
- 92. Nakatsukasa M (1996) Locomotor differentiation and different skeletal morphologies in mangabeys (Lophocebus and Cercocebus). Folia Primatol 66: 15–24.
- 93. Youlatos D (1998) Positional behavior of two sympatric Guianan capuchin monkeys, the brown capuchin (Cebus apella) and the wedge-capped capuchin (Cebus olivaceus). Mammalia 62: 351–365.
- 94. Ersoy A, Kelley J, Andrews P, Alpagut B (2008) Hominoid phalanges from the middle Miocene site of Paşalar, Turkey. J Hum Evol 54: 518–529.
- 95. Begun DR (1992) Phyletic diversity and locomotion in primitive European hominids. Am J Phys Anthropol 87: 311–340.
- 96. Merceron G, Kaiser TM, Kostopoulos DS, Schulz E (2010) Ruminant diets and the Miocene extinction of European great apes. Proc R Soc B 277: 3105–3112.
- 97. Merceron G, Kostopoulos DS, Bonis Ld, Fourel F, Koufos GD, et al. (2013) Stable isotope ecology of Miocene bovids from northern Greece and the ape/monkey turnover in the Balkans. J Hum Evol 65: 185–198.
- 98. Robinson JG (1986) Seasonal variation in use of time and space by the wedge-capped capuchin monkey, Cebus oliuaceus: Implications for foraging theory. Smithsonian Contrib Zool 431: 1–60.
- 99. Alba DM, Moyà-Solà S, Köhler M, Rook L (2001) Heterochrony and the cranial anatomy of Oreopithecus: some cladistic fallacies and the significance of developmental constraints in phylogenetic analysis. In: de Bonis L, Koufos GD, Andrews P, editors. Hominoid Evolution and Climatic Change in Europe, Vol. 2. Phylogeny of the Neogene Hominoid Primates of Eurasia. Cambridge, Cambridge University Press. pp. 284–315.
- 100. Zanolli C, Rook L, Macchiarelli R (2010) Analyse structurale à haute résolution des dents de Oreopithecus bambolii. Ann Univ Ferrara Museol Sci Natural 6: 69–76.
- 101. Galbany J, Moyà-Solà S, Pérez-Pérez A (2005) Dental microwear variability on buccal tooth enamel surfaces of extant Catarrhini and the Miocene fossil Dryopithecus laietanus (Hominoidea). Folia Primatol 76: 325–341.
- 102. Teaford MF, Robinson JG (1989) Seasonal or ecological differences in diet and molar microwear in Cebus nigrivittatus. Am J Phys Anthropol 80: 391–401.
- 103. Marmi J, Casanovas-Vilar I, Robles JM, Moyà-Solà S, Alba DM (2012) The paleoenvironment of Hispanopithecus laietanus as revealed by paleobotanical evidence from the Late Miocene of Can Llobateres 1 (Catalonia, Spain). J Hum Evol 62: 412–423.
- 104. Costeur L (2005) Cenogram analysis of the Rudabánya mammalian community: palaeoenvironmental interpretations. Palaeontogr Ital 90: 303–307.
- 105. Skinner MF, Dupras TL, Moyà-Solà S (1995) Periodicity of linear enamel hipoplasia among Miocene Dryopithecus from Spain. J Paleopathol 7: 195–222.
- 106. Eastham L, Skinner MM, Begun DR (2009) Resolving seasonal stress in the Late Miocene hominoid Hispanopithecus laietanus through the analysis of the dental developmental defect linearenamel hypoplasia. J Vert Paleontol 29: 91A.
- 107. Skinner MF, Hopwood D (2004) Hypothesis for the causes and periodicity of repetitive linear enamel hypoplasia in large, wild African (Pan troglodytes and Gorilla gorilla) and Asian (Pongo pygmaeus) apes. Am J Phys Anthropol 123: 216–235.
- 108. Moyà-Solà S, Köhler M (1996) A Dryopithecus skeleton and the origins of great-ape locomotion. Nature 379: 156–159.
- 109. Almécija S, Alba DM, Moyà-Solà S, Köhler M (2007) Orang-like manual adaptations in the fossil hominoid Hispanopithecus laietanus: first steps towards great ape suspensory behaviours. Proc R Soc B 274: 2375–2384.
- 110. Deane AS, Begun DR (2008) Broken fingers: retesting locomotor hypotheses for fossil hominoids using fragmentary proximal phalanges and high-resolution polynomial curve fitting (HR-PCF). J Hum Evol 55: 691–701.
- 111. Böhme M, Aziz HA, Prieto J, Bachtadse V, Schweigert G (2011) Bio-magnetostratigraphy and environment of the oldest Eurasian hominoid from the Early Miocene of Engelswies (Germany). J Hum Evol 61: 332–339.
- 112. Ward SC, Duren DL (2002) Middle and Late Miocene African Hominoids. In: Hartwig WC, editor. The primate fossil record. Cambridge, Cambridge University Press. pp. 385–397.
- 113. Andrews P, Bernor RL (1999) Vicariance biogeography and paleoecology of Eurasian Miocene hominoid primates. In: Agusti J, Rook L, Andrews, P, editors.The evolution of Neogene terrestrial ecosystems in Europe. Cambridge, Cambridge University Press. pp. 454–487.
- 114. Pérez de los Ríos M, Moyà-Solà S, Alba DM (2012) The nasal and paranasal architecture of the Middle Miocene ape Pierolapithecus catalaunicus (Primates: Hominidae): Phylogenetic implications. J Hum Evol 63: 497–506.
- 115. Utescher T, Bruch AA, Micheels A, Mosbrugger V, Popova S (2011) Cenozoic climate gradients in Eurasia e a palaeo-perspective on future climate change? Palaeogeogr Palaeoclimatol Palaeoecol 304: 351–358.
- 116. Andrews P (1996) Palaeoecology and hominoid palaeoenvironments. Biol Rev 71: 257–300.
- 117. Casanovas-Vilar I, Alba DM, Moyà-Solà S, Galindo J, Cabrera L, et al. (2008) Biochronological, taphonomical and paleoenvironmental background of the fossil great ape Pierolapithecus catalaunicus (Primates, Hominidae). J Hum Evol 55: 589–603.
- 118. DeMiguel D, Azanza B, Morales J (2011) Paleoenvironments and paleoclimate of the Middle Miocene of central Spain: A reconstruction from dental wear of ruminants. Palaeogeogr Palaeoclimatol Palaeoecol 302: 452–463.
- 119. Merceron G, Costeur L, Maridet O, Ramdarshan A, Göhlich UB (2012) Multi-proxy approach detects heterogeneous habitats for primates during the Miocene climatic optimum in Central Europe. J Hum Evol 63: 150–161.
- 120. Agustí J, Sanz de Siria A, Garcés M (2003) Explaining the end of the hominoid experiment in Europe. J Hum Evol 45: 145–153.
- 121. Matson SD, Rook R, Oriol O, Fox DL (2012) Carbon isotopic record of terrestrial ecosystems spanning the Late Miocene extinction of Oreopithecus bambolii, Baccinello Basin (Tuscany, Italy). J Hum Evol 63: 127–139.
- 122. Potts R (2004) Paleoenvironments and the evolution of adaptability in great apes. In: Russon AE, Begun DR, editors. The evolution of thought. Evolutionary origins of great ape intelligence. Cambridge, Cambridge University Press. pp. 237–258.
- 123. Alba DM (2010) Cognitive inferences in fossil apes (Primates: Hominoidea): does encephalization reflect intelligence? J Anthropol Sci 88: 11–48.