AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 151:573–582 (2013)
European Pliopithecid Diets Revised in the Light of Dental Microwear in Pliopithecus canmatensis and Barberapithecus huerzeleri -Sola 3 Daniel DeMiguel,1 David M. Alba,1,2* and Salvador Moya 1
Institut Catal a de Paleontologia Miquel Crusafont, Universitat Autonoma de Barcelona, Edifici ICP, Campus de la UAB s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain 2 Dipartimento di Scienze della Terra, Universit a degli Studi di Torino, Via Valperga Caluso 35, 10125 Torino, Italy 3 ICREA at Institut Catal a de Paleontologia Miquel Crusafont and Unitat d’Antropologia Biologica (Departament BABVE), Universitat Autonoma de Barcelona, Edifici ICP, Campus de la UAB s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain KEY WORDS
fossil primates; Pliopithecidae; diets; Catalonia; Spain
ABSTRACT Pliopithecinae and Crouzeliinae (Primates: Pliopithecidae) are distinguished dentally by the sharper crests, more compressed cusps, larger foveae, and narrower molars of the latter. Traditionally, such differences were qualitatively related to increased folivory in crouzeliines. This was subsequently disproved by microwear and shearing crest analyses, indicating that all pliopithecids were soft-fruit eaters, except for the more folivorous crouzeliine Barberapithecus. This seems however at odds with the occlusal morphology of the latter, intermediate between those of Pliopithecus and the more derived crouzeliine Anapithecus. To further assess dietary evolution in this group, we report results of dental microwear for two Iberian pliopithecids: Pliopithecus canmatensis, from several Abocador de Can Mata localities (11.8–11.7 Ma, MN8), and Barberapithecus huerzeleri from Castell de Barber a (ca. 11.2–10.5 Ma, MN8, or MN9). Contrary to previously published results, our
analyses suggest that all pliopithecids, including Barberapithecus, had a frugivorous diet with a significant sclerocarpic component—apparently more marked in some pliopithecines (such as P. canmatensis) than in the crouzeliine Anapithecus. If our interpretation is correct, it would mean that, within the framework of a frugivorous diet with some hard-object feeding, crouzeliine dental evolution would have been driven by selection pressures towards increased soft-fruit consumption instead of folivory. Dental differences between pliopithecids and hominoids with a significant sclerocarpic component (i.e., orangutans) might be related to phylogenetic constraints, different food-processing methods and/or fracture toughness of hard foods consumed. Although additional research would be required, results suggest that dietary niche partitioning played a significant role in the radiation of European pliopithecids. Am J Phys Anthropol 151:573–582, 2013. VC 2013 Wiley Periodicals, Inc.
Pliopithecoids constitute a clade of late early to early late Miocene catarrhines that, before hominoids, dispersed into Eurasia and hence initially diversified across this continent when it was devoid of other anthropoid primates (Begun, 2002; Harrison, 2005). Although the phylogenetic relationships of pliopithecoids with living and other extinct catarrhines are still unclear, it is currently widely accepted that they are stem catarrhines preceding the cercopithecoid-hominoid split (e.g., Begun, 2002; Harrison, 2005). Three different pliopithecoid subclades are customarily recognized (Table 1), being here classified into a single family Pliopithecidae with three distinct subfamilies (Moy a-Sol a et al., 2001; Alba et al., 2010; Alba and Moy a-Sol a, 2012): Dionysopithecinae, Pliopithecinae and Crouzeliinae. It has been proposed that pliopithecoids initially diversified in Asia by the early Miocene, and later dispersed into Europe by the early middle Miocene, where crouzeliines might have locally evolved, probably from a pliopithecine-like ancestor (Harrison, 2005). However, the recent report of a putative stem crouzeliine—still undescribed—in the early Miocene of Asia (Harrison and Jin, 2009) might alternatively suggest that both groups initially diversified there and only later dispersed independently into Europe. In any case, several authors have noted a likely sister-taxon relationship between pliopitheciines and
crouzeliines (Harrison and Gu, 1999; Harrison, 2005; Alba et al., 2010). Such a relationship might justify a distinct family status for dionysopithecines (Harrison, 2005), which are apparently the basal-most pliopithecids (Harrison and Gu, 1999; Harrison, 2005). However, given the contrasting systematic schemes adopted by other authors (Begun, 2002), here we prefer to
Ó 2013 WILEY PERIODICALS, INC.
Additional Supporting Information may be found in the online version of this article. Grant sponsor: Spanish Ministerio de Economıa y Competitividad; Grant numbers: CGL2011-28681, CGL2011-27343, CGL2010-21672/ BTE, JCI-2011-11697 to DDM, RYC-2009-04533 to DMA; Grant sponsor: Generalitat de Catalunya; Grant number: 2009 SGR 754 GRC. *Correspondence to: David M. Alba, Institut Catal a de Paleontologia Miquel Crusafont, Universitat Aut onoma de Barcelona, Edifici ICP, Campus de la UAB s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain. E-mail:
[email protected] Received 17 January 2013; accepted 29 April 2013 DOI: 10.1002/ajpa.22299 Published online in Wiley Online Library (wileyonlinelibrary.com).
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DEMIGUEL ET AL. TABLE 1. Systematic scheme of the Pliopithecidae to the genus level
Family Pliopithecidae Zapfe, 1961 Subfamily Dionysopithecinae Harrison and Gu, 1999 Genus Dionysopithecus Li, 1978 Genus Platodontopithecus Gu and Lin, 1983 Subfamily Pliopithecinae Zapfe, 1961 Genus Pliopithecus Gervais, 1849 Genus Epipliopithecus Zapfe and H€ urzeler, 1957 Subfamily Crouzeliinae Ginsburg and Mein, 1980 Tribe Crouzeliini Ginsburg and Mein, 1980 Genus Plesiopliopithecus Zapfe, 1961 Tribe Anapithecini Alba and Moy a-Sol a, 2012 Genus Anapithecus Kretzoi, 1975 Genus Laccopithecus Wu and Pan, 1984 Genus Egarapithecus Moy a-Sol a et al., 2001 Genus Barberapithecus Alba and Moy a-Sol a, 2012
distinguish the three pliopithecoid putative subclades merely at the subfamily level (Harrison and Gu, 1999; Moy a-Sol a et al., 2001; Alba et al., 2010; Alba and Moy aSol a, 2012). Recently, Alba and Moy a-Sol a (2012) erected a new crouzeliine tribe (Anapithecini) for all crouzeliine genera except Plesiopliopithecus, which is the oldest known European crouzeliine. Insufficient knowledge on the latter taxon (its upper dentition is completely unknown) hinders attaining a more secure assessment on the phylogenetic relationships between the various pliopithecid subfamilies, which mainly differ in dental occlusal details. Crouzeliines, in particular, display sharper crests, more compressed cusps, larger foveae, and relatively narrower and more elongated molars than pliopithecines (Andrews et al., 1996; Begun, 2002; Alba et al., 2010; Alba and Moy a-Sol a, 2012; see Fig. 1). It has been recognized that the strict monophyly of the several pliopithecoid subfamilies is uncertain—especially that of pliopithecines, which might be paraphyletic (e.g., Begun, 2002). However, most recently Alba and Moy a-Sol a (2012) further argued that the mosaic of dental features displayed by the putative anapithecin crouzeliine Barberapithecus—displaying several dental synapomorphies with Anapithecus, but still retaining a more pliopithecine-like occlusal morphology— might indicate an independent origin for anapithecins and crouzeliins. If so, the dental features traditionally employed to distinguish crouzeliines from pliopithecines might have evolved more than once, and crouzeliines as currently conceived would be paraphyletic. In order to further evaluate the possibility that crouzeliin and anapithecin dental similarities are homoplastic, more information is required on the selection pressures that might underlie the evolution of dental morphology in these taxa. On qualitative grounds, the differences in occlusal morphology between crouzeliines and pliopithecines were traditionally related to adaptations towards increased folivory (i.e., a heavy reliance on leaves and stems) in the former, contrasting with the frugivorous diet (primarily relying on fruit and bark components) inferred for pliopithecines (Ginsburg and Mein, 1980; Begun, 1989; Andrews et al., 1996). Such a hypothesis, largely interpreted as the result of a competitive exclusion model, was contradicted by subsequent quantitative analyses. In particular, shearing crest quotients (Ungar and Kay, 1995; Kay and Ungar, 1997; Ungar, 2005) and dental microwear analyses (Ungar, 1996, 2005) failed to confirm the possession of a folivorous diet in all crouzeliines. According to these studies, American Journal of Physical Anthropology
Fig. 1. Lower dentition of European pliopithecines and crouzeliines, depicted as from the left side. A,B: Pliopithecus antiquus M2-M3 from La Grive PB A (A, reversed) and P3-M3 from Sansan (B, holotype); C–E: P. canmatensis P3-M3 from ACM/C4A1 (C, holotype), ACM/C4-Cb (D, paratype) and ACM/C5-C3 (E, paratype); F: Barberapithecus huerzeleri composite P3-M3 from Castell de Barber a (holotype, some teeth reversed); G: Plesiopliopithecus auscitanensis from Sansan. Artwork by Marta Palmero, reproduced from Alba and Moy a-Sol a (2012).
only Barberapithecus was interpreted as extremely folivorous, whereas the crouzeliine Anapithecus emerged as equally frugivorous to the pliopithecines Pliopithecus and Epipliopithecus. The congruence between shearing crest and microwear analyses suggests that the depiction of Barberapithecus as more folivorous than Anapithecus is quite robust (Kay and Ungar, 1997; Ungar, 2005). This is however at odds with the qualitative description of the Barberapithecus occlusal morphology (Alba and Moy a-Sol a, 2012) as intermediate between pliopithecines (especially Pliopithecus canmatensis) and more derived anapithecins (such as Anapithecus). Understanding the selective pressures that underpin the dental differences between these taxa, and especially the pliopithecine P. canmatensis and the most primitive anapithecin Barberapithecus, is therefore of utmost significance for evaluating the evolution of European pliopithecids. Here we report new data of dental microwear for P. canmatensis and Barberapithecus huerzeleri (see Alba et al., 2011, and DeMiguel et al., 2012, for preliminary reports). In the light of these data, we review the paleodietary inferences for European pliopithecids, with particular emphasis on the potential role played by dietary compartmentalization in the evolution of this group.
MATERIAL AND METHODS Studied taxa The sample studied in this article includes the M2 of Barberapithecus huerzeleri from Castell de Barber a (CB), with an estimated age of ca. 11.2–10.5 Ma (MN8 or MN9, latest Aragonian or earliest Vallesian; Alba and Moy a-Sol a, 2012); and seven upper and lower molars of Pliopithecus canmatensis from four Abocador de Can Mata (ACM) localities (Alba et al., 2010), with estimated ages of 11.7 and 11.8 Ma (MN8, latest Aragonian; Alba et al., 2012): IPS41981, IPS41983 and IPS41984 from ACM/C5-C3; IPS41955 from C5-A8; IPS35036 and IPS41718 from C4-A1; and IPS41719 from C4-Cb (see
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EUROPEAN PLIOPITHECID DIETS TABLE 2. Results of the microwear analysis Taxon
Record No.
Tooth
P. canmatensis P. canmatensis P. canmatensis P. canmatensis P. canmatensis P. canmatensis P. canmatensis B. huerzeleri
IPS41981 IPS41955 IPS41718 IPS41983 IPS41719 IPS41984 IPS35036 IPS1724n
R L R L R L L R
Number of marks
% Pits
Pit Breadth
Scratch Breadth
39 42 42 28 38 31 89 37
41.03 33.33 33.33 46.43 39.47 32.26 42.70 32.43
5.89 6.94 6.28 5.25 4.27 4.00 3.65 5.57
2.26 2.69 2.10 4.07 3.13 2.40 1.97 3.57
M3 M1 M2 M1 M1 M2 M1 M2
Abbreviations: R, right; L, left.
TABLE 3. Comparative sample of extant and extinct species employed in this paper, based on previously published microwear data (N refers to the sample size employed in these studies) Extant species b
Gorilla gorilla Alouatta palliatab Colobus guerezab Cebus capucinusb Piliocolobus badiusb Cebus nigrivittatusj Papio cynocephaluso Pan troglodytesb Pongo pygmaeusb Cebus apellab Lophocebus albigenab Extinct species Anapithecus hernyakid,w Pliopithecus platyodond Epipliopithecus vindobonensisd
N
Dietary category
10 10 10 10 10 10 16 10 10 10 10 N 5 2 1
Folivoresa–c Folivoresb–f Folivoresb,d,g,h Frugivores / Mixed feedersb–d Frugivores / Mixed feedersb,i Frugivores / Mixed feedersc,j,k Frugivores / Mixed feedersc,l–o Frugivores / Mixed feedersb–d Hard-object specialistsb,c,p–s Hard-object specialistsb–d Hard-object specialistsb–d,t–v — — —
The dietary categories used in the cluster and discriminant analyses are also included. Sources for microwear data and dietary categories are indicated by means of superscript. a Fossey and Harcourt (1977). b Teaford (1988). c Teaford et al. (1996). d Ungar (1996). e Semprebon et al. (2004). f Estrada (1984). g Plumptre and Reynolds (1994). h Grassi (2006). i Clutton-Brock (1975). j Teaford (1985). k Teaford and Robinson (1989). l Butynski (1982). m Benefit and McCrossin (1990). n Benefit (1999). o El-Zaatari et al. (2005). p MacKinnon (1977). q Taylor (2006). r Vogel et al. (2008). s Daegling et al. (2011). t Chalmers (1968). u Waser (1975). v Waser (1977). w Ungar (2005).
Table 2 for tooth positions). Note that only a single molar of B. huerzeleri out of the eight available was examined, in order to avoid the error introduced by combining results from different teeth belonging to the same individual.
Dental microwear analyses After light microscopy examination at 50X, original specimens deemed suitable for microwear study were observed at a magnification of 500X using an Environmental Scanning Electron Microscope (ESEM) FEI Quanta 200 at the Serveis Cientificote`cnics of the Universitat de Barcelona (Spain). Occlusal surfaces were examined in secondary emissions mode and at 20 kV following the procedure described by Teaford (1988). Whenever possible, several micrographs were taken of each molar on the Phase II crushing/grinding facets of Kay (1977). An area of standardized size, corresponding to a field of view of 0.02 mm2 on the original facet (Ungar, 1996, 2005; Grine et al., 2006), was used for the analysis. Images were analyzed using Microware 4.02 (Ungar, 2002). All features in the present study were identified and measured by a single observer (DDM) in order to avoid interobserver error (Grine et al., 2002). Scratches and pits were directly categorized by following an arbitrarily set length to width ratio of 4:1 on the features (Solounias et al., 1988; Teaford, 1988; Ungar, 1996; Grine et al., 2002). That is, all features with a length to width ratio equal to or above 4:1 were classified as scratches, and all those with a ratio below 4:1 were classified as pits. The following three variables—the most informative for separating primates by diets in trophic analyses (Walker and Teaford, 1989; El-Zaatari et al., 2005)—were computed: percentage of pits, breadth of scratches and breadth of pits. Our results were compared with those previously obtained by Teaford (1985, 1988) for several extant primates with well-documented diets (see Table 3) by using a sufficiently similar technique to that described here to allow comparison of results. To the comparative sample, we also included data for Papio cynocephalus reported by El-Zaatari et al. (2005). The microwear pattern obtained for the fossil species was therefore compared with this set of 11 extant primates, which were partitioned into three distinct dietary categories (Table 3): folivores, mixed feeders (mainly frugivores), and hardobject feeders. The reason why we compile several species into a single category of “frugivores/mixed feeders,” following Teaford et al. (1996), is 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 (Altmann and Altmann, 1970; G€ unther and Boesch, 1993; Wahungu, 1998; Benefit, 1999; Fox et al., 2004). We also compared our results with the microwear data published by Ungar (1996, 2005) for other Miocene European pliopithecids (Andrews et al., 1996; Begun, 2002): the pliopithecines Epipliopithecus vindobonensis from Devinsk a Nov a Ves (MN6) in Slovakia, and Pliopithecus American Journal of Physical Anthropology
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DEMIGUEL ET AL.
Fig. 2. Environmental SEM micrographs of the occlusal surface of Pliopithecus canmatensis (A–E) and Barberapithecus huerzeleri (F). Specimens taken at 500X magnification. A: IPS41981; B: IPS35036; C: IPS41984; D: IPS41719; E: IPS41718; F: IPS1724.
platyodon from G€oriach (MN6) in Austria; and the crouzeliine Anapithecus hernyaki from Rudab anya in Hungary (MN9). It should be noted that Ungar (1996) also analyzed the Castell de Barber a taxon, recently described as Barberapithecus huerzeleri by Alba and Moy a-Sol a (2012). During the last decade, several authors (e.g., Grine et al., 2002; Mihlbachler et al., 2012) have noted that inter-observer error for microwear features can significantly complicate the interpretations when data derived by different researchers are combined into a single analysis. Providing new microwear results for the selected comparative sample is however outside the scope of this paper. However, such a limitation should be borne in mind when interpreting our results. Kolmogorov-Smirnov tests were used to determine goodness of fit to the normal distribution of the variables. Hierarchical cluster analysis was applied as an explorative technique for identifying species groups and emphasizing any inherent structure, based on similarities in microwear pattern. The analysis was performed using the Euclidean distance and Ward’s method. Discriminant analyses were also employed for evaluating the ability of the microwear variables to distinguish between different dietary categories among extant taxa. Pliopithecoids were classified according to the derived discriminant functions. All multivariate statistical tests and sample comparisons were performed using SPSS v. 11 statistical package, on the basis of the following variables: percentage of pits, breadth of scratches, and breadth of pits.
RESULTS Microwear signatures and percentage of pitting All the analyzed variables passed the normality tests (P > 0.05). Microwear summary results are reported in American Journal of Physical Anthropology
Table 2, whereas microwear patterns for the studied taxa are displayed in Figure 2. The percentage of pitting is 32.43% (N 5 1) in Barberapithecus and 38.36% (N 5 7, SD 5 5.48, range 32.26–46.43) in P. canmatensis (Fig. 3A). In turn, pit breadth ranges from 5.57 mm in Barberapithecus to 5.18 mm (SD 5 1.25; range, 3.65–6.94) in P. canmatensis, whereas striation breadth is 3.57 mm in the former and 2.66 mm (SD 5 0.73; range, 1.97–4.07) in the latter (Fig. 3A). Our results indicate that the two species analyzed do not vary significantly in their ratios of pits to scratches or in the size of microwear features. When only mean values are considered, our results would suggest that Barberapithecus displays on average a lower pitting incidence and somewhat larger features than P. canmatensis. However, the values for the single individual available from the former falls in all instances within the maximum2minimum range of P. canmatensis, and even within (percentage of pitting and pit breadth) or not far (striation breadth) one standard deviation from the mean of the latter. Given that interindividual variation in P. canmatensis encompasses that for B. huerzeleri, no significant dietary differences can be supported between these taxa. When compared with extant analogues (Fig. 3A), the percentage of pits in the two pliopithecids analyzed is intermediate between those of frugivores such as Pan troglodytes and mixed feeders such as Papio cynocephalus, on the one hand, and hard-object feeders on the other—the latter including both Pongo pygmaeus (a frugivorous taxon that relies on hard food items more than other extant great apes, especially as fallback foods; Vogel et al., 2008) and more specialized hard-object feeders such as Lophocebus albigena and Cebus apella (Teaford, 1985; McGraw et al., 2012). Both Barberapithecus and P. canmatensis display a pitting incidence
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EUROPEAN PLIOPITHECID DIETS
Fig. 3. Comparison of microwear patterns between pliopithecids and the extant comparative sample. A: Bivariate plot depicting pitting percentage vs. striation breadth. B: Hierarchical cluster diagram based on the percentage of pits, and the breadth of scratches and pits. Data for extant primates were taken from Teaford (1985, 1988) and El-Zaatari et al. (2005), whereas data for pliopithecids were taken from Ungar (1996) and this study.
intermediate between chimpanzees and orangutans, being closer on average to the latter in the case of P. canmatensis. Our data therefore suggest a frugivorous diet with some sclerocarpic component for the two studied pliopithecids. In fact, scratch breadth for Barberapithecus (Fig. 3A) falls within the ranges of specialized hard-object feeders (just below the mean of Lophocebus albigena and above those of Cebus apella and Pongo pygmaeus), although this should be interpreted very cautiously because a single Barberapithecus specimen was analyzed. The narrower scratches displayed on average by P. canmatensis—for which a much larger sample is available—are still intermediate between those of chimpanzees and orangutans (Fig. 3A), and hence compatible with a sclerocarpic diet. In contrast, hard-object feeding in Barberapithecus and P. canmatensis would be contradicted by the pit breadths displayed by these taxa, which are similar to those of the folivorous Colobus guereza and the soft-fruit eater Cebus capucinus, respectively. Pit breadth, however, is a more variable feature than scratch breadth among extant and extinct taxa (Teaford, 1988; King et al, 1999), so we do not consider the former to be a reliable paleodietary indicator. When the microwear signatures of the Valle`s-Penede`s taxa are compared with those published for other pliopithecids (E. vindobonensis, N 5 1; P. platyodon, N 5 2; and A. hernyaki, N 5 5), no significant differences in pit percentage can be observed. All these taxa display pit percentages intermediate between those of frugivores and those of Pongo pygmaeus and hard-object specialists (Fig. 3A). Next to the single individual of Barberapithecus, Anapithecus displays the lowest mean percentage of pits among pliopithecids (Fig. 3A). Such differences between anapithecins and pliopithecines, however, might not be significant, since the former overlap with the variation of P. canmatensis. Overall, our results for pitting percentages indicate that, within a frugivorous spectrum, the diet of all pliopithecines displayed a greater emphasis on sclerocarpy than previously suspected—which on the basis of striation breadth might have been even greater in the two Valle`s-Penede`s taxa.
Cluster and discriminant analyses A cluster analysis of dental microwear features in extant species (Supporting Information Fig. S1) successfully separates those primates that display a significant sclerocarpic component (cluster A) from those that mostly rely on soft items (cluster B, including folivores and frugivores). When fossil taxa are included in the analysis (Fig. 3B), all European pliopithecids cluster together within a new group (subcluster A1), within a larger cluster that further includes extant hard-object specialists and P. pygmaeus (subcluster A2). Multivariate discriminant analyses (Table 4, Fig. 4) based on the same variables (percentage of pits, and breadth of pits and scratches) in extant taxa provide a satisfactory discrimination of dietary types: 100% extant species are correctly classified when three dietary categories (folivores, frugivores/mixed feeders and hardobject feeders, the latter including orangutans) are distinguished (Fig. 4). Barberapithecus and P. canmatensis are classified as hard-object feeders (Fig. 4, Table 4), like the remaining pliopithecids. Note that all fossil pliopithecids clearly fall away from extant leaf-eaters in the first discriminant function (which explains most of the variance and is predominantly driven by the percentage of pitting), and occupy instead an intermediate position between frugivorous and hard-object feeders, thereby suggesting a somewhat intermediate dietary regime. In fact, pliopithecids are in all instances closer to the hardobject feeder centroid than to that of any other dietary regime, including frugivores/mixed feeders, although they fall outside the variation of this group (P < 0.05) in all instances except for P. canmatensis, which is the taxon that falls closest to Pongo when the second discriminant function (predominantly driven by scratch breadth) is also taken into account.
DISCUSSION Comparison with previous results Among microwear features, the relative proportion between pits and scratches most clearly enables one to American Journal of Physical Anthropology
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DEMIGUEL ET AL. TABLE 4. Results of the discriminant analysis based on microwear features
CV
Eigenvalue
% variance
% cumulative variance
Canonical correlation
CV1 CV2
10.355 0.348
96.7 3.3
96.7 100
0.955 0.508
Standardized coefficients of the CVs CV
Pitting percentage
Pit breadth
Scratch breadth
CV1 CV2
1.045 20.442
20.093 0.346
20.055 0.940
Nonstandardized coefficients of CV CV
Pitting percentage
Pit breadth
Scratch breadth
Constant
CV1 CV2
0.183 20.077
20.055 0.206
20.086 1.454
23.673 22.477
Group centroids CV
Folivores
Frugivores
Hard-object feeders
CV1 CV2
22.800 0.642
20.896 20.526
4.294 0.235
Predictions for fossils
1st group p D2 2nd group D2
Pliopithecus canmatensis Hard-object feeders
Barberapithecus huerzeleri Hard-object feeders
Anapithecus hernyaki Hard-object feeders
Pliopithecus platyodon Hard-object feeders
Epipliopithecus vindobonensis Hard-object feeders
0.259 2.698
0.016 8.252
0.013 8.643
0.029 7.115
0.016 8.273
Frugivorous 13.892
Frugivorous 9.988
Frugivorous 13.413
Frugivorous 12.264
Frugivorous 19.672
CV, canonical variate; D2, Squared Mahalanobis distance.
distinguish between broad dietary categories among primates, with frugivores displaying a higher percentage of pits than folivores, and hard-object feeders an even higher frequency of pits than the former (Teaford and Walker, 1984; Teaford, 1985, 1991; Ungar, 1992, 1996, 1998; King et al., 1999a; King, 2001). According to previous results (e.g., Ungar, 2005), all pliopithecines except Barberapithecus would display percentages of pitting intermediate between extant folivores and hard-object feeders, being interpreted as indicative of a frugivorous diet (Ungar, 1996, 1998, 2005). Barberapithecus, in turn, would display a higher prevalence of scratches (in percentage), indicative of a folivorous diet (Ungar, 1996). In contrast, our microwear results indicate that both P. canmatensis and Barberapithecus would be roughly similar to the other pliopithecids. Regarding Barberapithecus, the discrepancy between our results and those of Ungar (1996) is difficult to explain. The different results produced by these two studies should be related to how measurements were taken and/or analyzed. The various reasons that might explain the different results obtained by both studies are discussed in greater detail below. We employed a comparable methodology to Ungar’s (1996) regarding microscope magnification and the extent of tooth surface area to be analyzed. Although the results for Barberapithecus cannot be directly compared because Ungar (1996) did not report catalogue numbers, it should be noted that the total number of microwear features we measured in the M2 (37) and in the left M2 American Journal of Physical Anthropology
(43, not included in the analyses) is much lower than the counts of 124 and 107 provided by Ungar (1996) for two unspecified specimens out of the three available second molars of Barberapithecus. The results of both studies further differ regarding percentages of pitting, with Ungar (1996) reporting values of 23% and 11%, which contrast with the 32% documented by our study for the M2 and the even higher percentage of 63% recorded for the M2 not included in our analyses. Given that comparable measurement techniques were employed, differences might be related to the fact that we measured microwear features from ESEM micrographs taken on the original fossil remains, whereas Ungar (1996) relied on casts—which cannot be further evaluated because Ungar (1996) did not publish any SEM image for Barberapithecus. Alternatively, differences might be related to the treatment of post-mortem artifacts, but this seems unlikely because we detected no taphonomic artifacts that might have distorted the counting of microwear features. Most of the fossils from Castell de Barber a, like the teeth of P. canmatensis from Abocador de Can Mata, come from fine clay deposits (S.M.S.’s personal observation) that, unlike coarser sediments (especially mediumsized sands; King et al., 1999b), are highly unlikely to distort the original microwear signal. In addition, enamel surfaces of the specimens have not been acid etched and are therefore suitable for microwear study. In any case, our microwear results—indicating a broadly similar dietary regime for all pliopithecids—appear to be
EUROPEAN PLIOPITHECID DIETS
Fig. 4. Bivariate plot of the first two canonical axes delivered by the discriminant analysis based on three different dietary groups. Colored areas indicate the morphospace defined by dental microwear signatures of extant taxa, the ellipses being defined as the 95% confidence intervals. Large black symbols represent the centroids. Data sources as in Figure 3.
more consistent with the occlusal morphology of Barberapithecus (Alba and Moy a-Sol a, 2012) than those by Ungar (1996), which indicated marked dietary differences between Barberapithecus and Anapithecus.
Paleodietary inferences in pliopithecids Our study further differs from that of Ungar (1996, 1998, 2005) in that pliopithecids as a group are depicted as frugivores with a sclerocarpic component, since they are not intermediate between folivores and hard-object feeders (Ungar, 1996), but intermediate between frugivores with no significant sclerocarpic component (such as chimpanzees) and primates with a significant sclerocarpic component (orangutans). Our microwear data suggest that, among the comparative sample, Pongo would probably be the most similar taxon to pliopithecids in dietary preferences. The classification of Pongo as a hard-object feeder instead of a frugivore is not a semantic issue, but has important consequences for the paleodietary characterization. Sclerocarpic foraging refers to the consumption of hard food items, such as seeds and the mesocarp of unripe fruit (Kinzey and Norconk, 1990; Martin et al., 2003; Vogel et al., 2008). Orangutans are neither hardobject specialists—like other hominoids, they display a marked preference for ripe fruit—nor strict fruit-eaters. Among hominoids, emphasis on soft and hard fruits varies depending on the various species (Andrews and Martin, 1991), and orangutans consume harder fruits on average and also more frequently unripe fruits than other great apes (Ungar, 1992, 1995; King, 2001; and references therein). Moreover, whereas chimpanzees become
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seasonal folivores when ripe fruit is not available, orangutans habitually consume tougher and harder items as fallback foods (Vogel et al., 2008). Our microwear results therefore suggest that all pliopithecids had a sclerocarpic component in their diets that was greater than previously thought (e.g., Ungar, 1996, 2005). The variability observed in microwear signals in the sample of P. canmatensis might be partly attributable to seasonal dietary differences, since extant frugivores customarily consume poorer food items than usual as fallback foods during the unfavorable season (Teaford, 1985; Teaford and Robinson, 1989; Teaford and Runestad, 1992). However, the sample size analyzed for P. canmatensis (N 5 7)—entirely comparable, or even higher than those employed by Ungar (1996)—should be considered a priori representative of the dietary behavior of this taxon. The molars of P. canmatensis analyzed in this study come from four different localities with a similar estimated age of 11.8–11.7 Ma (Alba et al., 2010) within the same geographic area. These facts suggest similar paleoenvironmental conditions, but there is no reason to assume ad hoc that they were deposited during the same season, so that seasonal differences in dietary behaviors are unlikely to have skewed our results for this taxon. The subtle differences observed between P. canmatensis and Barberapithecus might be simply attributable to a sampling effect, given that only a single individual of the latter is available. However, the comparison of P. canmatensis with the larger sample of Anapithecus suggests that some dietary differences might have existed among pliopithecids. While the former most closely resembles orangutans, Anapithecus displays a primarily frugivorous diet with a lesser sclerocarpic component. Such differences might imply that the evolutionary changes in crouzeliine occlusal morphology might not be related to increased folivory—as traditionally hypothesized (Ginsburg and Mein, 1980; Begun, 1989; Andrews et al., 1996)—but rather to a decreased emphasis on sclerocarpic foraging and a higher reliance on soft fruits. The percentage of pitting in P. canmatensis is comparable to that reported by Ungar (1996) for Epipliopithecus vindobonensis. The latter author did not mention a sclerocarpic component for this taxon, because he considered Pongo as a frugivore instead of as a hard-object feeder, even including it within the same frugivorous category as Pan and several monkeys (Ungar, 2005, his Fig. 1), in spite of the fact that the former taxon consumes a greater proportion of hard-food items. Some degree of simplification is unavoidable when inferring categories. However, these categories are required in order to do discriminant analyses that take into account several other microwear features simultaneously. Here we follow Teaford et al. (1996) and other subsequent authors (e.g., Taylor, 2006; Vogel et al., 2008; Daegling et al., 2011) in considering orangutans as hard-object feeders (even recognizing that they are not hard-object specialists), and also in considering that mixed feeders such as Papio cynocephalus are best included into the same category than more strictly frugivorous taxa such as Pan. Such a categorization is supported by the results of our cluster analysis—which does not assume categories a priori—whereas lumping together orangutans and chimpanzees into a single frugivorous category (e.g., Ungar, 2005) would obscure the significant dietary differences (and associated microwear signal) between these taxa. Such interpretative and analytical differences compared to Ungar’s (1996, 2005) American Journal of Physical Anthropology
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explain our differing conclusion that pliopithecid diets included a significant sclerocarpic component. Our interpretation is apparently contradicted by shearing crest quotients derived for Barberapithecus (Ungar and Kay, 1995; Ungar, 1996, 1998; Kay and Ungar, 1997), but it should be taken into account that shearing crest quotients are highly dependent on the particular group being analyzed (Ungar, 2005). Interpreting pliopithecid shearing quotients in the light of the extant hominoid standard (e.g., Ungar and Kay, 1995) is probably unwarranted, because pliopithecids are stem catarrhines only distantly related to hominoids. Preliminary results on enamel thickness for the two Iberian pliopithecids (Alba et al., 2011) have also suggested a thin-enameled condition, which would be contradictory given the relationship noted by several authors between hard-object feeding and thick enamel (Schwartz, 2000; Andrews and Martin, 2001; Lucas et al., 2008; Vogel et al., 2008). However, there is no good link between enamel thickness and dietary behavior—the former being highly influenced by phylogenetic constraints (Olejniczak et al., 2008)—and there is no threshold value for distinguishing hard-object feeders on the basis of enamel thickness alone (Dumont, 1995; Maas and Dumont, 1999). Thick enamel is not a necessary prerequisite for hard-object feeding, as shown by pitheciins, which employ the anterior dentition for breaking hardfood items and the posterior (thin-enameled) dentition to process softer foods (Martin et al., 2003). Experimental data, however, indicate that hard-food items leave a recognizable microwear signal even if processed at the front of the mouth (Teaford et al., 2010). Microwear analyses have the advantage, over morphology-based paleodietary indicators (such as shearing crest analysis and relative enamel thickness), that they provide an ecophenotypic signal, i.e., data reflecting actual use instead of adaptation (Ungar, 2005). In this regard, microwear results are free from evolutionary inertia, and hence probably more reliable than enamel thickness or shearing quotients for making paleodietary inferences in an extinct group of stem catarrhines, such as pliopithecids, which potentially might have displayed a dietary behavior unlike any extant catarrhine.
CONCLUSIONS Our microwear analyses suggest that pliopithecids displayed a frugivorous diet with a higher sclerocarpic component than previously recognized, apparently more marked in pliopithecines than in crouzeliines. Although differences between Barberapithecus and Pliopithecus are difficult to ascertain given the small available sample for the former, differences emerge when the crouzeliine Anapithecus is compared to pliopithecines (especially P. canmatensis). If our interpretation is correct, then the sharper crests and other associated morphological traits of crouzeliines, if derived from a pliopithecine-like ancestor, should be interpreted as adaptations towards a frugivorous diet with a higher incidence of soft fruits, i.e., with a lesser reliance on hard-fruit items. In summary, crouzeliine dental evolution might have been driven by decreased sclerocarpy, instead of increased folivory as traditionally assumed. Differences in occlusal morphology and enamel thickness of pliopithecids compared to hominoids with a significant sclerocarpic component (such as orangutans) might be simply related to phylogenetic constraints, although American Journal of Physical Anthropology
differences in food processing methods (as illustrated by the thin-enameled pitheciines) and/or in the nature of the consumed hard-food items (i.e., arthropods/mollusks vs. hard fruits) should not be discounted. Additional research, including the study of incisor microwear in pliopithecids, and enlarging the sample of extant taxa available for comparison, would be required in order to confirm the presence of a significant sclerocarpic component in the diet of pliopithecids, as well as to further assess the role played by dietary niche partitioning between crouzeliines and pliopithecins during the Miocene radiation of the Pliopithecidae.
ACKNOWLEDGMENTS The authors are grateful to Mark F. Teaford for providing valuable literature, Peter Ungar for helpful assistance with the microwear protocol, and Terry Harrison, the Editor and Associated Editor, and two anonymous reviewers for providing helpful comments and suggestions on previous versions of this article.
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