Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology
Buccal microwear patterns on teeth are good indicators of the abrasiveness of foodstuffs and have been used to trace the dietary habits of fossil species, including primates and hominids. However, few studies have addressed the variability of this microwear. The abrasiveness of dietary components depends not only on the hardness of the particles ingested, but also on the presence of dust and other exogenous elements introduced during food processing. These elements are responsible for the microwear typology observed on the enamel surfaces of primate teeth. Here we analyzed the variability of buccal microwear patterns in African Great Apes (Gorilla gorilla and Pan troglodytes), using tooth molds obtained from the original specimens held in several osteological collections. Our results suggest that ecological adaptations at subspecies or population level account for differences in microwear patterns, which are attributed to habitat and ecological conditions within populations rather than differences between species. The findings from studies on the variability of buccal dental microwear in extant species will contribute to a better understanding of extinct hominids’ diet and ecology.
KeywordsDental microwear SEM Pan troglodytes Gorilla gorilla
Dental microwear on occlusal or buccal enamel surfaces has been examined in modern human hunter-gatherer populations as well as in fossil hominids (Puech 1982, 1984, 1986a, b; Grine 1986, 1987; Ungar and Grine 1991; Lalueza and Pérez-Pérez 1993; Lalueza et al. 1993, 1996; Martínez et al. 2001; Pérez-Pérez et al. 1994, 1999, 2003a, b; Martínez and Pérez-Pérez 2004; Romero et al. 2003/2004). Studies of buccal tooth surfaces of extant primates, though scarce (Ungar and Teaford 1996; Galbany et al. 2002; Galbany and Pérez-Pérez 2004), are useful for interpreting the dietary habits of fossil primates (Galbany et al. 2005a; Galbany 2006). Hominoidea primates show much more homogeneous microwear patterns than Cercopithecoidea species of the genus Cercopithecus, Colobus or Papio (Galbany and Pérez-Pérez 2004; Galbany et al. 2005a). However, preliminary analyzes of these patterns within Hominoidea indicate differences in ecological conditions and dietary habits within species. Populations living in isolated, singular habitats, such as the gorillas in Congo or Nigeria (Rogers et al. 2004), show distinct microwear patterns, whereas species subjected to similar ecological conditions, such as chimpanzees and gorillas in Cameroon, show similar patterns (Galbany et al. 2002). If the differences in ecological conditions, food availability and food choice result in variations in microwear patterns within Hominoidea, then microwear patterns of fossil hominid specimens could be used to infer the ecological diversification of our hominid ancestors, independently of habitat reconstruction or the morphological adaptations of dentition.
Here we focused on the within-group variability of microwear in several extant Hominoidea groups, not only at the subspecies level but also in populations from distinct localities. We also addressed the relation between this variability and ecological, environmental and dietary differences, with a view to explaining these patterns in extant hominoid populations.
Dietary habits and ecology of the African Hominoidea
Although gorillas are not strict leaf-eaters, they are mostly folivorous (Fleagle 1999), except in habitats that do not allow alternative diets, where they will show a preference for soft fruit if available (Rogers et al.1990). Gorillas have highly selective diets, consisting mainly of staple piths, leaves, roots and shoots from abundant monocotyledonous plants, from either firm forests or swampy areas. Their diet also includes seasonal ripe fruits from a wide variety of species and fallback foods, often of lower nutritional quality, such as leaves, bark and fibrous fruits (Rogers et al. 1990, 1994; Remis et al. 2001; Tutin et al. 1997), and in some sites also large amounts of sweet succulent fruits, which account for 51% of total food intake in Bai Hokou (Central Africa Republic) and up to 70% in Mondika (Central African Republic), even when availability is low (Jones and Sabater Pi 1971; Sabater-Pi 1977; Doran and McNeilage 1998; Remis 1997; Tutin et al. 1997). However, gorillas consume many other items year-round, such as leaves, stems, pith, shoots, roots, bark and cambium, phloem of trees or lianas and aquatic herbaceous vegetation (Doran and McNeilage 1998). Distinct geographical groups share many food items, though at varying frequencies (Rogers et al. 2004). In Rio Muni (Equatorial Guinea), Gorilla gorilla gorilla subsists largely on the profuse growth of wild ginger Aframomum by eating its leaves, pith, roots and fruits (Jones and Sabater Pi 1971), and in the Lopé reserve (Gabon), gorillas obtain more than 83% of their food, such as fruits, leaves or bark, directly from trees (Tutin and Fernández 1994), although they live in a mosaic habitat of open savannas and Marantaceae forests (Rogers et al. 2004).
There is no evidence of meat ingestion among gorillas (Sabater-Pi 1977), although insects, mainly Cubitermes and several species of Hymenoptera, are eaten in many localities (Tutin and Fernandez 1983, 1992; Remis 1997; Deblauwe et al. 2003). Sabater-Pi (1960) described a gorilla chewing wax from a subterranean nest of bees. Remis (1997) recorded sex-related differences in diet among gorillas, males being more frugivorous than females during the dry season, but also consuming more abrasive food stuffs, such as bark and grasses or herbs, than females.
The diet of the chimpanzee varies greatly from one population to another and even from one community to the next, not only because of botanical differences but also because of family-related traditional preferences (Estes 1997; Whiten 2007). Chimpanzees occupy tropical forests and dry arboreal savannas. They frequently feed on the ground, walking from one feeding site to another, mainly consuming fruits and nuts, which account for up to 70–80% of their total food intake (Tutin et al. 1997). However, this proportion greatly depends on the population analyzed. Basabose (2002) reported 58% fruit consumption in the Kahuzi chimpanzee population (Pan t. schweinfurthii), whereas in the Democratic Republic of the Congo, for the same subspecies, Tweheyo and Obua (2001) and Tweheyo and Lye (2003) described 83% fruit ingestion at the Budongo Forest Reserve in Uganda. Other studies have reported 87% consumption of fruits and seeds for Pan t. troglodytes (Tutin and Fernández 1993) and 72% for Pan t. verus in Bossou (Sugiyama and Koman 1992), similar to the percentage reported for the Kibale Pan t. schweinfurthii (67%) (Wrangham et al. 1991). Other resources, such as leaves and stems, account for up to 20% of the chimpanzee’s total food intake, depending on the population studied (Estes 1997). McGrew et al. (1988) reported that 20% of the chimpanzee’s diet was comprised by leaves, stems and bark consumption in Mt Assirik (Senegal), similar to 19% in Gombe (Wrahgham 1977) and 19.7% in Budongo (Newton-Fisher 1999). In contrast, only 2.6% of the diet comprised these foods for primates in Kibale (Wrahgham et al. 1996). These studies indicate the variability in the importance of fruit and leaves in the feeding ecology between chimpanzee populations, although part of this variability could be due to differences in the study methodology used, or the effects of seasonality in fruit consumption on the results of short-term studies.
Seasonal shifts in the diet of the chimpanzee have also been described (Fleagle 1999; Sabater-Pi 1979), as well as geographical differences (Whiten 2007). Although savanna chimpanzees are highly dependent on gallery forest or patches of evergreen forests, their diet may also include bark, resins, flowers and seeds (Nishida et al. 2000; Yamakoshi 1998). Moreover, a population of savanna chimpanzees in Ugalla, Tanzania, uses tools to harvest the underground storage organs of several plants in the rainy season (Hernández-Aguilar et al. 2007). Chimpanzees can spend up to 5% of their feeding time consuming animal proteins, mainly in the form of insects (termites, ants, bees and other insect larvae and eggs, caterpillars, leaf galls, etc.) and several mammal species, generally young antelopes and bushpigs, monkeys (Colobus or Papio), bushbabies, nestling birds and eggs (Wrangham 1984), bushbucks, duikers and young baboons (Wrangham and Riss 1990). Predation and hunting behavior in chimpanzee communities has been reported in many localities (Stanford et al. 1994; Newton-Fisher 1999; Boesch 2001).
Materials and methods
Extant Hominoidea specimens studied
Sample sizes of the species and groups analyzed, geographical origin and osteological collections
Subspecies or group
Gorilla g. gorilla
AMNH, NHML, IMAZ, HMCZ
Eq. Guinea and Gabon
Gorilla g. graueri
Democratic Republic of Congo
Pan t. troglodytes
Cameroon, Eq. Guinea, Gabon, Nigeria
AMNH, NHML, IMAZ, MNCN
Pan t. schweintfurthii
Republic of Congo, Tanzania, Uganda
AMNH, NMK, NHML, MRAC
Pan t. verus
Specimen preparation and microwear analysis
Given that scanning electron microscope (SEM) analysis requires the handling of dental specimens, and museum collections must ensure the conservation of their collections, we made casts of the relevant dental specimens. The enamel surfaces were cleaned with pure acetone and ethanol using a cotton earbud to remove chemical preservatives and dust. Molds were obtained with President Microsystem regular body polyvinylsiloxane (Colténe™). In order to standardize data comparisons, a single tooth, the lower left second molar (LM2), was consistently selected and molded as a representative of the buccal microwear pattern of each individual. The impression material, which shows excellent dimensional stability and reproduction detail (Andritsakis and Vlamis 1986; Teaford and Oyen 1989), was applied from the occlusal border to the tooth roots, including the cemento-enamel junction, and from the mesial to the distal borders (Galbany et al. 2004a). Using the molds, a cast was obtained with a stable, two-base component epoxy resin (Epo-Tek 301, from Química del Aditivo), which provides reliable replicas with excellent detail for scientific research (Rose 1983), or with the two-component polyurethane FEROPUR PR-55, which provides the same microscopic detail (Galbany et al. 2004a). The epoxy resin or polyurethane were gently stirred and then put into the molds using a Pasteur pipette. Molds were then centrifuged for 2 min at 2,500 rpm to remove air bubbles in contact with buccal surfaces. Replicas were mounted on SEM stubs and sputter-coated with a 400 Å gold layer for SEM observation. They were then stored in a dust-free cupboard as part of a larger collection (Galbany et al. 2004a, b). Several of the molds analyzed were originally from the MRAC (Royal Museum for Central Africa) and were provided by Peter S. Ungar, who obtained them by following the same procedure. Positive casts were made from these molds using the same methodology. It has been reported that up to four successive replicas from the same mold provide the same quality as the originals (Galbany et al. 2006).
Microwear striations were counted and measured (length in μm and orientation in degrees from 0° to 180° relative to the cemento-enamel junction) within the 0.56 mm2 area by the Sigma Scan ProV (SPSS™ v.15) package. All measurements were done by the same researcher to avoid inter-observer error, thereby implying only intra-observer error, which is smaller than the former (Galbany et al. 2005b). A striation was defined as a linear mark on the enamel surface at least four times longer than its width and with a minimum length of 15 μm, regardless of curvature. All striation angles, relative to the cemento-enamel junction, were measured in degrees and classified into 45° orientation class-groups (Pérez-Pérez et al. 1999): horizontal (H), vertical (V), mesio-distal (MD) and disto-mesial (DM). For each category, as well as for the total number of striations (T), the average number (N), length (X) and standard deviation of the length (S) of all striations were calculated. Thus, a total of 15 variables were derived for each image: NH, XH, SH, NDM, XDM, SDM, NMD, XMD, SMD, NV, XV, SV, NT, XT and ST (number, average length and standard deviation of the length for each orientation category). Kolmogorov–Smirnov normality tests, single-classification ANOVA and discriminant function analyzes were performed with the SPSS v.15 statistical package, and plots were done with Microsoft Excel and Statistica StatSoft©.
Variability of dental microwear in extant Hominoidea
Descriptive statistics of all variables for all subspecies and groups analyzed
G. g. gorilla (Cameroon) n = 31
G. g. gorilla (Nigeria) n = 3
G. g. gorilla (Congo) n = 4
G. g. gorilla (Eq. Guinea) n = 8
G. g. graueri n = 7
Pan t. troglodytes n = 10
Pan t. schweintfurthii n = 9
Pan t. verus n = 7
Moreover, the dispersion plot (Fig. 2) shows how gorillas from Congo, Equatorial Guinea and Gabon, and Nigeria showed the most distinct microwear patterns from all the others. Plots of Pan t. troglodytes and Gorilla gorilla gorilla from Cameroon overlapped greatly, but Pan t. verus, which showed the lowest values for the total number of microstriations, did not. Pan t. schweintfurthii overlapped slightly with Pan t. troglodytes but not with Gorilla gorilla gorilla from Cameroon.
Analysis of variance (ANOVA) of the 15 variables studied for all groups considered
Bonferroni post-hoc test of 15 variables for all groups studied
G. g. g. Congo
G. g. g. Cameroon
G. g. g. Nigeria
G. g. g. Nigeria
G. g. g. Eq. Guinea
Gorilla g. graueri
Pan t. troglodytes
Pan t. schweinfurthii
Pan t. verus
Pan t . verus
G. g. g. Nigeria
G. g. g. Cameroon
G. g. graueri
Pan t. schweinfurthii
Pan t. schweinfurthii
Pan t. schweinfurthii
G. g. g. Eq. Guinea
Pan t. schweinfurthii
Pan t. schweinfurthii
Pan t. verus
G. g. g. Cameroon
G. g. graueri
Pan t. verus
Pan t. schweinfurthii
To work on quantitative variables to characterize dental microwear pattern, here we followed the same methodology as described by Dr. Pérez-Pérez (Pérez-Pérez et al. 1994, 1999, 2003a; Galbany et al. 2004a, 2005a). Like many other semi-automated techniques (Grine et al. 2002; Galbany et al. 2005b), this methodology has some error rates but gives better results than 3-D interferometric microscopy automated analyzes of roughness or texture in enamel surfaces (Estebaranz et al. 2007). However, both manual counting and texture analyzes are used in research on hominid and primate occlusal dental microwear and provide acceptable results (Ungar and Teaford 1996; Organ et al. 2005; Scott et al. 2005; Merceron et al. 2006; Ungar et al. 2008).
Although the samples of extant Hominoidea were selected from restricted distributions and showed geographical differences in diet (Wrangham et al. 1991; Sugiyama and Koman 1992; Tutin and Fernández 1993; Tutin et al. 1997; Remis 1997; Yamakoshi 1998; Newton-Fisher 1999; Tutin 1999; Tweheyo and Obua 2001; Basabose 2002; Doran et al. 2002; Stanford and Nkurunungi 2003; Rogers et al. 2004), the buccal microwear patterns showed great homogeneity compared with other primate groups (Galbany et al. 2005a). ANOVA analyzes between subspecies indicated that 7 of the 15 variables showed significant differences between the subspecies analyzed (Table 3); however, the Bonferoni post-hoc test showed general homogeneity given the overall number of comparisons. The main differences occurred between some variables of Gorilla gorilla gorilla from the Congo, Nigeria, Equatorial Guinea, and Gabon, and a few of the remaining subspecies and groups considered (Table 4). These results are consistent with previous studies on buccal microwear patterns of all Catarrhini that reported no great differences between Hominoidea (Galbany and Pérez-Pérez 2004; Galbany et al. 2005a).
The dispersion two-variable plot and the cladogram show similarities in buccal dental microwear patterns between groups, which may indicate diet abrasiveness and composition. The close relationship between Cameroon gorillas and Pan t. troglodytes and Pan t. schweintfurthii in the single-linkage cluster analysis is consistent with previous preliminary studies which showed a great similarity of dental microwear between these groups (Galbany et al. 2002). Moreover, Cameroon gorillas and Pan t. troglodytes did not show any Bonferroni post-hoc difference. These species are sympatric and exploit food resources in a similar manner. This observation may account for similar buccal dental microwear patterns. Tutin and Fernández (1994) noted that Pan t. troglodytes and Gorilla gorilla gorilla in the Lopé reserve in Gabon share 127 food items, most of them fruit, which amounts to 82% of their total ingested food.
The other Gorilla gorilla gorilla groups analyzed from Congo, Nigeria, Equatorial Guinea and Gabon showed greater differences in dental microwear pattern. They were therefore the most remote groups in the cladogram (Fig. 3), placed far from the rest of the groups in the dispersion plot (Fig. 2). These differences in dental microwear could be caused by a distinct diet composition, as certain geographical and dietary differences have been reported between populations (Rogers et al. 2004). Gorillas from Rio Muni, in Equatorial Guinea, subsist largely on wild ginger Aframomum, especially its leaves, pith, roots and fruits (Jones and Sabater Pi 1971), although this study was neither quantitative nor long-term. In contrast, gorillas from Gabon obtain more than 83% of their food directly from trees and very few items from the ground (Tutin and Fernández 1994). Food items from the upper canopy, at least in Costa Rica, may have a lower density of extrinsic abrasive particles (Ungar et al. 1995), therefore implying less microwear on teeth. In this regard, the buccal surfaces of several populations of baboons have a high density of microwear features (Galbany et al. 2005a). This finding could be attributed to the greater abundance of mineral particles in the savanna soil than in the canopy. These particles are harder than enamel and may be ingested when feeding on food sources on the ground, such as roots or Graminaceae corms (Altmann and Altmann 1970; Alberts et al. 2005; Galbany et al. 2008). Gorillas from Gabon (and also from Congo, as developed further), may therefore have a more abrasive microwear pattern because of extrinsic particles and also abrasive food items, as they live in a mosaic habitat of open savannas and Marantaceae forests that have a dense understore of abrasive grasses of the Marantaceae, Zingiberaceae and Commelinaceae families (White 2001; Rogers et al. 2004). Savanna and Marantaceae forest habitats and the derived feeding ecology of populations from Gabon and Equatorial Guinea may explain the distinct microwear patterns observed on dental enamel.
The differences in dental microwear of gorillas from Congo could also be explained by ecology or environment. Bermejo (1997) noted that Lossi, south of the Odzala National Park, has many savannas and extensive Marantaceae forests. These habitats, the main vegetation links between the Gabonese and Congolese ecosystems and the main difference with other sites, imply a higher number of abrasive particles in the diet, both extrinsically and present in leaves. However, the west Congo basin also includes characteristic forest types such as swamp forest (White 2001). Thus, the diets of gorillas from the Congo basin may differ slightly from those of populations in Equatorial Guinea and Gabon (Rogers et al. 2004), thereby leading to some differences in their dental microwear patterns. It is not only herbaceous species that contribute to dental microwear, but also other common species that serve as fallback foods. However, these slight differences in ecology and diet between these two populations did not appear to cause great differences in dental microwear patterns, as shown by the observation of similar patterns. The overall contribution of swamp food (Cyperaceae or Hydrocharis, for example) in gorillas’ diets is currently unclear because these apes visit swamps sporadically. However, food from swamps may be important fallback foods because of their abundance, nutritional value and mineral content (Kuroda et al. 1996; Doran et al. 2002; Rogers et al. 2004).
Finally, Gorilla gorilla gorilla populations from Nigeria are the farthest west of all groups and show distinct feeding habits, including large amounts of fruit (Rogers et al. 2004). This high fruit consumption could account for some differences in the dental microwear pattern observed between the other gorilla groups, especially their longer total microstriations, although not significantly longer, as also occurs with frugivorous guenons (Cercopithecus sp.), as described elsewhere (Ungar and Teaford 1996; Galbany and Pérez-Pérez 2004; Galbany et al. 2005a).
In chimpanzees, Pan t. verus showed the fewest microstriations in all orientations, although differences were not significant. Nevertheless, this subspecies eats a wide variety of food items, as well as many parts of plants. However, it appears to eat less fruit and more low-quality foods, such as seeds, pods and underground storage organs, than other chimpanzees (McGrew et al. 1988). These results do not fit the remaining analyzes, in which the groups that present more abrasive feeding ecologies showed the most abrasive buccal dental microwear patterns. Nevertheless, the general pattern associates more abrasive diets with greater buccal microwear, although extrinsic abrasive particles deposited on food may also contribute to microwear formation. However, in addition to the toughness of food, which is related to digestibility, many other factors influence food selection by primates (Hill and Lucas 1996). These food preferences could reduce the proportion of abrasive items consumed and affect the microwear features caused by phytoliths. Moreover, other variables, such as the biomechanics of mastication or tooth size, should also be considered when interpreting dental microwear variability between gorillas and chimpanzees. However, a previous study indicates that tooth size does not affect the number or length of microstriations in Hominoidea (Galbany and Pérez-Pérez 2006).
A solid knowledge of buccal dental microwear in African Apes, as in other primate species, and its relation to geographical and ecological variability is essential to interpret the diet of our ancestors, who inhabited similar environments. In this regard, Estebaranz et al. (2009, submitted to J Hum Evol) analyzed the variability of buccal dental microwear pattern in Australopithecus afarensis and its relation to extant Hominoidea species by considering its geographical distribution and diet. These authors gave an interesting interpretation of the feeding ecology of our ancestors. In addition, dental microwear variability of other primate species from distinct habitats, such as baboons, should be analyzed in depth, as they also live in habitats that Australopithecus once occupied. The ecological and feeding data of numerous baboon populations are well documented, such as the Amboseli population (Altmann and Altmann 1970; Altmann et al. 2002; Alberts et al. 2005). To identify the parameters related to the formation of microwear patterns, and also to establish how these patterns can help us to better interpret our ancestors’ diet and ecology, future studies should address the dynamics behind the formation of buccal dental microwear pattern in vivo and its relation to the seasonality of feeding ecology, food proportions and extrinsic abrasive particles, as well as food properties. A study of this kind has been conducted on the Amboseli baboon population, and some preliminary results have been presented (Galbany et al. 2008). Further research on this population will reveal the dietary components that contribute to dental microwear patterns, and the weight of extrinsic particles in this process. Meanwhile, buccal dental microwear in African Hominoidea shows that variability in these patterns are more related to ecological and diet composition than to taxonomy.
This research was funded by the Spanish CGL2004-00775/BTE and CGL-200760802 projects and was supported by the “Departament d’Educació i Universitats de la Generalitat de Catalunya––Beatriu de Pinós 2006.” We thank the institutions that granted permission to study the extant primate specimens and Dr. Peter S. Ungar (University of Arkansas) for lending us his Hominoidea molds taken in the Royal Museum for Central Africa (MRAC) in Tervuren (Belgium). We also thank Núria Garriga (Universitat de Barcelona) and Dr. Alejandro Romero (Universidad de Alicante) for their help in plot generation. Furthermore, thanks go to the two anonymous referees for their reviews and useful comments. All SEM images were obtained at the “Serveis Cientificotècnics” of the Universitat de Barcelona.
- Alberts SC, Hollister-Smith J, Mututua RS, Sayialel SN, Muruthi PM, Warutere JK, Altmann J (2005) Seasonality and long term change in a savannah environment. In: Brockman DK, Van Schaik CP (eds) Primate seasonality: implications for human evolution. Cambridge University Press, London, pp 157–196Google Scholar
- Altmann SA, Altmann J (1970) Baboon ecology: African field research (Bibliotheca Primatologica, vol 12). University of Chicago Press/Karger, Chicago/Basel, pp 144–169Google Scholar
- Bermejo M (1997) Study of western lowland gorillas in the Lossi forest of North Congo and a pilot gorilla tourism plan. Gorilla Conserv News 11:6–7Google Scholar
- Boesch C (2001) Hunting strategies of Gombe and Taï chimpanzees. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, pp 77–91Google Scholar
- Estebaranz F, Galbany J, Martínez LM, Pérez-Pérez A (2007) 3-D Interferometric microscopy applied to the study of buccal enamel microwear. In: Bailey SE, Hublin JJ (eds) Dental perspectives on human evolution. Springer, Berlin, pp 389–401Google Scholar
- Estes RD (1997) The behaviour guide to African mammals. Russel Friedman, Halfway HouseGoogle Scholar
- Fleagle J (1999) Primate adaptation and evolution. Academic, LondonGoogle Scholar
- Galbany J (2006) El patró de microestriació dental de primats Catarrhini: un model ecològic per primats fòssils i homínids. Ph.D. dissertation, Universitat de BarcelonaGoogle Scholar
- Galbany J, Pérez-Pérez A (2004) Buccal enamel microwear variability in Cercopithecoidea primates as a reflection of dietary habits in forested and open savannah environments. Anthropologie 42(1):13–19Google Scholar
- Galbany J, Pérez-Pérez A (2006) Tamaño dental, desgaste oclusal y microestriación dentaria en primates Hominoidea. Rev Esp Antropol Biol 26:9–15Google Scholar
- Galbany J, Martínez LM, Pérez-Pérez A (2002) Variabilidad del patrón de microestriación dentaria en primates Hominoideos: ¿una cuestión de especie o de entorno ecológico? Rev Esp Antropol Biol 23:77–83Google Scholar
- Galbany J, Martínez LM, Pérez-Pérez A (2004a) Tooth replication tecniques, SEM imaging and microwear analysis in primates: methodological obstacles. Anthropologie 42(1):5–12Google Scholar
- Galbany J, Martínez LM, Hiraldo O, Espurz V, Estebaranz F, Sousa M, Martínez López-Amor H, Medina AM, Farrés M, Bonnin A, Bernis C, Turbón D, Pérez-Pérez A (2004b) Teeth: Catálogo de los moldes de dientes de homínidos de la Universitat de Barcelona. Universitat de Barcelona, BarcelonaGoogle Scholar
- Galbany J, Altmann J, Pérez-Pérez A, Alberts SC (2008) Abstract: buccal dental microwear in a living population of baboons from Amboseli (Kenya). Am J Phys Anthropol 135(S46):100Google Scholar
- Grine FE (1987) Quantitative analysis of occlusal microwear in Australopithecus and Paranthropus. Scan Microsc 1:647–656Google Scholar
- Hernández-Aguilar A, Moore J, Pickering T (2007) Savanna chimpanzees use tools to harvest the underground storage organs of plants. Proc Natl Acad Sci USA 104:19210–19213Google Scholar
- Jones C, Sabater Pi J (1971) Comparative ecology of Gorilla gorilla (Savage and Wyman) and Pan troglodytes (Blumenbach) in Rio Muni, West Africa. Bibliogr Primatol 13:1–96Google Scholar
- Kingdon J (2001) The Kingdon field guide to African mammals. Academic, LondonGoogle Scholar
- Kuroda S, Nishihara T, Suzuki S, Oko RA (1996) Sympatric chimpanzees and gorillas in the Ndoki forest, Congo. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 58–70Google Scholar
- Martínez LM, Pérez-Pérez A (2004) Post-mortem wear as indicator of taphonomic processes affecting enamel surfaces of hominin teeth from Laetoli and Olduvai (Tanzania): implications to dietary interpretations. Anthropologie 42(1):37–42Google Scholar
- Martínez LM, López-Amor HM, Pérez-Pérez A (2001) Microestriación dentaria y alteraciones del esmalte dentario en homínidos Plio-Pleistocénicos de Laetoli I Olduvai (Tanzania). Rev Esp Antrop Biol 22:61–72Google Scholar
- McGrew WC, Baldwin PJ, Tutin CEG (1988) Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. Am J Phys Anthropol 16:213–226Google Scholar
- Pérez-Pérez A, Bermúdez de Castro JM, Arsuaga JL (1999) Non-occlusal dental microwear analysis of 300.000 year-old Homo heilderbergensis teeth from Sima de los Huesos (Sierra de Atapuerca, Spain): implications of intrapopulation variability for dietary analysis of hominid fossil remains. Am J Phys Anthropol 108(4):433–457PubMedCrossRefGoogle Scholar
- Pérez-Pérez A, Farrés M, Martínez LM, Martínez López-Amor H, Galbany J (2003b) Correlación entre tamaño dentario y microestriación vestibular en homínidos Pli-Pleistocénicos de Kenia y Tanzania. In: Aluja MP, Malgosa A, Nogués R (eds) Antropología y biodiversidad. Edicions Bellaterra, Barcelona, pp 407–413Google Scholar
- Puech PF (1982) L’usure dentaire de l’homme de Tautavel. In: L’Homo erectus et la place de l’homme de Tautavel parmi les hominides fossiles. In: CNRS (ed) Nice Colloque Internacional du CNRS. CNRS, Paris, pp 249–275Google Scholar
- Puech PF (1986a) Australopithecus afarensis Garusi 1, diversite et specialization des primers hominides d’apres les caracteres maxillo-dentaires. C R Acad Sci Paris Ser II 303:1819–1824Google Scholar
- Puech PF (1986b) Tooth microwear in Homo habilis at Olduvai. Mem Mus Hist Natur Paris Ser C 53:399–414Google Scholar
- Remis MJ (1997) Western lowland Gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J Phys Anthropol 43:87–109Google Scholar
- Remis MJ (2003) Are gorillas vacuum cleaners of the forest floor? The roles of gorilla body size, habitat and food preferences on dietary flexibility and nutrition. In: Taylor AB, Goldsmith ML (eds) Gorilla biology: a multidisciplinary perspective. Cambridge University Press, Cambridge, pp 385–404Google Scholar
- Rogers ME, Maisels F, Williamson EA, Fernández M, Tutin CEG (1990) Gorilla diet in Lope Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339Google Scholar
- Rogers ME, Tutin CEG, Williamson EA, Parnell RJ, Voysey BC, Fernández M (1994) Seasonal feeding on bark by gorillas: an unexpected keystone food? In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds) Ecology and evolution. Universite Louis Pasteur, Strasbourg, pp 37–43Google Scholar
- Rogers ME, Abernethy K, Bermejo M, Cipolletta C, Doran D, McFarland K, Nishihara T, Remis M, Tutin CEG (2004) Western Gorilla diet: a synthesis from six sites. Am J Phys Anthropol 64:173–192Google Scholar
- Romero A, Juan De (2006) Análisis de microdesgaste dentario vestibular bajo dieta ad libitum. Rev Esp Antrop Fís 26:103–108Google Scholar
- Romero A, Martínez-Ruiz N, Amorós A, De Juan J (2003/2004) Microdesgaste dental in vivo: modelo preliminar para interpretar su formación y variabilidad en grupos humanos antiguos. Rev Esp Antrop Fís 24:5–18Google Scholar
- Sabater-Pi J (1960) Beitrag zür biologie del flachlandgorillas (Gorilla gorilla gorilla). Z Säugetierkd 25:133–141Google Scholar
- Sugiyama Y, Koman J (1992) The flora of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13:127–169Google Scholar
- Tutin CEG, Fernández M (1994) Comparison of food processing by sympatric apes in the Lopé Reserve, Gabon. In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds) Ecology and evolution. Universite Louis Pasteur, Strasbourg, pp 29–35Google Scholar
- White LJT (2001) Forest-savanna dynamics and the origins of Marantaceae forest in central Gabon. In: Weber W, White LJT, Vedder A, Naughton-Treves L (eds) African rain forest ecology, conservation. Yale University Press, New Haven, pp 165–182Google Scholar
- Whiten A (2007) Pan African culture: memes and genes in wild chimpanzees. Proc Natl Acad Sci USA 104:17559–17560Google Scholar
- Wrahgham RW (1977) Feeding behaviour of chimpanzees in Gombe national park, Tanzania. In: Cluttin-Brock TH (ed) Primate ecology. Academic, LondonGoogle Scholar
- Wrahgham RW, Chapman CA, Clark-Arcadi AP, Isabirye-Basuta G (1996) Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great apes groups. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, CambridgeGoogle Scholar
- Wrangham RW (1984) Chimpanzees. In: MacDonald DW (ed) The encyclopedia of mammals. Facts on File, Inc., New York, pp 422–427Google Scholar