Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus

Many living primates that feed on hard food have been observed to have thick-enameled molars. Among platyrrhine primates, members of the tribe Pitheciini (Cacajao, Chiropotes, and Pithecia) are the most specialized seed and nut predators, and Cebus apella also includes exceptionally hard foods in its diet. To examine the hypothesized relationship between thick enamel and hard-object feeding, we sectioned small samples of molars from the platyrrhine primates Aotus trivergatus, Ateles paniscus, Callicebus moloch, Cebus apella, Cacajao calvus, Chiropotes satanas, Pithecia monachus, and Pithecia pithecia. We measured relative enamel thickness and examined enamel microstructure, paying special attention to the development of prism decussation and its optical manifestation, Hunter-Schreger Bands (HSB). Cebus apella has thick enamel with well-defined but sinuous HSB overlain by a substantial layer of radial prisms. Aotus and Callicebus have thin enamel consisting primarily of radial enamel with no HSB, Ateles has thin enamel with moderately developed HSB and an outer layer of radial prisms, and the thin enamel of the pitheciins (Cacajao, Chiropotes, and Pithecia) has extremely well-defined HSB. Among platyrrhines, two groups that feed on hard objects process these hard foods in different ways. Cebus apella masticates hard and brittle seeds with its thick-enameled cheek teeth. Pitheciin sclerocarpic foragers open hard husks with their canines but chew relatively soft and pliable seeds with their molars. These results reveal that thick enamel per se is not a prerequisite for hard object feeding. The Miocene hominoid Kenyapithecus may have included hard objects in its diet, but its thick-enameled molars indicate that its feeding adaptations differed from those of the pitheciins. The morphology of both the anterior and posterior dentition, including enamel thickness and microstructure, should be taken into consideration when inferring the dietary regime of fossil species.     

Tooth use and the physical properties of food

For decades, natural historians and comparative anatomists have acknowledged the form/function relationship between an animal's dentition and its food. Historically, anthropologists have cited this relationship to explain adaptations observed in modern species as well as to infer the diets of extinct animals found in the fossil record. Anthropologists have described morphological differences between species that permit dietary niche partitioning which allows closely related primates to co-exist within a single ecosystem. For example, Robinson¹ postulated that the anatomical differences between Australopithecus and Paranthropus are the result of their adaptations to different diets. Jolly's² seed-eating hypothesis suggested that early hominids' morphological divergence from apes resulted from their specialized feeding on small and hard grass seeds. Early work by Kay³ suggested that Sivapithecus' thick molar enamel was an adaptation to habitually eating resistant food items such as hard nuts or seeds enclosed in tough pods.     

Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei

Background

Primates—including fossil species of apes and hominins—show variation in their degree of molar enamel thickness, a trait long thought to reflect a diet of hard or tough foods. The early hominins demonstrated molar enamel thickness of moderate to extreme degrees, which suggested to most researchers that they ate hard foods obtained on or near the ground, such as nuts, seeds, tubers, and roots. We propose an alternative hypothesis—that the amount of phytoliths in foods correlates with the evolution of thick molar enamel in primates, although this effect is constrained by a species'' degree of folivory.

Methodology/Principal Findings

From a combination of dietary data and evidence for the levels of phytoliths in plant families in the literature, we calculated the percentage of plant foods rich in phytoliths in the diets of twelve extant primates with wide variation in their molar enamel thickness. Additional dietary data from the literature provided the percentage of each primate''s diet made up of plants and of leaves. A statistical analysis of these variables showed that the amount of abrasive silica phytoliths in the diets of our sample primates correlated positively with the thickness of their molar enamel, constrained by the amount of leaves in their diet (R² = 0.875; p<.0006).

Conclusions/Significance

The need to resist abrasion from phytoliths appears to be a key selective force behind the evolution of thick molar enamel in primates. The extreme molar enamel thickness of the teeth of the East African hominin Paranthropus boisei, long thought to suggest a diet comprising predominantly hard objects, instead appears to indicate a diet with plants high in abrasive silica phytoliths.     

黑尾蜡嘴雀冬季对树木果实的取食作用

2009年11月至2011年2月,在江苏省南京市观察到黑尾蜡嘴雀冬季取食12种树木的果实及种子。该鸟通常咬破果皮或种皮,取食种子的胚和胚乳等营养物质,为种子捕食者。由于其他一些食果鸟类也同期取食有关树木的果实,并传播其种子,黑尾蜡嘴雀的取食对这些树木的种子传播的影响是有限的。在初冬季节,黑尾蜡嘴雀常在树冠层取食果实,而在深冬季节,则主要在地表取食落果。黑尾蜡嘴雀能够咬碎枫杨等坚果的坚硬果皮,可为一起在地表觅食的麻雀取食种子碎屑物提供便利条件。黑尾蜡嘴雀与麻雀之间的偏利取食关系属于首次报道。文中对于城市环境管理中合理利用树木落果,为黑尾蜡嘴雀等鸟类提供越冬食物等方面提出了相关建议。     

Predation and dispersal of large and small seeds of a tropical palm

Seed size may vary greatly among individuals within plant species. What effects the extremes of this variation have for seeds taken by small mammals are poorly understood. Not all seeds removed by small mammals are necessarily eaten. Small rodents are common seed predators, but they may disperse a significant proportion of seeds by scatter hoarding them via burial. Size-dependent predation and dispersal of seeds has not been directly tested within a plant species for tropical rodents. This study tested whether or not large and small nuts of Astrocaryum mexicanum (Palmae) differed in their fates due to handling by the spiny pocket mouse Heteromys desmarestianus (Heteromyidae). Exclosures were used to give small rodents exclusive access to A. mexicanum nuts. H. desmarestianus preferentially consumed large over small A. mexicanum nuts, but cached (in burrows and by scatter hoarding) similar proportions of these nuts by size. Small nuts tended to be buried farther away from exclosures than large nuts. Although sample sizes of buried nuts were small, the rodents retrieved all buried large nuts, but 30% of the small nuts remained buried long enough to germinate. I also examined predispersal predation by insects and found that insects appear to have no size preference for A. mexicanum nuts, but insect predation appears to hinder nut development. Thus, nuts attacked by insects develop to be significantly smaller, with a low proportion of undamaged endosperm, than uninfested nuts. It is hypothesized that the preferential predation of large A. mexicanum nuts by H. desmarestianus is a response by these rodents to insect predation.     

Long-term variation in fruiting and the food habits of wild Japanese macaques on Kinkazan Island, northern Japan

We studied the relationship between the food habits of Japanese macaques (Macaca fuscata) and the availability of nuts (Fagus crenata, Zelkova serrata, Carpinus spp., and Torreya nucifera) on Kinkazan Island, northern Japan, from 1997 to 2005 to examine the long-term variations in both food habits and availability. The food habits of the monkeys showed clear seasonal changes: the staple foods were woody leaves and flowers in spring (May and June), woody leaves and seeds or fruits other than nuts in summer (July and August), nuts and seeds or fruits other than nuts in fall (September-November), and herbaceous plants in winter (December-April). The availability of nuts, combinations of masting species, and energy production varied among years. Food habits varied among years, but the magnitude of variability of food habits differed among seasons, with large variability during summer and winter, and small variability in spring. Food availability was poor in summer and winter, but in several years the monkeys were able to consume nuts during those seasons. We emphasize the importance of conducting long-term studies on both food availability and the food habits of animals in the temperate zone.     

广西化石猩猩牙齿釉质厚度研究

华南和东南亚发现大量更新世的猩猩牙齿化石。本研究应用CT扫描三维重建的技术方法研究了广西更新世化石猩猩牙齿釉质厚度,并与现生类人猿、现代人、化石类人猿以及早期人类进行比较分析。结果显示:广西猩猩同类牙齿的釉质厚度与牙齿大小相关性很小;臼齿和前臼齿釉质厚度在上下颌之间不存在显著性差异;来自广西不同地区的猩猩化石牙釉质厚度无显著差异。与早期人科成员相比,广西猩猩的牙釉质相对较薄,平均与相对釉质厚度值都明显小于南方古猿、傍人。与早期人属相比,小于直立人、尼人以及非洲和欧洲的早期人属化石。与现代人和现生灵长类相比,广西化石猩猩釉质厚度明显大于大部分猴类和非洲大猿;平均釉质厚度稍大于现生猩猩,而与现代人更为接近;相对釉质厚度小于现代人,而与现生猩猩差异不大,都属于偏厚型釉质。本文讨论了釉质厚度与系统分类演化、食性适应的相关问题,作者推测釉质厚度可能是物种的特征属性,与牙齿功能适应有密切关联。     

Indentation as a technique to assess the mechanical properties of fallback foods

A number of living primates feed part-year on seemingly hard food objects as a fallback. We ask here how hardness can be quantified and how this can help understand primate feeding ecology. We report a simple indentation methodology for quantifying hardness, elastic modulus, and toughness in the sense that materials scientists would define them. Suggested categories of fallback foods—nuts, seeds, and root vegetables—were tested, with accuracy checked on standard materials with known properties by the same means. Results were generally consistent, but the moduli of root vegetables were overestimated here. All these properties are important components of what fieldworkers mean by hardness and help understand how food properties influence primate behavior. Hardness sensu stricto determines whether foods leave permanent marks on tooth tissues when they are bitten on. The force at which a food plastically deforms can be estimated from hardness and modulus. When fallback foods are bilayered, consisting of a nutritious core protected by a hard outer coat, it is possible to predict their failure force from the toughness and modulus of the outer coat, and the modulus of the enclosed core. These forces can be high and bite forces may be maximized in fallback food consumption. Expanding the context, the same equation for the failure force for a bilayered solid can be applied to teeth. This analysis predicts that blunt cusps and thick enamel will indeed help to sustain the integrity of teeth against contacts with these foods up to high loads. Am J Phys Anthropol 140:643–652, 2009. © 2009 Wiley-Liss, Inc.     

Brief communication: Enamel thickness and durophagy in mangabeys revisited

The documentation of enamel thickness variation across primates is important because enamel thickness has both taxonomic and functional relevance. The Old World monkeys commonly referred to as mangabeys have figured prominently in investigations of feeding ecology and enamel thickness. In this article, we report enamel thickness values for four mangabey taxa (Cercocebus atys, Cercocebus torquatus, Lophocebus aterrimus, and Lophocebus albigena), offer revised interpretation of the significance of thick enamel in papionin evolution, and place our new data in a broader comparative framework. Our data indicate that all mangabeys have thick enamel and that the values obtained for Cercocebus and Lophocebus equal or exceed those published for most extant non-human primates. In addition, new field data combined with a current reading of the dietary literature indicate that hard foods make up a portion of the diet of every mangabey species sampled to date. Clarification on the relationship between diet and enamel thickness among mangabeys is important not only because of recognition that mangabeys are not a natural group but also because of recent arguments that explain thick enamel as an evolved response to the seasonal consumption of hard foods.     

Teasing apart the contributions of hard dietary items on 3D dental microtextures in primates

3D dental microtexture analysis is a powerful tool for reconstructing the diets of extinct primates. This method is based on the comparison of fossils with extant species of known diet. The diets of primates are highly diversified and include fruits, seeds, grass, tree leaves, bark, roots, tubers, and animal resources. Fruits remain the main component in the diets of most primates. We tested whether the proportion of fruit consumed is correlated with dental microtexture. Two methods of microtexture analysis, the scale-sensitive fractal analysis (SSFA) and the Dental Areal Surface Texture Analysis (DASTA; after ISO/FDIS 25178-2), were applied to specimens of eight primate species (Alouatta seniculus, Gorilla gorilla, Lophocebus albigena, Macaca fascicularis, Pan troglodytes, Papio cynocephalus, Pongo abelii, Theropithecus gelada). These species largely differ in the mean annual proportion of fruit (from 0 to 90%) in their diet, as well as in their consumption of other hard items (seeds, bark, and insect cuticles) and of abrasive plants. We find the complexity and heterogeneity of textures (SSFA) to correlate with the proportion of fruits consumed. Textural fill volume (SSFA) indicates the proportion of both fruits and other hard items processed. Furthermore, anisotropy (SSFA) relates to the consumption of abrasive plants like grass and other monocots. ISO parameters valley height, root mean square height, material volume, density of peaks, and closed hill and dale areas (DASTA) describe the functional interaction between food items and enamel facets during mastication. The shallow, plastic deformation of enamel surfaces induced by small hard particles, such as phytoliths or dust, results in flat microtexture relief, whereas the brittle, deep fracture caused by large hard items such as hard seeds creates larger relief.     

Fruit Removal and Natural Seed Dispersal of the Brazil Nut Tree (Bertholletia excelsa) in Central Amazonia,Brazil

Experimental approaches to study seed dispersal of the Brazil nut tree have hitherto relied on exposed seeds deposited on the forest floor. Here we use a new method to study the natural dispersal by large rodents such as agoutis; tracking experimentally manipulated and tagged fruits containing individually marked seeds. Fruit manipulation did not deter agoutis from handling fruits. We found that agoutis usually moved intact fruits away from their original location below the parent tree before either hiding them or gnawing through the pericarp to access the seeds inside. Most fruits were moved to distances of 15–30 m from their original position, but some fruits could be taken as far as 60 m. A large number of seeds extracted from manipulated fruits appeared to be eaten immediately. Only 27 out of 1740 experimental seeds were found buried in shallow caches, generally within 5 m of the opened fruit. Fruit removal distance accounted for a disproportionate amount of total seed movement and seeds in the current study were dispersed significantly farther than in a previous experiment using exposed seeds, suggesting that classic dispersal experiments of this character may severely underestimate seed dispersal distances. We therefore conclude that the new method provides a more realistic and accurate approach to investigate natural seed dispersal of Brazil nuts and that the removal of fruits from underneath parent trees before being opened is the key to the significantly increased distances at which seeds are dispersed. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Tooth chipping can reveal the diet and bite forces of fossil hominins

Mammalian tooth enamel is often chipped, providing clear evidence for localized contacts with large hard food objects. Here, we apply a simple fracture equation to estimate peak bite forces directly from chip size. Many fossil hominins exhibit antemortem chips on their posterior teeth, indicating their use of high bite forces. The inference that these species must have consumed large hard foods such as seeds is supported by the occurrence of similar chips among known modern-day seed predators such as orangutans and peccaries. The existence of tooth chip signatures also provides a way of identifying the consumption of rarely eaten foods that dental microwear and isotopic analysis are unlikely to detect.     

Brief communication: a preliminary study on the influence of physical fruit traits on fruit handling and seed fate by white-handed Titi monkeys (Callicebus lugens)

Callicebus and the pitheciins are closely related; however, differences in their diets and dental morphology suggest that they differ in the use of mechanically protected food. We describe physical traits of fruits consumed by white-handed titi monkeys (Callicebus lugens) and determine their influence on fruit part selection and immediate seed fate after fruit handling. We tested two hypotheses about the effects of mechanical fruit traits on fruit part selection and seed fate: (1) fruits selected for seed consumption are harder than fruits selected for their fleshy parts and (2) consumed seeds are softer than seeds with other fates. In addition, we analyzed the influence of other physical fruit traits on fruit part selection and seed fate. C. lugens included 69 species in its diet, from which it mainly consumed their fleshy parts. It also consumed seeds, alone or with fleshy fruit parts, but most of them ended up close to parent trees after being dropped or spat out. The first hypothesis was supported while the second was rejected, indicating that C. lugens tends to rely on hard fruits for obtaining seeds, while seed hardness had no influence on fruit part selection and seed fate, contrasting with the pattern reported for Pithecia and Chiropotes in other studies. Ripeness was the most influential factor for fruit part and seed fate discrimination. Results suggest a tendency to sclerocarpic foraging in C. lugens when feeding on seeds.     

Dietary reconstruction of the Amphipithecidae (Primates, Anthropoidea) from the Paleogene of South Asia and paleoecological implications

The primate family, Amphipithecidae, lived during the early Cenozoic in South Asia. In this study, the diet of late middle Eocene amphipithecids from the Pondaung Formation (Central Myanmar) is characterized using three different approaches: body mass estimation, shearing quotient quantification and dental microwear analysis. Our results are compared with other Paleogene amphipithecids from Thailand and Pakistan, and to the other members of the primate community from the Pondaung Formation. Our results indicate a majority of frugivores within this primate community. Pondaungia and “Amphipithecus” included hard objects, such as seeds and nuts, in their diet. Folivory is secondary for these taxa. Myanmarpithecus probably had a mixed diet based on fruit and leaves. Contrasting results and a unique dental morphology distinguish Ganlea from other amphipithecids. These render interpretation difficult but nevertheless indicate a diet tending towards leaves and fruit. However, the anterior dentition of Ganlea suggests that this taxon engaged in seed predation, using its protruding canine as a tool to husk hard fruits and obtain the soft seeds inside. Bahinia and Paukkaungia, two other Pondaung primates, are small (<500 g) and therefore would have depended on insects as their source of protein. As such, they occupied a very different ecological niche from Pondaung amphipithecids. This primate community is then compared with the Eocene-Oligocene primate communities of the Fayum from North Africa. Similarities between the late middle Eocene Pondaung primate community and extant equatorial and tropical South American primate communities are noted.     

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.     

Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii

The divergent molar characteristics of Pan troglodytes and Pongo pygmaeus provide an instructive paradigm for examining the adaptive form-function relationship between molar enamel thickness and food hardness. Although both species exhibit a categorical preference for ripe fruit over other food objects, the thick enamel and crenulated occlusal surface of Pongo molar teeth predict a diet that is more resistant to deformation (hard) and fracture (tough) than the diet of Pan. We confirm these predictions with behavioral observations of Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii in the wild and describe the mechanical properties of foods utilized during periods when preferred foods are scarce. Such fallback foods may have exerted a selective pressure on tooth evolution, particularly molar enamel thinness, which is interpreted as a functional adaptation to seasonal folivory and a derived character trait within the hominoid clade. The thick enamel and crenulated occlusal surface of Pongo molars is interpreted as a functional adaptation to the routine consumption of relatively tough and hard foods. We discuss the implications of these interpretations for inferring the diet of hominin species, which possessed varying degrees of thick molar enamel. These data, which are among the first reported for hominoid primates, fill an important empirical void for evaluating the mechanical plausibility of putative hominin food objects.     

Physical and chemical properties of fruit and seeds eaten byPithecia andChiropotes in Surinam and Venezuela

Pithecia pithecia andChiropotes satanas are seed predators that eat fruits with hard pericarps. We measured resistance to puncturing and crushing of fruit and seeds eaten by these two pitheciins at two localities: in evergreen rain forest at Raleighvallen-Voltzberg, Surinam, and in tropical dry/transitional moist forest on islands in Guri Lake, Venezuela. Average measurements of pericarp hardness were similar at both sites for fruit eaten byChiropotes, but a higher maximum value was obtained at the rainforest site.Chiropotes andPithecia both ate fruits that had harder pericarps than did fruits eaten byAteles paniscus, but crushing resistances of seeds eaten were lower than values forAteles. Thus, both pitheciins selected fruits with hard pericarps and soft seeds, although there were notable intergeneric differences in hardness of fruit ingested. When fruit became scarce,Pithecia ate more flowers, whileChiropotes continued to eat fruits with hard seed coverings. Chemical analysis of species of seeds eaten byPithecia suggests that they avoided seeds with extremely high tannin levels, though they tolerated moderate tannin levels in combination with high levels of lipids. We propose that sclerocarpic harvesting (the preparation and ingestion of fruit with a hard pericarp) allows pitheciin monkeys to obtain nutritious seeds, with reduced tannins, that are softer than those ingested by other frugivores.Presented at XIIIth Congress, International Primatological Society, July 27, 1990.     

Tooth Chipping as a Tool to Reconstruct Diets of Great Apes (Pongo, Gorilla, Pan)

Most methods of dietary reconstruction are limited in their applicability to either extant or extinct taxa. We apply and discuss a method in which dietary information can be reconstructed from chips in the tooth enamel of both living and fossil primates. Such chips can be used to indicate the presence of large hard foods in the diet, and also to provide an estimate of the bite force that was used when the chip was created. Furthermore, the equations derived from this method allow an estimate of maximum bite force to be obtained from a simple measurement of tooth size. We use this method to investigate dietary differences in nonhuman great apes (Pongo, Gorilla, Pan). The high frequency of chips on teeth of Pongo indicate that they frequently use high forces to process hard foods such as seeds and nuts. Gorilla can generate even higher bite forces, but their low incidence of tooth chips suggests that they do so when consuming soft but tough foods. Tooth chips provide a lasting dietary signal that is not easily masked or erased, making them particularly useful for the study of rarely eaten items such as some fallback foods.     

How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals

Some plants that are dispersed by scatter-hoarding animals appear to have evolved the ability to manipulate the behaviour of those animals to increase the likelihood that seeds and nuts will be stored and that a portion of those items will not be recovered. Plants have achieved this in at least four ways. First, by producing large, nutritious seeds and nuts that are attractive to animals and that stimulate hoarding behaviour. Second, by imposing handling costs that cause animals to hoard rather than to eat items immediately. These handling costs can take one of two forms: physical barriers (e.g. hard seed coats) that take time to remove and secondary chemicals (e.g. tannins) that impose metabolic costs. Third, by masting, where a population of plants synchronizes reproductive effort, producing large nut crops at intervals of several years. Mast crops not only satiate seed predators, but also increase the amount of seed dispersal because scatter-hoarding animals are not easily satiated during caching (causing animals to store more food than they can consume) but are satiated during cache recovery. And fourth, by producing seeds that do not emit strong odours so that buried seeds are less likely to be discovered. These, and perhaps other, traits have increased the relative success of plant species with seeds dispersed by scatter-hoarding animals.     

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.