Diets of fossil primates from the Fayum Depression of Egypt: a quantitative analysis of molar shearing

Over the last 90 years, Eocene and Oligocene aged sediments in the Fayum Depression of Egypt have yielded at least 17 genera of fossil primates. However, of this diverse sample the diets of only four early Oligocene anthropoid genera have been previously studied using quantitative methods. Here we present dietary assessments for 11 additional Fayum primate genera based on the analysis of body mass and molar shearing crest development. These studies reveal that all late Eocene Fayum anthropoids were probably frugivorous despite marked subfamilial differences in dental morphology. By contrast, late Eocene Fayum prosimians demonstrated remarkable dietary diversity, including specialized insectivory (Anchomomys), generalized frugivory (Plesiopithecus), frugivory+insectivory (Wadilemur), and strict folivory (Aframonius). This evidence that sympatric prosimians and early anthropoids jointly occupied frugivorous niches during the late Eocene reinforces the hypothesis that changes in diet did not form the primary ecological impetus for the origin of the Anthropoidea. Early Oligocene Fayum localities differ from late Eocene Fayum localities in lacking large-bodied frugivorous and folivorous prosimians, and may document the first appearance of primate communities with trophic structures like those of extant primate communities in continental Africa. A similar change in primate community structure during the Eocene-Oligocene transition is not evident in the Asian fossil record. Putative large anthropoids from the Eocene of Asia, such as Amphipithecus mogaungensis, Pondaungia cotteri, and Siamopithecus eocaenus, share with early Oligocene Fayum anthropoids derived features of molar anatomy related to an emphasis on crushing and grinding during mastication. However, these dental specializations are not seen in late Eocene Fayum anthropoids that are broadly ancestral to the later-occurring anthropoids of the Fayum's upper sequence. This lack of resemblance to undisputed Eocene African anthropoids suggests that the "progressive" anthropoid-like dental features of some large-bodied Eocene Asian primates may be the result of dietary convergence rather than close phyletic affinity with the Anthropoidea.     

Femoral anatomy of Aegyptopithecus zeuxis,an early Oligocene anthropoid

Three partial femora from Quarries I and M of the early Oligocene Jebel Qatrani Formation in the Fayum of Egypt are attributed to Aegyptopithecus zeuxis on the basis of their appropriate size and anthropoid morphology. Compared with extant catarrhines, Aegyptopithecus is unusual in having a distinct gluteal tuberosity (third trochanter) and a relatively deep distal femoral articulation. In the estimated neck angle, Aegyptopithecus resembles arboreal quadrupeds rather than either leaping or suspensory primates. It seems likely that the femur of this species was relatively robust and short for its body mass. In aspects of its femoral anatomy, Aegyptopithecus is quite different from the parapithecid Apidium and more similar to Catopithecus from late Eocene deposits of the Fayum, and also to small hominoids from the Miocene of East Africa. Am J Phys Anthropol 106:413–424, 1998. © 1998 Wiley-Liss, Inc.     

The generic classification of Fayum anthropoidea

The early anthropoid species initially described asAegyptopithecus zeuxis Simons, 1965, from the Oligocene of Egypt, although retained by many authors in the monotypic genusAegyptopithecus, has been lumped by others into the genusPropliopithecus. Similarly, the species originally described asParapithecus grangeri Simons, 1974, has been ranked by some authors in a monotypic genusSimonsius, while others retain it inParapithecus. Criteria to be considered in resolving these taxonomic debates are (1) the adequacy and consistency of proposed morphological differences between species; (2) analogy with the degree of morphological variation tolerated within extant genera; and (3) nomenclatural conservatism. A philosophy that would require strict monophyletic classification is of insufficient practical value for assessing the validity of Fayum genera. Characters cited as distinguishing vetweenAegyptopithecus andPropliopithecus, and betweenSimonsius andParapithecus, are reviewed and evaluated. The results indicate thatA. zeuxis is generically distinct from species ofPropliopithecus, based on differences in the crown structure and proportions of the molars.Pa. grangeri cannot be shown to differ at the generic level from the type and only known specimen ofPa. fraasi, thus establishing Simonsius as a junior synonym ofParapithecus.     

Anatomy of the bony pelvis in parapithecid primates

Four partial innominate bones, attributed to the parapithecid primates Parapithecus grangeri and Apidium phiomense, have recently been recovered from Oligocene deposits in the Fayum of Egypt. These fossils provide the first documentation of pelvic morphology for early anthropoids. In pelvic anatomy, parapithecids show definite similarities to higher primates rather than to prosimians, but cannot be clearly allied with any one extant group. Functionally, the fossils indicate quadrupedal or leaping habits rather than suspensory or bipedal behaviors.     

The humerus of Aegyptopithecus zeuxis: a primitive anthropoid

Two complete humeri of Aegyptopithecus zeuxis have been recovered from Oligocene deposits in the Fayum Province of Egypt. These new specimens support previous interpretations of the locomotor adaptations of this species and indicate that A. zeuxis was a robust, slowly moving arboreal quadruped. While the previously described distal articular region of the humerus is virtually identical with the same region in many extant ceboids and the Miocene hominoid Pliopithecus vindobonensis, the more proximal parts of the humerus show many primitive "prosimianlike" features not found the limbs of extant anthropoids. The primitive features include the absence of a distinct deltoid plane, a broad shallow bicipital groove, a large brachialis flange, and an entepicondylar foramen. In most features, the humerus of Aegyptopithecus zeuxis is more primitive than the hypothetical last common ancestor of extant cercopithecoids and hominoids based on neontological comparisons. This supports other lines of evidence indicating that the hominoids from the Egyptian Oligocene are morphologically ancestral to both Old World monkeys and apes.     

New early Eocene anaptomorphine primate (Omomyidae) from the Washakie Basin,Wyoming, with comments on the phylogeny and paleobiology of anaptomorphines

Recent paleontological collecting in the Washakie Basin, southcentral Wyoming, has resulted in the recovery of over 100 specimens of omomyid primates from the lower Eocene Wasatch Formation. Much of what is known about anaptomorphine omomyids is based upon work in the Bighorn and Wind River Basins of Wyoming. This new sample documents greater taxonomic diversity of omomyids during the early Eocene and contributes to our understanding of the phylogeny and adaptations of some of these earliest North American primates. A new middle Wasatchian (Lysitean) anaptomorphine, Anemorhysis savagei, n. sp., is structurally intermediate between Teilhardina americana and other species of Anemorhysis and may be a sister group of other Anemorhysis and Trogolemur. Body size estimates for Anemorhysis, Tetonoides, Trogolemur, and Teilhardina americana indicate that these animals were extremely small, probably less than 50 grams. Analysis of relative shearing potential of lower molars of these taxa indicates that some were primarily insectivorous, some primarily frugivorous, and some may have been more mixed feeders. Anaptomorphines did not develop the extremes of molar specialization for frugivory or insectivory seen in extant prosimians. Incisor enlargement does not appear to be associated with specialization in either fruits or insects but may have been an adaptation for specialized grooming or food manipulation. © 1994 Wiley-Liss, Inc.     

Paleobiology of the oligopithecines,the earliest known anthropoid primates

Anthropoid primates of the subfamily Oligopithecinae are late Eocene in age, and have a known distribution of Northeast Africa and the Arabian Peninsula. Body sizes of the three known oligopithecine species are estimated from allometric molar size regressions to be 700–1000 g forOligopithecus savagei, 600–900 g forCatopithecus browni, and 500 g for the least well-known and smallest species,Proteopithecus sylviae. Occlusal features of the molar teeth, considered in conjunction with body size, suggest that all three species were frugivorous and insectivorous. The orbital size ofCatopithecus indicates a diurnal activity cycle. A relatively broad interobital region in this species may indicate prosimian-like or callitrichid-like olfactory adaptations. Structural features of the crushed skull suggest thatCatopithecus had a smaller cranial capacity than those of extant anthropoids with a similar body size. Fossil plants and birds from localities yielding oligopithecines suggest a wet, warm, tropical, forested, swampy environment. These paleobiological inferences about the extinct oligopithecines are discussed in relation to questions about primate adaptations near the prosimian-anthropoid transition.     

The Fayum primate forest: Did it exist?

The primates have the reputation of being essentially arboreal, forest-adapted animals. Yet there are many genera and species that inhabit an extremely wide array of non-forest habitats. Nevertheless, palaeoprimatologists often tend to depict fossil primate habitats as being more arboreal and more forest-like than is justified by the facts. It is worthwhile, therefore, to reconsider some current interpretations. In this paper, evidence of the Fayum Oligocene primate deposits are reviewed and discussed. The following conclusions emerge:(1) The large number of primate species indicates that the Fayum ecosystem was an optimum or near-optimum habitat for primates. (2) The lithological characteristics point to a sahélien type of climate. (3) The calcified and silicified root systems, having diameters up to 4 cm, suggest a sahélien type of shrub, bushland and/or small-tree vegetation. (4) The large fossilized logs cannot have grown on the spot and apparently represent driftwood from a more humid climatic belt in the south, as is indicated by damage resulting from fluvial transportation and by palaeobotanical data. (5) There may have been some minor patches or strips of medium-height forests and/or wood-lands in the Fayum delta, but there is no evidence of these.Thus the tall forest in which the earliest known African primates are currently supposed to have lived probably never existed. Grounds for this conclusion were presented by Unger 121 years ago, by Beadnell 75 years ago and by Kräusel 41 years ago, but sank into oblivion. The classic image of the primates as arboreal specialists seems to have interfered with seeing the facts. However, more extensive verification of the evidence by means of palaeobotanical research is still required. The fossil material to do so is readily available.     

Molar microwear in extant small-bodied faunivorous mammals: An analysis of feature density and pit frequency

This study quantitatively examined molar microwear in nine species of extant small-bodied faunivorous primates and microchiropterans. Comparative analyses were performed within the food category faunivory, both between hard- and soft-object feeding faunivores and between primarily insectivorous and carnivorous taxa. Additionally, microwear in faunivores was compared to that reported in the literature for frugivorous and folivorous primates. The results indicated that although insectivores and carnivores could not be distinguished by microwear analyses, hard-object faunivores (i. e., those that primarily consume beetles or actively comminute bone) can be readily distinguished from soft-object faunivores (i. e., moth, caterpillar, or vertebrate flesh specialists). The hard-object faunivores consistently exhibited greater pit frequencies (in excess of 40%). Furthermore, comparisons of these microwear data on faunivorous mammals to previous work on frugivorous and folivorous primates (Teaford, 1988, pers. comm.; Teaford and Runestad, 1992, pers. comm.; Teaford and Walker: American Journal of Physical Anthropology 64:191–200, 1984) permitted three observations to be made. 1) Faunivores tend to have higher mean feature densities than either frugivores or folivores, although these differences are not consistently statistically distinct. 2) Faunifores and frugivores that feed on hard-objects have comparable mean pit frequencies. 3) Although it is impossible to distinguish faunivores and folivores on the basis of metric analysis of gross molar morphology, this distinction can be made on microwear criteria. Both hard- and soft-object faunivores exhibit much higher mean pit frequencies than primarily folivorous species. © 1993 Wiley-Liss, Inc.     

The stuttgart collection of oligocene primates from the fayum province of Egypt

In 1907, R. Markgraf made a small collection of Oligocene fossil primates from Egypt for the Staatliches Museum für Naturkunde in Stuttgart. Circumstances of discovery suggest that this collection came from the same stratigraphic horizon (the Upper Fossil Wood zone) and possibly the same locality as a similar collection made earlier that year byMarkgraf for the American Museum of Natural History in New York. Three new genera and species were described bySchlosser, based on the Stuttgart collection.Parapithecus fraasi Schlosser is a junior synonym ofApidium phiomense Osborn. “Parapithecus“grangeri Simons is placed in the new genusSimonsius. Propliopithecus haeckeli Schlosser andMoeripithecus markgrafi Schlosser have previously been recognized as synonyms. In addition,Aegyptopithecus zeuxis Simons is known from the Upper Fossil Wood zone.     

Tooth Wear Difference Between the Yuanmou Hominoid and <Emphasis Type="Italic">Lufengpithecus</Emphasis>

The Late Miocene hominoids recovered from Lufeng (Lufengpithecus) and Yuanmou of Yunnan Province, China, are among the most numerous hominoid fossils in Eurasia. They have yielded critical evidence for the evolutionary history, biogeography and paleobiology of Miocene hominoids. We examined and compared the wear pattern and differences of 804 molars of the Yuanmou hominoid and Lufengpithecus. Our results indicate that both the upper and lower molars of the Yuanmou hominoids were more heavily worn than those of Lufengpithecus. The wear patterns of the individual molars between the Yuanmou hominoid and Lufengpithecus also are different. The heaviest wear of lower molars of the Yuanmou hominoid occur in M₂, followed by M₁ and M₃. In Lufengpithecus, M₁ and M₃ were more heavily worn than M₂. There are differences in wear between the upper and lower molars for the two hominoids. Among the various factors related to tooth wear, we suggest that the main reason for the tooth wear differences between the Yuanmou hominoid and Lufengpithecus may be that they had different diets. More soft dietary items like leaves and berries were probably consumed by Lufengpithecus, and the Yuanmou hominoid may mainly have feed on harder or frugivorous diets. This result complements findings from previous studies of tooth size proportion, and the development of lower molar shearing crests in the 2 samples. Enamel thickness, living environment, behavior patterns, and population structure also might account for dental wear differences between the Yuanmou hominoid and Lufengpithecus.     

Puncture marks on early African anthropoids

Field studies of living primates have shown that primate predation is a rare event. This must also have been true for past primate communities. In the Fayum Oligocene of Egypt, specimens of all four species of Upper Fossil Wood Zone primates show evidence of tooth puncture marks. Of the four potential groups of primate predators--the snakes, the raptors, the crocodiles, and the primitive carnivores or creodonts--only the crocodiles and the creodonts could have made these puncture marks. When one compares the feeding habits of living crocodiles and mammalian carnivores with the evidence from the Fayum, it appears that the Fayum primates were preyed upon and/or scavenged by mammalian carnivore-like animals. The dismemberment of the Fayum primates by Oligocene predators indicates, in part, why the Fayum fossil material is rarely articulated. Bone damage by predators may well set limits on what bone associations can be discovered in the Fayum even before the bones are scattered and buried by depositional processes.     

Dentition ofSivaladapis nagrii (Adapidae) from the late Miocene of India

Two genera and three species of adapid primates are known from the middle and late Miocene of India and Pakistan. Most fossil specimens are fragmentary, but the best-known species, Sivaladapis nagrii,is now represented by enough specimens to permit composite reconstruction of much of the dentition. The incisors of Sivaladapishave spatulate crowns, and the canines are large, projecting teeth. Premolars and molars exhibit complex occlusion involving simultaneous approximation of pointed leading cusps on upper and lower molars, with linear trailing lophs. The premolar eruption sequence in Sivaladapisappears to be P ₂-P₄-P₃, as in most extant prosimians. Symphyseal fusion of the mandibular rami occurred early in ontogeny, before the eruption of any of the anterior permanent teeth. We interpret Sivaladapisto have been a specialized arboreal folivore that became extinct near the end of the Miocene, when the distribution of forests was increasingly restricted and colobine monkeys first invaded South Asia.     

The Role of Fruits and Insects in the Nutrition of Frugivorous Bats: Evaluating the Use of Stable Isotope Models1

We estimated the relative contribution of fruits and insects as sources of dietary protein in two species of Neotropical frugivorous bats (Artibeus jamaicensis and Sturnira lilium) using stable carbon and nitrogen isotope analyses. An insectivorous species (Pteronotus parnellii) was also included for comparison. We found constant patterns in stable carbon and nitrogen isotope composition in blood that separated the two species of frugivorous bats from the insectivorous bat. When we used these isotopic values (combined with those of dietary fruits and insects) to estimate the percent contribution of fruits and insects to the diet of the bats, we obtained different results, depending on assumptions and model adopted. We tested models using both 8“N and 8′³C results simultaneously and separately and further used diet‐tissue fractionation factors of 3%o for nitrogen and 1 and 3.5%o for carbon. We found that a carbon‐based model with a diet‐blood enrichment factor of 3.5%o produced the most parsimonious results. The model estimated that A. jamaicensis and S. lilium obtained most of their protein requirements from fruits, whereas P. parnellii fed mostly on insects. No sexual or seasonal variations in the diet of the two frugivorous species were detected. We found no evidence that the diet of sexually active females differed from that of nonsexually active females in the two species of frugivorous bats. We suggest that future studies better define isotopic fractionation between diet and tissues of bats using captive rearing and controlled diets.     

Differential habitat use byCebus apella andSaimiri sciureus in central surinam

Cebus apella, the black-capped or tufted capuchin, andSaimiri sciureus, the squirrel monkey, are frequently found in mixed species feeding and foraging groups throughout tropical South America and have been reported previously to show marked differences in techniques of insect foraging. Individuals of these taxa observed in central Surinam show numerous additional species-specific differences in other aspects of habitat utilization including gross dietary preferences, utilization of forest strata, locomotor behavior and arboreal support preferences.Cebus apella is more frugivorous, frequents the middle and lower levels of the main canopy, is predominantly quadrupedal and moves on medium-sized arboreal supports. By contrast, the smallerSaimiri sciureus is more insectivorous, frequents the lower strata of the forest, is more saltatory and moves on the smallest arboreal supports. Many of these differences in habitat use are interrelated and accord with patterns of habitat use seen in other primate taxa. The differences betweenCebus apella andSaimiri sciureus also accord with the types of behavioral differences frequently associated with differences in body size.     

A new species of Propliopithecus from the Fayum, Egypt

Propliopithecus ankeli is described as a new species of hominoid from the early Oligocene of Egypt. The new species occurs at a stratigraphic level 80 m below quarries yielding P. chirobates and Aegyptopithecus zeuxis. P. ankeli differs from other species of the genus in its large size, relatively robust canines, larger and proportionally broader premolars, and M1 that has as great or greater mesiodistal length than M2. Thus, P. ankeli is characterized by increased relative size and robustness of the antemolar dentition, which contrasts with the pattern observed in the Fayum's other large hominoid, A. zeuxis. P. ankeli probably represents a lineage not ancestral to other Fayum hominoids. Discovery of this new species emphasizes the diversity of anthropoid primates that had already evolved by the early Oligocene.     

Subchondral Bone Apparent Density and Locomotor Behavior in Extant Primates and Subfossil Lemurs <Emphasis Type="Italic">Hadropithecus</Emphasis> and <Emphasis Type="Italic">Pachylemur</Emphasis>

We analyze patterns of subchondral bone apparent density in the distal femur of extant primates to reconstruct differences in knee posture, discriminate among extant species with different locomotor preferences, and investigate the knee postures used by subfossil lemur species Hadropithecus stenognathus and Pachylemur insignis. We obtained computed tomographic scans for 164 femora belonging to 39 primate species. We grouped species by locomotor preference into knuckle-walking, arboreal quadruped, terrestrial quadruped, quadrupedal leaper, suspensory and vertical clinging, and leaping categories. We reconstructed knee posture using an experimentally validated procedure of determining the anterior extent of the region of maximal subchondral bone apparent density on a median slice through the medial femoral condyle. We compared subchondral apparent density magnitudes between subfossil and extant specimens to ensure that fossils did not display substantial mineralization or degradation. Subfossil and extant specimens were found to have similar magnitudes of subchondral apparent density, thereby permitting comparisons of the density patterns. We observed significant differences in the position of maximum subchondral apparent density between leaping and nonleaping extant primates, with leaping primates appearing to use much more flexed knee postures than nonleaping species. The anterior placement of the regions of maximum subchondral bone apparent density in the subfossil specimens of Hadropithecus and Pachylemur suggests that both species differed from leaping primates and included in their broad range of knee postures rather extended postures. For Hadropithecus, this result is consistent with other evidence for terrestrial locomotion. Pachylemur, reconstructed on the basis of other evidence as a committed arboreal quadruped, likely employed extended knee postures in other activities such as hindlimb suspension, in addition to occasional terrestrial locomotion.     

Molar enamel thickness in European Miocene and extant hominoidea

Based on a roentgenographic analysis, the molar enamel of certain European Miocene dryopithecines is absolutely thick (r=1.03–1.30 mm in thickness); the molar enamel of certain European pliopithecines is thin (r=0.32–0.82 mm thick). The rank order for enamel thickness in extant hominoids (from thickest to thinnest) is confirmed to beHomo, Pongo, Gorilla, Pan, andHylobates. There is a great deal of enamel thickness variability within the great ape sample. Extant analogues suggest that dryopithecines were probably adapted to a frugivorous/gramnivorous dietary regimen, while pliopithecines were probably better suited to folivory.