Osteological evidence for the evolution of activity pattern and visual acuity in primates.

Examination of orbit size and optic foramen size in living primates reveals two adaptive phenomena. First, as noted by many authors, orbit size is strongly correlated with activity pattern. Comparisons of large samples of extant primates consistently reveal that nocturnal species exhibit proportionately larger orbits than diurnal species. Furthermore, nocturnal haplorhines (Tarsius and Aotus) have considerably larger orbits than similar-sized nocturnal strepsirrhines. Orbital hypertrophy in Tarsius and Aotus accommodates the enormously enlarged eyes of these taxa. This extreme ocular hypertrophy seen in extant nocturnal haplorhines is an adaptation for both enhanced visual acuity and sensitivity in conditions of low light intensity. Second, the relative size of the optic foramen is highly correlated with the degree of retinal summation and inferred visual acuity. Diurnal haplorhines exhibit proportionately larger optic foramina, less central retinal summation, and much higher visual acuity than do all other primates. Diurnal strepsirrhines exhibit a more subtle but significant parallel enlargement of the optic foramen and a decrease in retinal summation relative to the condition seen in nocturnal primates. These twin osteological variables of orbit size and optic foramen size may be used to draw inferences regarding the activity pattern, retinal anatomy, and visual acuity of fossil primates. Our measurements demonstrate that the omomyiforms Microchoerus, Necrolemur, Shoshonius, and Tetonius, adapiform Pronycticebus, and the possible lorisiform Plesiopithecus were likely nocturnal on the basis of orbit diameter. The adapiforms Leptadapis, Adapis, and Notharctus, the phylogenetically enigmatic Rooneyia, the early anthropoids Proteopithecus, Catopithecus, and Aegyptopithecus, and early platyrrhine Dolichocebus were likely diurnal. The activity pattern of the platyrrhine Tremacebus is obscure. Plesiopithecus, Pronycticebus, Microchoerus, and Necrolemur probably had eyes that were very similar to those of extant nocturnal primates, with a high degree of retinal summation and rod-dominated retinae. Leptadapis and Rooneyia likely had eyes similar to those of extant diurnal strepsirrhines, with moderate degrees of retinal summation, a larger cone:rod ratio than in nocturnal primates, and, more speculatively, well-developed areae centrales similar to those of diurnal strepsirrhines. Adapis exhibited uncharacteristically high degrees of retinal summation for a small-eyed (likely diurnal) primate. None of the adapiform or omomyiform taxa for which we were able to obtain optic foramen dimensions exhibited the extremely high visual acuity characteristic of extant diurnal haplorhines.

Revised geochronology of the Casamayoran South American Land Mammal Age: climatic and biotic implications.

Isotopic age determinations (40Ar/39Ar) and associated magnetic polarity stratigraphy for Casamayoran age fauna at Gran Barranca (Chubut, Argentina) indicate that the Barrancan "subage" of the Casamayoran South American Land Mammal "Age" is late Eocene, 18 to 20 million years younger than hitherto supposed. Correlations of the radioisotopically dated magnetic polarity stratigraphy at Gran Barranca with the Cenozoic geomagnetic polarity time scale indicate that Barrancan faunal levels at the Gran Barranca date to within the magnetochronologic interval from 35.34 to 36.62 megannums (Ma) or 35. 69 to 37.60 Ma. This age revision constrains the timing of an adaptive shift in mammalian herbivores toward hypsodonty. Specifically, the appearance of large numbers of hypsodont taxa in South America occurred sometime between 36 and 32 Ma (late Eocene-early Oligocene), at approximately the same time that other biotic and geologic evidence has suggested the Southern high latitudes experienced climatic cooling associated with Antarctic glaciation.

Phylogenetic analysis of anthropoid relationships.

The relationships of anthropoids to other primates are currently debated, as are the relationships among early fossil anthropoids and crown anthropoids. To resolve these issues, data on 291 morphological characters were collected for 57 taxa of living and fossil primates and analyzed using PAUP and MacClade. The dental evidence provides weak support for the notion of an adapid origin for anthropoids, the cranial evidence supports the tarsier-anthropoid hypothesis, and the postcranial evidence supports a monophyletic Prosimii and a monophyletic Anthropoidea. Combining these data into a single data set produces almost universal support for a tarsier-anthropoid clade nested within omomyids. Eosimias and Afrotarsius are certainly members of this clade, and probably basal anthropoids, although the Shanghuang petrosal may not belong to Eosimias. The tree derived from the combined data set resembles the tree derived from the cranial data set rather than the larger dental data set. This may be attributable to relatively slower evolution in the cranial characters. The combined data set shows Anthropoidea to be monophyletic but the features traditionally held to be anthropoid synapomorphies are found to have evolved mosaically. Parapithecines are the sister taxon to crown anthropoids; qatraniines and oligopithecids are more distantly related sister taxa. There is support for a relationship of a Tarsius + Anthropoidea clade with either washakiines on Uintanius. These elements of tree topology remain fairly stable under different assumptions sets, but overall, tree topology is not robust. Previously divergent hypotheses regarding anthropoid relationships are attributable to the use of restricted data sets. This large data set enables the adapid-anthropoid hypothesis to be rejected, and unites Tarsius, Anthropoidea and Omomyiformes within a clade, Haplorhini. However, relationships among these three taxa cannot be convincingly resolved at present.

A new pitheciin primate from the middle Miocene of Argentina.

We report here a new fossil primate from the middle Miocene of Argentina. The material consists of isolated teeth, mandibular fragments, and a talus. The fossils were collected in the Collón Cura formation at Cañadón del Tordillo in Neuquén Province. An age of 15.71 +/- 0.07 Ma has been reported for the Pilcaniyeu Ignimbrite, which lies just below the paleosols in which the fossils were found. This material is thus the youngest occurrence of fossil primates in Argentina (hitherto documented in the Santacrucian and older land mammal ages) but still is older than the middle Miocene platyrrhine primates from La Venta, Colombia, in particular the pitheciins Nuciruptor and Cebupithecia. The material is recognized as a new genus and species of Pitheciinae, Propithecia neuquenensis. The mesiodistally compressed, high-crowned incisors are specialized and similar to species in the tribe Pithecini and to the nonpitheciin Soriacebus (early Miocene, Patagonia). We rule out a phylogenetic relationship to the latter because of differences in molar morphology. Propithecia does, however, fit well into the pattern of pitheciin evolution, being more derived than the middle Miocene pitheciin Nuciruptor but not as much as another middle Miocene taxon, Cebupithecia. As such, this makes Propithecia the oldest taxon that can be confidently placed within this modern New World monkey subfamily. By analogy with the molar structures and diets of extant platyrrhines, Propithecia has a molar structure consistent with a variety of low-fiber diets ranging from fruit and gum to seeds. Its incisors suggest seed-eating in much the same way as extant pitheciins, like Pithecia. The talus resembles that of Callicebus, suggesting arboreal quadrupedal locomotion.

The hypoglossal canal and the origin of human vocal behavior.

The mammalian hypoglossal canal transmits the nerve that supplies the muscles of the tongue. This canal is absolutely and relatively larger in modern humans than it is in the African apes (Pan and Gorilla). We hypothesize that the human tongue is supplied more richly with motor nerves than are those of living apes and propose that canal size in fossil hominids may provide an indication about the motor coordination of the tongue and reflect the evolution of speech and language. Canals of gracile Australopithecus, and possibly Homo habilis, fall within the range of extant Pan and are significantly smaller than those of modern Homo. The canals of Neanderthals and an early "modern" Homo sapiens (Skhul 5), as well as of African and European middle Pleistocene Homo (Kabwe and Swanscombe), fall within the range of extant Homo and are significantly larger than those of Pan troglodytes. These anatomical findings suggest that the vocal capabilities of Neanderthals were the same as those of humans today. Furthermore, the vocal abilities of Australopithecus were not advanced significantly over those of chimpanzees whereas those of Homo may have been essentially modern by at least 400,000 years ago. Thus, human vocal abilities may have appeared much earlier in time than the first archaeological evidence for symbolic behavior.

Primate species richness is determined by plant productivity: implications for conservation.

The explanation of patterns in species richness ranks among the most important tasks of ecology. Current theories emphasize the interaction between historical and geographical factors affecting the size of the regional species pool and of locally acting processes such as competitive exclusion, disturbance, productivity, and seasonality. Local species richness, or alpha diversity, of plants and primary consumers has been claimed to peak in habitats of low and intermediate productivity, which, if true, has major implications for conservation. Here, by contrast, we show that local richness of Neotropical primates (platyrrhines) is influenced by both historical biogeography and productivity but not by tree species richness or seasonality. This pattern indicates that habitats with the highest plant productivity are also the richest for many important primary consumers. We show further that fragmentation of Amazonian rain forests in the Pleistocene, if it occurred, appears to have had a negligible influence on primate alpha species richness.

Nuciruptor rubricae, a new pitheciin seed predator from the Miocene of Colombia.

A new genus and species of platyrrhine primate, Nuciruptor rubricae, are added to the increasingly diverse primate fauna from the middle Miocene of La Venta, Columbia. This species displays a number of dental and gnathic features indicating that it is related to living and extinct Pitheciinae (extant Callicebus, Pithecia, Chiropotes, Cacajao, and the Colombian middle Miocene Cebupithecia sarmientoi). Nuciruptor is markedly more derived than Callicebus but possesses a less derived mandibular form and incisor-canine complex than extant and extinct pitheciins (Cebupithecia, Pithecia, Chiropotes, and Cacajao), suggesting that it is a primitive member of the tribe Pitheciini within the larger monophyletic Pitheciinae. Nuciruptor has procumbent and moderately elongate lower incisors and low-crowned molars, suggesting that is was a seed predator, as are living pitheciins. Its estimated body size of approximately 2.0 kg places it within the size range of extant pitheciines. The dental and gnathic morphology of Nuciruptor clarifies several aspects of dental character evolution in Pitheciinae and makes it less likely that the enigmatic Mohanamico hershkovitzi (m. Miocene, Columbia) is a pitheciin.

Anthropoid origins.

Recent fossil discoveries have greatly increased our knowledge of the morphology and diversity of early Anthropoidea, the suborder to which humans belong. Phylogenetic analysis of Recent and fossil taxa supports the hypotheses that a haplorhine-strepsirrhine dichotomy existed at least at the time of the earliest record of fossil primates (earliest Eocene) and that eosimiids (middle Eocene, China) are primitive anthropoids. Functional analysis suggests that stem haplorhines were small, nocturnal, arboreal, visually oriented insectivore-frugivores with a scurrying-leaping locomotion. A change from nocturnality to diurnality was the fundamental adaptive shift that occurred at the base of the tarsier-eosimiid-anthropoid clade. Stem anthropoids remained small diurnal arborealists but adopted locomotor patterns with more arboreal quadrupedalism and less leaping. A shift to a more herbivorous diet occurred in several anthropoid lineages.

Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America).

A comparison of the species richness and macroniche composition of diet, locomotor and body-size classes among 16 nonvolant mammalian faunas in tropical South America reveals numerous significant positive correlations with rainfall. In particular, significant and strong positive correlations with rainfall are found in 18 attributes, including the number of nonvolant mammal species, number of primate species, number of frugivores, primary consumers, arborealists, and the number of species between 100 g to 10 kg in body weight. Estimates of annual rainfall derived from least-squares and polynomial regressions and principal components analysis yield a modal estimate of between 1500 and 2000 mm annual rainfall for the Monkey Beds assemblage at La Venta. This level of rainfall is associated today with the transition between savanna and forest environments in lowland equatorial South America. Paleontological evidence strongly suggests the presence of forest biotopes at La Venta. Paleontologic and sedimentologic evidence together indicate a dynamic and heterogeneous riparian mosaic associated with the shifting course of meandering rivers. Faunal evidence also suggests that habitat heterogeneity and canopy discontinuity extended into the interfluvial area. Seasonal rainfall was probably only of secondary importance in shaping the structural and spatial configuration of the dominantly forested mosaic habitat at La Venta. The fossil record is not consistent with the presence of extensive primary or undisturbed, continuous-canopy, evergreen tropical rainforest. The reconstructed middle Miocene environment at La Venta differs significantly from modern environments of similar geography on the piedmont east of the Andes at the same latitude. This in turn suggests that the extensive evergreen rainforests of the upper Amazonian piedmont that today receive more than 4000 mm of rainfall may post-date the initiation of Andean uplift.

The dietary adaptations of European Miocene catarrhines.

European Miocene "apes" have been known for nearly a century and a half but their phylogenetic significance is only now becoming apparent with the recent discovery of many relatively complete remains. Some appear to be close in time and morphology to the last common ancestor of modern great apes and humans. The current study is an attempt to reconstruct the diets of these fossils on the basis of quantitative data. Results suggest that these primates varied more greatly in their diets than modern apes, with adaptations ranging from hard-object feeding to soft-object frugivory to folivory.

"Giant" tamarin from the Miocene of Colombia.

A nearly complete but badly crushed skull and mandible of Lagonimico conclucatus, gen. et sp. nov. is described from the La Victoria Formation, Colombia. The specimen is of middle Miocene age and dates from about 13.5 Ma. Features of the dentition suggest Lagonimico is a sister group to living Callitrichinae (Saguinus, Leontopithecus, Callithrix, and Cebuella). These features include having elongate compressed lower incisors, a reduced P2 lingual moiety, and the absence of upper molar hypocones. The new taxon also has autapomorphies, such as a relatively deep jaw, that rule it out of the direct ancestry of any living callitrichine. This animal is assigned to a new tribe of the callitrichine clade. The orbits of L. conclucatus are small, suggesting diurnal habits. Inflated, low-crowned (bunodont) cheek teeth with short, rounded shearing crests, as well as premolar simplification and M3 size reduction, suggest fruit- or gum-eating adaptations, as among many living callitrichines. Procumbent and slightly elongate lower incisors suggest this species could use its front teeth as a gouge, perhaps for harvesting tree gum. Estimates from jaw size suggest Lagonimico weighed about 1,200 g, about the size of Callicebus, the living titi monkey of South America. Judged from tooth size and jaw length, Lagonimico would have been slightly smaller than Callicebus, but still larger than Callimico or any living callitrichine. Therefore, many of the distinctive anatomical features of the callitrichine clade, sometimes explained by phyletic dwarfing, may have evolved at larger body size. Evolutionary size reduction may have occurred in parallel in callitrichines and Callimico.

Partial humeri of two Miocene Colombian primates.

Distal portions of humeri from two Miocene Colombian primates were recovered during field work in 1986. The larger IGM 183420 is very similar in size and morphology to the humerus included in the type specimen of Cebupithecia sarmientoi, recovered from La Venta in 1945 (Stirton and Savage: Serv. Geol. Nac. Bogata 7:345-356, 1951) and is assigned to this taxon. IGM 183420 presents a number of features of the humerus associated with clinging postural behaviors in living platyrrhines, including a medial epicondyle with very little dorsal angulation, a cylindrical trochlea, and a contact facet for the coronoid process of the ulna. In these and other features Cebupithecia most closely resembles the extant genus Pithecia. IGM 183512 is approximately the size of Saimiri sciureus and is very similar in morphology to the humerus of this small arboreal quadruped. The medial epicondyle is more dorsally angled, the medial lip of the trochlea is more pronounced and the capitulum is less spherical as compared to Cebupithecia. This fossil is assigned to the taxon Neosaimiri fieldsi.

Sexual selection and canine dimorphism in New World monkeys.

Social and ecological factors are important in shaping sexual dimorphism in Anthropoidea, but there is also a tendency for body-size dimorphism and canine dimorphism to increase with increased body size (Rensch's rule) (Rensch: Evolution Above the Species Level. London: Methuen, 1959.) Most ecologist interpret Rensch's rule to be a consequence of social and ecological selective factors that covary with body size, but recent claims have been advanced that dimorphism is principally a consequence of selection for increased body size alone. Here we assess the effects of body size, body-size dimorphism, and social structure on canine dimorphism among platyrrhine monkeys. Platyrrhine species examined are classified into four behavioral groups reflecting the intensity of intermale competition for access to females or to limiting resources. As canine dimorphism increases, so does the level of intermale competition. Those species with monogamous and polyandrous social structures have the lowest canine dimorphism, while those with dominance rank hierarchies of males have the most canine dimorphism. Species with fission-fusion social structures and transitory intermale breeding-season competition fall between these extremes. Among platyrrhines there is a significant positive correlation between body size and canine dimorphism However, within levels of competition, no significant correlation was found between the two. Also, with increased body size, body-size dimorphism tends to increase, and this correlation holds in some cases within competition levels. In an analysis of covariance, once the level of intermale competition is controlled for, neither molar size nor molar-size dimorphism accounts for a significant part of the variance in canine dimorphism. A similar analysis using body weight as a measure of size and dimorphism yields a less clear-cut picture: body weight contributes significantly to the model when the effects of the other factors are controlled. Finally, in a model using head and body length as a measure of size and dimorphism, all factors and the interactions between them are significant. We conclude that intermale competition among platyrrhine species is the most important factor explaining variations in canine dimorphism. The significant effects of size and size dimorphism in some models may be evidence that natural (as opposed to sexual) selection also plays a role in the evolution of increased canine dimorphism.

Early hominid diets from quantitative image analysis of dental microwear.

The dietary habits of the early hominids Australopithecus and Paranthropus have long been debated. Robinson argued that the two species differed in the proportions of meat and vegetables consumed. More recently it has been suggested that Paranthropus, with its presumably larger body size, simply processed greater amounts of the same foods eaten by Australopithecus to maintain 'functional equivalence'. Microscopic dental wear patterns are related to the dietary habits of extant mammals, and quantification of these patterns is useful in distinguishing among primates with different diets. Nevertheless, few attempts have been made to use microwear in the reconstruction of early hominid diets, and only very recently has the quantification of such data been initiated. While microwear fabrics can be reduced to individual elements (for example, scratches and pits), there is some disagreement over exactly how they should be defined and measured. Fourier transforms have been applied successfully in the study of a variety of physical and biological patterns, and recently they have been used to characterize and distinguish different tooth wear patterns more objectively. Here we report the first combined use of image processing and other quantitative techniques to analyse the dental microwear of early hominids. Our results suggest that Paranthropus ate substantially more hard food items than Australopithecus.

New material of Qatrania from Egypt with comments on the phylogenetic position of the parapithecidae (primates, Anthropoidea).

New material of the early anthropoid primate Qatrania wingi and a new species of that genus are described. Several features of the dental anatomy show that Qatrania, while quite primitive relative to other anthropoids in many ways, is most likely a parapithecid primate. The new material suggests that several dental features previously thought to ally parapithecids with the catarrhine primates were actually evolved in parallel in catarrhines and some parapithecids. Furthermore, all nonparapithecid anthropoids (including platyrrhines and catarrhines) share a suite of derived dental and postcranial features not found in parapithecids. Therefore, parapithecid origins may predate the platyrrhine/catarrhine split.

Analysis of primate dental microwear using image processing techniques.

This paper introduces Fourier transformation as a rapid, replicable means for characterizing and distinguishing patterns of microscopic wear on primate teeth. The two-dimensional power spectra obtained from numerical Fourier transformation are shown to be different between two test patterns, one of which is composed of linear features and the other of randomly-spaced dots. A comparison is made, using Fourier transformation, of dental microwear patterns of small samples of two primate species, Ateles geoffroyi, the spider monkey, and Chiropotes satanas, the bearded saki. Ateles, with a scratch-dominated pattern of microwear, has a Fourier transform resembling that of the linear test pattern. Chiropotes, with a pit-dominated microwear pattern, resembles the transform of the dot pattern. The significance of this is discussed in light of the dietary differences between the two species.

Miocene characid fishes from Colombia: evolutionary stasis and extirpation.

Fossil fishes from the Miocene La Venta fauna of the Magdalena River Valley, Colombia, are identified as Colossoma macropomum (Characidae), a living species from the Orinoco and Amazon basins. The fossils document a long and conservative history for a species that is highly specialized for feeding on streamside plants. The phylogenetically advanced position of Colossoma in the subfamily Serrasalminae implies that six related genera and other higher characid taxa originated well before 15 million years ago. This discovery also corroborates neontological evidence for a vicariance event that contributed species from Miocene Orinoco-Amazon faunas to the original Magdalena region fauna. The fossils suggest a formerly diverse Magdalena fauna that has suffered local extinction, perhaps associated with late Cenozoic tectonism. This new evidence may help explain the depauperate nature of the modern Magdalena River.

Cementum annulus counts provide a means for age determination in Macaca mulatta (primates, anthropoidea).

14 teeth of 8 rhesus macaques (Macaca mulatta) of known age were analyzed to assess the usefulness of cementum annuli counts as a means of estimating chronological age. Methods used were histological examination of stained thin sections by light microscopy, and examination of polished and etched epoxy-embedded sections by scanning electron microscopy. In 11 of 14 cases, the known chronological ages of the individuals fell within the predicted age ranges based on cementum annuli counts; in 2 other cases, it fell within half a year of the ranges. Cementum annulus counts can provide valuable information about the age of primates living in semitropical environments. This is the most accurate method for aging skeletally adult primates that has yet been tested on animals of known age.

Dental formulae and dental eruption patterns in Parapithecidae (Primates, Anthropoidea).

The eruption sequence for the lower teeth of Apidium phiomense based on 18 juvenile specimens is dP3, dP4, M1, M2, P2, P4, (P3, M3), C. Only five specimens of Parapithecus grangeri show developing lower teeth. P2, M1, and M2 all erupted before P3 and P4; C and M3 were the last cheek teeth to erupt. Late eruption of the lower canines in parapithecids is a possible shared derived resemblance linking these species with Anthropoidea and Adapidae and distinguishing both from Omomyidae, Tarsiidae, and tooth-combed lemurs. Late eruption of M3 in parapithecids is a shared derived resemblance with Anthropoidea alone. The lower dental formula of Apidium phiomense is confirmed as 2 X 1 X 3 X 3 by additional specimens which show the incisors. Based in part on tooth socket counts, the deciduous lower dental formula was 2 X 1 X 3. New specimens of Parapithecus grangeri now demonstrate an adult mandibular dental formula of 0 X 1 X 3 X 3 (not 2 X 1 X 3 X 3 as previously thought) and a juvenile formula of 1 X 1 X 3. The number of incisors possessed by Parapithecus fraasi is again open to debate. Material is insufficient to judge whether this species had a pair of incisors in each lower jaw quadrant, by analogy with Apidium, or had undergone reduction to just one incisor. In any event, the presence of two incisors in another parapithecid Apidium shows anterior tooth reduction of Parapithecus grangeri occurred independent of, and should not be considered a shared derived similarity with, Tarsiidae, as was once thought.

True grit: a microwear experiment.

Recently we noted the effects of experimental diets on microscopic dental wear in the American opossum and concluded that it might prove difficult to distinguish the microwear produced by an insectivorous diet from that produced by some kinds of herbivorous ones. We also noted that wear caused by gritty diets and those containing plant opal, although they might be confused with one another, are easily distinguished from other sorts of dietary wear. Our conclusions have been challenged on the basis that possibly we did not allow sufficient time in the experiments for diagnostic wear patterns to emerge. Additional data reported here show that this is not so. Even in our "control" animals, fed a relatively soft unabrasive diet, enough time elapsed to produce significant dental wear. A new technique is described which for the first time allows the study of changing patterns of microscopic wear in a living animal over a period of time, thus allowing each animal to serve as its own control. A solution containing a broad-spectrum proteolytic enzyme when applied to the teeth of an anesthetized animal removes the proteinaceous coat (pellicle) which will otherwise obscure wear scratches. Precision dental impressions can then be made which reveal the details of the pattern of microwear on the teeth.