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Cenozoic Mammals of Africa$

Lars Werdelin

Print publication date: 2010

Print ISBN-13: 9780520257214

Published to California Scholarship Online: March 2012

DOI: 10.1525/california/9780520257214.001.0001

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Cercopithecoidea

Cercopithecoidea

Chapter:
(p.393) Twenty-Three Cercopithecoidea
Source:
Cenozoic Mammals of Africa
Author(s):

Nina G. Jablonski

Stephen Frost

Publisher:
University of California Press
DOI:10.1525/california/9780520257214.003.0023

Abstract and Keywords

Old World monkeys are some of the most common and visible components of the modern mammalian fauna of Africa, and are the dominant nonhuman primates in Africa today with respect to the overall numbers of species present and the number of ecological zones inhabited. What is rarely appreciated is that Old World monkeys have risen to a position of ecological dominance among primates only recently in geological time. During the early and middle Miocene, the Cercopithecoidea were well established in Africa, but not taxonomically diverse. The absence or near absence of monkey fossils from prolific early Miocene sites like Rusinga Island suggests that the animals were genuinely rare elements of the mammalian fauna at the time. The earliest African cercopithecoids belong to the Victoriapithecidae, an extinct family from the early to middle Miocene of eastern Africa that exhibit a mosaic of basal catarrhine and modern Old World monkeylike morphological features. This chapter describes the systematic paleontology of Cercopithecoidea.

Keywords:   Cercopithecoidea, paleontology, Old World monkeys, Africa, Miocene, fossils, cercopithecoids, Victoriapithecidae

Old World monkeys are some of the most common and visible components of the modern mammalian fauna of Africa, and are the dominant nonhuman primates in Africa today with respect to the overall numbers of species present (from 39 to 44, depending on species definitions) and the number of ecological zones inhabited (from primary evergreen rainforests and swamp forests, to woodlands, savannas, grassy plateaus, arid subdeserts, and steppes). What is rarely appreciated is that Old World monkeys have risen to a position of ecological dominance among primates only recently in geological time. During the early and middle Miocene, the Cercopithecoidea were well established in Africa, but not taxonomically diverse. The absence or near absence of monkey fossils from prolific early Miocene sites like Rusinga Island suggests that the animals were genuinely rare elements of the mammalian fauna at the time.

The earliest African cercopithecoids belong to the Victoriapithecidae, an extinct family from the early to middle Miocene of eastern Africa that exhibit a mosaic of basal catarrhine and modern Old World monkeylike morphological features. The ambiguity of the morphology of the victoriapithecids has persuaded most authorities that the group represents an early radiation, distinct from rather than ancestral to, other Old World monkeys; however, the possibility that they are a series of only loosely related stem cercopithecoids cannot be ruled out. They are often classified in a family equivalent to the Cercopithecidae. The latter is here divided into two subfamilies, the Cercopithecinae (comprising the modern vervets, guenons, mangabeys, mandrills, geladas, common baboons and their fossil relatives) and Colobinae (comprising the green, red, and black-and-white colobus monkeys and their fossil relatives), following Groves (Groves, 2001) and the generally accepted convention for the discipline, but in contrast to the scheme followed in a previous review (Jablonski, 2002).

In this chapter, we refer to fossil-bearing sites within various regions of Africa, such as northern Africa. For our purposes, northern Africa comprises Morocco, Algeria, Libya, Egypt, and the Sudan. Northeastern Africa includes Ethiopia, Somalia, and Eritrea. Eastern includes Kenya, Uganda, and Tanzania. Southern Africa comprises South Africa, while southwestern Africa refers to Angola.

The events that produced the major lineages recognized at the family and subfamily levels within the Cercopithecoidea occurred in the early Miocene of Africa, based on first appearances of Victoriapithecidae in the fossil record of northern and eastern Africa beginning approximately 20 mya (Benefit and McCrossin, 2002) and the absence of fossil cercopithecoids outside of Africa until the very late Miocene (Barry, 1987; Jablonski, 2002). Molecular methods have been used increasingly in the last two decades to aid in the reckoning of cercopithecoid phylogeny in the face of widespread morphological homoplasy and to refine the timing of lineage splitting events in the absence of informative fossils. The split between the Colobinae and Cercopithecinae has been estimated using mtDNA at about 16.2 Ma (with an approximate 95% confidence interval of 14.4–17.9 Ma; Raaum et al., 2005), but detailed knowledge of this milestone and of the early history of the modern subfamilies is still unclear due to a paucity of middle Miocene fossils.

By the late Miocene, clearly differentiated members of the Cercopithecinae and Colobinae are present in the African fossil record, and from this time onward, Old World monkey lineages underwent increasing cladogenesis and dispersal. Dispersal of at least one major lineage each of colobine and cercopithecine monkeys into Eurasia in the late Miocene resulted in the seeding of that continent with the ancestors of Mesopithecus (and descendant colobines) and the earliest forms of macaques, respectively. Increased fragmentation of forests and greater habitat heterogeneity resulting from major mountain-building events and their climatic sequelae in Asia, Europe, and Africa created new ecological opportunities for the Cercopithecoidea throughout the Old World from the late Miocene onward. Phyletic and ecological diversification of the group increased through the Plio-Pleistocene of Africa, mirroring an increase in environmental seasonality and habitat heterogeneity on the continent. By the Plio-Pleistocene, Cercopithecoidea were among the most diverse, widespread, and prolific of mammals in Africa, even without taking into account the many taphonomic factors, which biased the fossil record against preservation of small-bodied and forest-dwelling species.

(p.394) The success of many cercopithecoid species in Africa today is due to their adaptability and behavioral flexibility, which render them less sensitive to increases in climatic variability, environmental seasonality, and other ecological disturbances than strepsirrhines and apes. Cercopithecoids can eat a wider variety of foods and can engage more readily in food switching than other primates (excepting humans). They also exhibit relatively fast life histories typified by early age at first birth, short interbirth intervals, and relatively short weaning periods. These attributes permit successful reproduction under highly seasonal conditions or during times of environmental uncertainty (Jablonski et al., 2000). The parallel evolution of these qualities in the Old World monkey and human lineages has been one of the main reasons sustaining consistently high levels of scholarly interest in the fossil record of African Cercopithecoidea over the last half century. African fossil Cercopithecoidea have been offered as models of hominin differentiation, evolution, and behavior in numerous studies, the most enduring and worthy of these being Clifford Jolly’s “seed-eater hypothesis” in which PlioPleistocene Theropithecus was invoked as a model organism in the study of the adaptive radiation of hominids (Jolly, 1970).

The roots of the adaptability and evolutionary success of the Old World monkeys can be traced not only to their dietary flexibility and life histories, but also to their generalized anatomies. Cercopithecoidea are distinguished from Hominoidea in their dentition and skeleton by bilophodont molars, a prominent developmental sulcus on the buccal surface of the male upper canine, the absence or considerable reduction of the paranasal sinuses, and a prominent medial trochlear keel on the distal humerus (Szalay and Delson, 1979; Strasser and Delson, 1987). Cercopithecoids are agile quadrupeds with grasping cheiridia. While a lack of hooves precludes seasonal migrations and reduces potential day range size, dexterous and sensitive fingers permit extraction and harvesting of a wide variety of foods on the ground and in trees. Foods picked with the fingers are further processed in the mouth by spatulate incisors and bilophondont molars. The dental formula for the group is 2.1.2.3 in both jaws. Bilophodont molars, one of the hallmarks of the Cercopithecoidea, are capable of reducing a variety of foods by cutting and crushing, depending on the thickness of the enamel, height of the cusps, steepness of the shearing surfaces, and total occlusal surface area. Cercopithecines, with a few notable exceptions, are eclectic feeders. They manually harvest and eat fruits, seeds, flowers, rhizomes, insects, and even small vertebrates, which they triturate with thick-enameled molars of generally low relief. The living species have ischial callosities and all have cheek pouches, which can provide temporary storage space for high-quality food items. This capability can be particularly important in light of frequently high levels of within-group scramble competition for food. Colobines concentrate on eating plant foods with generally higher fiber and allelochemical content, including young leaves, seeds, and unripe fruits that are harvested by hand and slowly digested with the assistance of bacterial symbionts in a ruminant stomach. Most colobine species exhibit greatly reduced or absent external thumbs. Although they are often referred to as the leaf-eating monkeys, seeds are important components of the diet of most extant species (Lucas and Teaford, 1994), and seed eating may have been one of the selective forces involved in the original differentiation of the group. Molars with thin enamel, high cusp relief, and tall shearing crests permit colobines to finely shred and pulverize ingested vegetation, thus increasing the surface area of material exposed to salivary enzymes (Stewart et al., 1987; Zhang et al., 2002). Foregut fermentation, including recruitment of lysozyme as a bacteriolytic enzyme in the stomach, evolved independently in colobines and ruminant artiodactyls, and it was a major element of the evolutionary success of both groups in the changing environments of the late Miocene and Pliocene. Colobines do not chew the cud, but their ruminant digestive apparatus permits them to chemically transform the complex carbohydrates in vegetation into fatty acids as a source of energy. The prolonged and chemically complex digestive processes in the colobine gut also break down toxic secondary compounds found in seeds and leaves, a process that renders many “nonprimate foods” suitable fare. Ruminant digestion also reduces animals’ dependence on drinking water, thus increasing potential niche breadth (Van Soest, 1982).

Fossils of Old World monkeys in Africa have been recovered in significant numbers from a wide variety of sites in northern and sub-Saharan Africa. Readers are referred to recently published reviews for discussions of the history of discovery of fossil Cercopithecoidea in these regions (Benefit and McCrossin, 2002; Jablonski, 2002). The distribution of fossil sites in space and time in Africa is uneven, however, and our knowledge of the past occurrences, evolutionary histories, and adaptations of African Cercopithecoidea is biased and incomplete. The largest concentrations of monkey-bearing sites occur along the Great Rift Valley of eastern and northeastern Africa, and in the breccia-filled caves of the Transvaal region of South Africa and Angola. Most of these sites are of Pliocene and Pleistocene age, but recent finds of late Miocene monkeys from Ethiopia, Kenya, and Chad (Brunet et al., 2002; Hlusko, 2006, 2007; Frost et al., 2009) have shed light on an earlier and little-known phase of the group’s evolution. A scattering of Plio-Pleistocene sites yielding monkey fossils also occurs in Algeria, Morocco, and Egypt. The evolutionary proximity and co-occurrence of hominins and cercopithecoids has meant that, at most sites, monkey fossils have been collected completely and prepared promptly, leaving paleontologists with much to study.

The propinquity of the Old World monkeys to humans has led to intensive study of the phylogeny and systematics of the Cercopithecoidea, and numerous modifications to the classification of the group in recent decades. Controversies have arisen in large part because the recency of the group’s radiation has contributed to the existence of considerable homoplasy in features of the dentition, skull, and postcranial skeleton of phyletically distant taxa. The increased use of soft tissue and molecular characters, as mentioned above, has overcome some of these problems, and has yielded some considerable surprises for classification of the group in general. Among these are the recognition that mangabeys are diphyletic (Barnicot and Hewtt-Emmett, 1972; Gilbert, 2007b), that the so-called odd-nosed monkeys of Asia comprise a distinct clade (Sterner et al., 2006), recognition of a single “terrestrial” clade among the guenons (Disotell and Raaum, 2002; Tosi et al., 2002a, 2004; Xing et al., 2005, 2007), and that pronounced elongation of the muzzle evolved independently at least four times within the Papionini (in Mandrillus, Papio, the Theropithecus brumpti lineage; Eck and Jablonski, 1987), and the Plio-Pleistocene baboon-like macacines Paradolichopithecus and Procynocephalus of Eurasia (Szalay and Delson, 1979). With the introduction of better and more stable molecular phylogenies, classifications of the Cercopithecoidea are now (p.395) being duly revised (Benefit and McCrossin, 2002; Jablonski, 2002), but efforts to fit fossil species into these schemes are still in their infancy. This is because many African monkey fossil species are not clearly related to living species except by suites of shared ancestral features, and because some higher taxa contain only extinct species (e.g., all of the Victoriapithecidae and six of the eight recognized genera of African Colobinae are known only in the fossil record). For these reasons, no attempt has been made here to present a phylogenetic hypothesis or evolutionary tree summarizing the positions of the fossil monkeys of Africa.

Institutional Abbreviations

AMNH = American Museum of Natural History, New York; ARA-VP = Aramis, Middle Awash, National Museum of Ethiopia; CGM = Cairo Geological Museum, Cairo, Egypt; KA = Kromdraai A, Department of Palaeontology, Transvaal Museum, Pretoria, South Africa; KNM = National Museums of Kenya, Nairobi, Kenya (suffixes–BC = Baringo Chemeron; –BN = Baringo Ngeringerowa; -ER = East Turkana; -KP = Kanapoi; -LT = Lothagam; -MB = Maboko; -NK = Narok District, including Lemudong’o; WT = West Turkana); M = British Museum (Natural History), London; M (and MP) = Makapans-gat, Department of Anatomy, University of the Witwatersrand and Bernard Price Instititute, Johannesburg, South Africa; NME = National Museum of Ethiopia, Addis Ababa, Ethiopia; SAM = Iziko South African Museum, Capetown, South Africa; SB = Schurweberg (Skurweberg, Skurveberg), Department of Palaeontology, Transvaal Museum, Pretoria, South Africa; SK = Swartkrans, Department of Palaeontology, Transvaal Museum, Pretoria, South Africa; STS = Sterkfontein (pre-1966), Department of Palaeontology, Transvaal Museum, Pretoria, South Africa; SWP = Sterkfontein (post-1966) = Department of Anatomy, University of the Witwatersrand, Johannesburg, South Africa; and YPM = Yale Peabody Museum.

Systematic Paleontology

The classification of the Cercopithecoidea followed here (Table 23.1) is based on that used in previous reviews (Benefit and McCrossin, 2002; Jablonski, 2002), duly updated to reflect recent fossil discoveries and phylogenetic interpretations. Interpretations of the geological contexts and ages of many African fossil Cercopithecoidea have been controversial (Table 23.2); a useful review of this information for East African fossils has been published elsewhere and should be consulted (Gundling and Hill, 2000).

No tribes are recognized within the Colobinae because of ongoing study of the phyletic relationships between genera within the subfamily. Old World monkeys and their fossils have been studied by many people over more than a century, and, as a consequence, the synonymies for many species are lengthy and complex. Considerations of length preclude their reproduction in full here, so the reader is commended to other sources for this information (Freedman, 1957; Simons and Delson, 1978; Szalay and Delson, 1979; Groves, 2001). Photographs of specimens are by the authors unless otherwise stated.

  • Order PRIMATES Linnaeus, 1758
  • Family VICTORIAPITHECIDAE von Koenigswald, 1969

Victoriapithecidae is an extinct family of basal cercopithecoids. Victoriapithecids differ from other Cercopithecoidea in the possession of a lower and narrow neurocranium, supraor-bital costae, a frontal trigon formed in part by the anterior convergence of the temporal lines, orbits that are taller than wide, a deep malar region, variable occurrence of the crista obliqua on the deciduous P4–M3, absence of transverse distal lophs on the upper molars and deciduous upper premolars, and other features (Benefit, 1993, 1999; Benefit and McCrossin, 2002). Although the nominate genus is represented by abundant well-preserved fossils from Maboko Island (Kenya), Prohylobates is not, and considerable uncertainty remains over the morphology and taxonomic status of some of the earliest Old World monkeys. Renewed study of victoriapithecids from Egypt and northern Kenya (including fossils originally classified as Prohylobates sp. nov. from Buluk, Kenya; Leakey, 1985; Miller et al., 2009) has led to a forthcoming revision of the family that promises to shed light on these problems.

  • Genus PROHYLOBATES Fourtau, 1918

Diagnosis Delson (1979); Miller et al. (2009). Distinguished from Victoriapithecus by the possession of lower permanent molars exhibiting incomplete bilophodonty, and a reduced M3 hypoconulid.

Description Prohylobates is known from relatively few fossil jaws and teeth from the type locality of Wadi Moghara in Egypt and Jabal Zaltan, Libya.

Age Early–middle Miocene.

African Occurrence Northern Africa.

Remarks Poor preservation of most specimens has hindered detailed comparison with Victoriapithecus and assessment of the position of the genus within its family. Despite these difficulties, the molar morphology of available specimens indicates incomplete development of bilophodonty, and the conclusion that the genus is more primitive than Victoriapithecus (Benefit, 2009).

Northern Africa was a center of catarrhine diversification from the Oligocene through the middle Miocene. The region’s importance in cercopithecoid evolution was great and is increasingly recognized as such as more fossils of middle Miocene age are recovered from sites in Egypt and Libya. Logistical and physical difficulties continue to hamper this effort throughout the region, however.

  • PROHYLOBATES SIMONSI Delson, 1979

Diagnosis Miller et al. (2009). Differs from other species of Prohylobates in its much larger size and possession of M2 and M3 of equal size. Its distinctive morphology may warrant placement in a new genus.

Description The species is known from the holotype, AMNH 17768, a partial mandible.

Age Middle Miocene.

African Occurrence Jabal Zaltan (= Gebel Zelten)(Libya).

Remarks This species shares with other Victoriapitheci-dae a quadrate arrangement of cusps on a waisted M2, pronounced molar flare, and molar wear that begins as circular depressions on cusp tips (Benefit and McCrossin, 2002).

  • PROHYLOBATES TANDYI Fourtau, 1918

Diagnosis Prohylobates tandyi exhibits smaller molar teeth than most members of its family and differs from other species of its genus in its possession of a P4 which is large relative to the lower molars, and a very small M3 relative to M2 and equal to M1 (Benefit and McCrossin, 2002; Miller et al., 2009).

(p.396)

Table 23.1 Classification of the fossil Cercopithecoidea of Africa followed in this chapter

Order

Primates Linnaeus, 1758

  Infraorder

Catarrhini É. Geoffroy Saint-Hilaire, 1812

    Superfamily

Cercopithecoidea Gray, 1821

      Family

Victoriapithecidae von Koenigwald, 1969

          Genus

Prohylobates Fourtau, 1918

Prohylobates simonsi Delson, 1979

Prohylobates tandyi Fourtau, 1918

          Genus

Victoriapithecus von Koenigswald, 1969

Victoriapithecus macinnesi von Koenigswald, 1969

      Family

Cercopithecidae Gray, 1821

          Subfamily

Colobinae Jerdon, 1867

              Genus

Cercopithecoides Mollett, 1947

Cercopithecoides kerioensis M. G. Leakey, Teaford, and Ward, 2003

Cercopithecoides kimeui M. G. Leakey, 1982

Cercopithecoides meaveae Frost and Delson, 2002

Cercopithecoides williamsi Mollett, 1947

Cercopithecoides alemayehui Gilbert and Frost, 2008

cf. Cercopithecoides

              Genus

Colobus Illiger, 1811

Colobus freedmani Jablonski and M.G. Leakey, 2008

Colobus guereza Rüppell, 1835 Colobus sp. indet.

              Genus

Kuseracolobus Frost 2001

Kuseracolobus aramisi Frost, 2001

Kuseracolobus hafu Hlusko, 2006

              Genus

Libypithecus Stromer, 1913

Libypithecus markgrafi Stromer, 1913

              Genus

Microcolobus Benefit and Pickford, 1986

Microcolobus tugenensis Benefit and Pickford, 1986

              Genus

Paracolobus R. E. F. Leakey, 1969

Paracolobus chemeroni R. E. F. Leakey, 1969

Paracolobus enkorikae Hlusko, 2007

Paracolobus mutiwa M. G. Leakey, 1982

Paracolobus sp. indet.

              Genus

Rhinocolobus M. G. Leakey, 1982

Rhinocolobus turkanensis M. G. Leakey, 1982

        Subfamily

Cercopithecinae Gray, 1821

          Tribe

Cercopithecini Gray, 1821

                Genus

Cercopithecus Brunnich, 1772

Cercopithecus sp. indet.

                Genus

Chlorocebus Gray, 1879

Chlorocebus cf. patas

cf. Chlorocebus aff. aethiops

            Tribe

Papionini Burnett, 1828

              Subtribe

Macacina Owen, 1843

                  Genus

Macaca Lacépède, 1799

Macaca libyca Stromer, 1920

Macaca sylvanus Linnaeus, 1758

            Subtribe

Papionina Burnett, 1828

                Genus

Cercocebus É. Geoffroy Saint-Hilaire, 1812

Cercocebus sp. indet.

                Genus

Dinopithecus Broom, 1937

Dinopithecus ingens Broom, 1937

                Genus

Gorgopithecus Broom and Robinson, 1949

Gorgopithecus major Broom, 1940

                Genus

Lophocebus Palmer, 1903

Lophocebus cf. albigena Gray, 1850

                Genus

Papio Müller, 1773

Papio hamadryas Linneaus, 1758

Papio izodi Gear, 1926

                Genus

Parapapio Jones, 1937

Parapapio ado Hopwood, 1936

Parapapio broomi Jones, 1937

Parapapio jonesi Broom, 1940

Parapapio lothagamensis M. G. Leakey, Teaford, and Ward, 2003

Parapapio sp. indet.

                Genus

Pliopapio Frost 2001 Pliopapio alemui Frost, 2001

                Genus

Procercocebus Gilbert, 2007

Procercocebus antiquus (Haughton, 1925)

                Genus

Theropithecus I. Geoffroy Saint-Hilaire, 1843

              Subgenus

Theropithecus Geoffroy Saint-Hilaire, 1843

Theropithecus (Theropithecus) darti (Broom and Jensen, 1946)

Theropithecus (Theropithecus) oswaldi Andrews, 1916

              Subgenus

Omopithecus Delson, 1993

Theropithecus (Omopithecus) baringensis (R. Leakey, 1969)

Theropithecus (Omopithecus) brumpti (Arambourg, 1947)

Theropithecus (Omopithecus) quadratirostris (Iwamoto, 1982)

Theropithecus (Omopithecus) sp. indet.

              Subgenus

Theropithecus sp. indet.

(p.397)

Table 23.2 Summary of major site occurrences and ages for African fossil Cercopithecoidea Age ranges provided are based on the most recent chronometric estimates available; otherwise age has been estimated only to epoch or subepoch. See text for details and complete list of site occurrences.

Taxon

Major Site Occurrences

Age

Key References

VICTORIAPITHECIDAE

Prohylobates simonsi

Jabal Zaltan [= Gebel Zelten] (Libya)

Middle Miocene

Delson, 1979

Prohylobates tandyi

Wadi Moghra (Egypt)

Early Miocene

Victoriapithecus macinnesi

Maboko Island (Kenya), Napak (Uganda)

19.5 Ma (Napak); ∼15–12.1 Ma (Maboko)

Benefit, 1993, 1999; Benefit and McCrossin, 2002

CERCOPITHECIDAE: COLOBINAE

Cercopithecoides kerioensis

Lothagam (Kenya)

5–4.2 Ma

Leakey et al., 2003

Cercopithecoides kimeui

East Turkana and Rawi Gulley (Kenya); Hadar (Ethiopia)

3–1.5 Ma

Frost et al., 2003b; Jablonski et al., 2008a

Cercopithecoides meaveae

Hadar (Ethiopia)

3.4–3.28 Ma

Frost and Delson, 2002

Cercopithecoides williamsi

East Turkana (Kenya); Sterkfontein, Makapansgat, Swartkrans, and Kromdraai (South Africa)

3.3–1.5 Ma

Freedman, 1957; Heaton, 2006; Jablonski et al., 2008a

Colobus freedmani

East Turkana (Kenya)

1.527–1.485 Ma

Jablonski and Leakey, 2008b

Colobus guereza

Wad (Wadi) Medani (Sudan)

Pleistocene

Simons, 1967; Frost and Alemseged, 2007

Colobus sp. indet.

Kanam East (Kenya); Omo Group, Afar, and Middle Awash (Ethiopia); Kazinga (Uganda)

Plio-Pleistocene; late Pleistocene

Frost and Alemseged, 2007

Kuseracolobus aramisi

Middle Awash and Gona (Ethiopia)

5.2–4.4 Ma

Frost, 2001b

Kuseracolobus hafu

Asa Issie (Ethiopia)

4.4–3.75 Ma

Hlusko, 2006

Libypithecus markgrafi

Wadi Natrun (Egypt)

Latest Miocene

Stromer, 1913; Delson, 1975

Microcolobus tugenens

Ngeringerowa (Kenya)

9.5–9.0 Ma

Benefit and Pickford, 1986

Paracolobus chemeroni

Chemeron (Kenya); Middle Awash (Ethiopia)

3–2 Ma

Leakey, 1969; Birchette, 1982

Paracolobus enkorikae

Lemudong’o (Kenya)

6 Ma

Hlusko, 2007

Paracolobus mutiwa

East and West Turkana (Kenya)

3.36–1.88 Ma

Leakey, 1982

Paracolobus sp. indet.

Laetoli (Tanzania); Western Rift (Uganda)

3.8–?2.5 Ma

Leakey and Delson, 1987; Senut, 1994

Rhinocolobus turkanensis

Omo Group (Ethiopia); East Turkana (Kenya)

3.4–1.5 Ma

Leakey, 1982; Jablonski et al., 2008a

CERCOPITHECIDAE: CERCOPITHECINAE: CERCOPITHECINI

Cercopithecus sp. indet.

Omo Group (Ethiopia); East Turkana and Kanam East (Kenya)

Pliocene and Pleistocene

Eck and Howell, 1972; Harrison and Harris, 1996; Jablonski et al., 2008b

Chlorocebus cf. patas cf. Chlorocebus aff. aethiops

Asbole and Middle Awash (Ethiopia)

Pleistocene

Frost, 2001a; Frost and Alemseged, 2007

CERCOPITHECIDAE: CERCOPITHECINAE: PAPIONINI

Macaca sylvanus

North Africa

Plio-Pleistocene

Macaca libyca

Wadi Natrun (Egypt)

Latest Miocene

Stromer, 1913; Delson, 1980

Cercocebus sp. indet.

Makapansgat, Kromdraai, and ?Swartkrans (South Africa)

Late Pliocene

Gilbert, 2007b

Dinopithecus ingens

Schurweberg and Swartkrans (South Africa)

Late Pliocene

Broom, 1937; Freedman, 1957; Szalay and Delson, 1979

Gorgopithecus major

Kromdraai (South Africa)

Plio-Pleistocene

Broom and Robinson, 1949; Freedman, 1957; Heaton, 2006

Lophocebus cf. albigena

East Turkana (Kenya)

?2.0–1.38 Ma

Jablonski et al., 2008b

Lophocebus sp. indet.

Kanam East (Kenya)

Plio-Pleistocene

Harrison and Harris, 1996

Papio hamadryas

Sterkfontein, Kromdraai, Drimolen, Swartkrans, and Bolt’s Farm (South Africa); Olduvai Gorge (Tanzania); Asbole, (Ethiopia)

Pleistocene

Freedman, 1976; Frost and Alemseged, 2007

Papio izodi

Taung, Sterkfontein Members 2 and 4, Kromdraai, and Coopers, (South Africa)

Plio-Pleistocene

Freedman, 1957; Szalay and Delson, 1979; Heaton, 2006

Parapapio ado

Laetoli (Tanzania); East Turkana (Kenya)

Pliocene

Leakey and Delson, 1987; Jablonski et al., 2008b

Parapapio broomi

Sterkfontein and Bolt’s Farm (South Africa)

Pliocene

Jones, 1937; Broom, 1940; Freedman, 1957; Heaton, 2006

Parapapio jonesi

Makapansgat, Sterkfontein (South Africa); Afar and Middle Awash (Ethiopia)

Pliocene

Freedman, 1957; Frost, 2001b; Frost and Delson, 2002

Parapapio lothagamensis

Lothagam (Kenya)

7.4–ca. 5 Ma

Leakey et al., 2003; Jablonski et al., 2008b

Parapapio sp. indet.

East and West Turkana and Lothagam (Kenya)

Plio-Pleistocene

Jablonski et al., 2008b

Pliopapio alemui

Middle Awash (Ethiopia)

?5.7–4.2 Ma

Frost, 2001b; Frost et al., 2009

Procercocebus antiquus

Taung (South Africa)

Plio-Pleistocene

Freedman, 1957; Gilbert, 2007b

Theropithecus (Theropithecus) darti

Omo Group, Middle Awash, and Hadar (Ethiopia); Makapansgat (South Africa)

3.5–2.4 Ma

Freedman, 1957, 1976; Eck, 1993; Frost, 2001b

Theropithecus (Theropithecus) oswaldi

Ain Jourdel and Ternifine (Algeria); Thomas Quarries (Morocco); Omo Group, Middle Awash, Afar Region, and Konso (Ethiopia); East and West Turkana, Olorgesailie, and Kapthurin (Kenya); Olduvai Gorge and Peninj (Tanzania); Kaiso (Uganda); and Swartkrans, Sterkfontein, Hopefi eld, and Bolt’s Farm (South Africa)

2.5–0.25 Ma

Jolly, 1972; Dechow and Singer, 1984; Eck, 1987; Delson, 1993; Delson et al., 1993; Delson and Hoffstetter, 1993; Leakey, 1993; Jablonski et al., 2008b

Theropithecus (Omopithecus) baringensis

Chemeron (Kenya); Leba (Angola)

3–2 Ma

Leakey, 1969; Eck and Jablonski, 1984; Delson and Dean, 1993

Theropithecus (Omopithecus) brumpti

East and West Turkana (Kenya); Omo Group (Ethiopia)

3.4–2.68 Ma

Eck and Jablonski, 1987; Leakey, 1993; Jablonski et al., 2002

Theropithecus (Omopithecus) quadratirostris

Omo Group (Ethiopia)

∼3 Ma

Iwamoto, 1982; Eck and Jablonski, 1984; Delson and Dean, 1993

Theropithecus (Omopithecus) sp. indet.

East Turkana (Kenya)

3.94 Ma

Jablonski et al., 2008b

Theropithecus subgen. et sp. indet.

Middle Awash (Ethiopia)

3.9 Ma

Frost, 2001a

(p.398)

Description This species is known from few specimens, including the holotype, CGM 30936, and a newly referred specimen, DPC 6235, both mandible fragments (Benefit and McCrossin, 2002).

Age Early Miocene.

African Occurrence Wadi Moghra (Egypt).

Remarks Understanding of this important species has been hampered by a small sample of specimens, all of which have abraded teeth.

  • Genus VICTORIAPITHECUS von Koenigswald, 1969
  • VICTORIAPITHECUS MACINNESI von Koenigswald, 1969
  • Figure 23.1

Diagnosis Benefit and McCrossin (2002). Distinguished from Prohylobates by a cercopithecine-like inferior transverse torus on the mandible, P4 small compared to molars, presence of metaconid on p3, molar size gradient M1 〈 M2 〉 M3 and m1 〈 m2 〈 m3.

Description The skull of Victoriapithecus is known from many, mostly fragmentary craniodental remains, the best of which are the male cranium, KNM-MB 29100 (Figure 23.1), maxillae KNM-MB 18995 and KNM-MB 18996, the mandible KNM-MB 18993.

Age Early–middle Miocene, 19.5 Ma (Napak); and ∼15–12.1 Ma (Maboko Formation)(Gundling and Hill, 2000; Benefit and McCrossin, 2002).

African Occurrence Numerous sites in Kenya, especially Maboko Island (Kenya), Napak (Uganda), and possibly Ongoliba (Democratic Republic of the Congo), as enumerated elsewhere (Benefit and McCrossin, 2002) but not universally accepted (Delson, 1979).

Remarks At present, the genus contains the single species, V.macinnesi, which is the best known of the Victoriapithecidae. It exhibits a distinctive mosaic of cercopithecine-like and colobine-like traits that are consistent with its age and its status as a generalized basal monkey. The cranium is narrower and lower relative to length than those of other cercopithecoids and exhibits slight ventral deflection of the cranial vault relative to the basicranium (klinorhynchy)(Benefit and McCrossin, 1997). It resembles those of cercopithecines in its narrow interorbital region and narrow nasal bones, low and narrow nasal aperture, moderately long and anteriorly tapering snout, and moderately long premaxilla (Benefit and McCrossin, 1997, 2002). The molar teeth Victoriapithecus are bilophodont but lack most of the derived specializations seen in the molars of Cercopithecinae and Colobinae, as thoroughly described by Benefit (Benefit, 1993; Benefit and McCrossin, 2002). The postcranial elements known for the species suggest that it was a mostly terrestrial quadruped, as reviewed elsewhere (Harrison, 1989).

(p.399)

Cercopithecoidea

Figure 23.1 Victoriapithecus macinnesi. Lateral view of male cranium KNM-MB 29100 with mandible KNM-MB 18993. Photograph courtesy of Brenda Benefit; © National Museums of Kenya.

  • Family CERCOPITHECIDAE Gray, 1821
  • Subfamily COLOBINAE Jerdon, 1867

Medium- to very large-sized monkeys with reduced or absent thumbs in most species, long tails, bilophodont molars with long shearing crests and steep sides in most species, and a sacculated stomach accommodating bacterial symbionts for foregut fermentation. The distal humerus, which is often preserved as a fossil, is distinguished in colobines by medial and lateral pillars flanking the olecranon fossa that are approximately equal in width and are relatively flat, giving the dorsal surface of the distal humerus a flattened look.

  • Genus CERCOPITHECOIDES Mollett, 1947

Diagnosis Distinguished from other colobines by its shallow mandibular corpus with a slightly convex inferior border in most specimens, a shallow and relatively thin mandibular symphysis, a nonexpanded gonion, and a low ramus oriented obliquely relative to the occlusal plane. Differs from other colobines in its squared muzzle and strong terrestrial adaptations in the postcranium, especially the forelimb. Differs from Rhinocolobus, Libypithecus, and Nasalis in its short muzzle and short, rounded calvaria. It differs from Asian colobines, Paracolobus, and Rhinocolobus in the absence of a protocone on the P3.

Description The earliest occurrences of the genus are fragmentary gnathic and postcranial remains in early Pliocene exposures in the East African Rift Valley recognized as cf. Cercopithecoides and C. kerioensis. The genus is best known from plentiful remains of C. williamsi retrieved from the PlioPleistocene limestone breccias of most of the South African cave sites, where it is one of the few fossil colobines known until the late Pleistocene (see Colobus, later). In East Africa, C. williamsi appears to have been rare but is represented by one partial skeleton in good condition from Koobi Fora, KNM-ER 4420. More common and widespread in the East African PlioPleistocene is C. kimeui, which is significantly larger. It is represented by several crania and mandibles, most of which bear heavily worn teeth (Jablonski et al., 2008a). Cercopithecoides meaveae is smaller than C. williamsi and known only from the middle Pliocene of the Afar region. Cercopithecoides kerioensis from the early Pliocene of Lothagam is the oldest known member of the genus.

Age Pliocene and early Pleistocene.

African Occurrence Eastern and southern Africa.

Remarks In most species, the face of Cercopithecoides is wide, and the large, widely spaced orbits are rectangular. The nasal aperture is small and the nasal bones are moderately long. The supraorbital torus is thick; the postorbital constriction is not marked. Sexual dimorphism appears low to moderate. The molars bear thin enamel and exhibit relatively high, columnar cusps with capacious basins and large foveae. The canines and P3 are sexually dimorphic. The postcranium is fairly well-known and shows many features characteristic of terrestrial cercopithecoids, especially in the forelimb.

Cercopithecoides was an agile and committed terrestrialist, and it shows many of the specializations to mostly terrestrial locomotion seen today in forms of Papio baboons in Africa and in temple langurs (Semnopithecus entellus) in Asia. The unique shallow but thick mandibular morphology in later species of the genus suggests that these forms of Cercopithecoides ate foods of a different consistency than those known for other colobines. In craniodental morphology, early species of Cercopithecoides most closely resemble Colobus. The similarities are strongest between Colobus and the earliest, most primitive forms of Cercopithecoides, (p.400) C. kerioensis from Lothagam and the specimens of the genus from early Pliocene horizons of the Koobi Fora Formation that share deep and relatively thin mandibles. Although Colobus and Cercopithecoides differ in limb proportions, they share many similarities in the morphology of the proximal and distal humerus and femur. These morphological resemblances suggest that modern Colobus may have descended from an early, primitive species of Cercopithecoides. This hypothesis warrants testing.

Cercopithecoides was the dominant colobine of the African Pliocene, but it became less common by the later Pliocene and earlier Pleistocene, and extinct by the middle Pleistocene. From the Cercopithecoides lineage arose severally regionally restricted species of different body sizes and locomotor propensities.

  • CERCOPITHECOIDES KERIOENSIS Leakey et al., 2003

Diagnosis Differs from C. kimeui and C. williamsi males in its small size, thin supraorbital tori, narrow interorbital width, strong nuchal crests, a sagittal crest close to inion, and a relatively short and deep mandibular corpus (Leakey et al., 2003). Differs from C. meaveae in its deeper and more sloping mandibular symphysis (Frost and Delson, 2002).

Description The species is represented by the holotype, KNM-LT 9277, a male partial skull.

Age Early Pliocene, ca. 5–4.2 Ma.

African Occurrence Lothagam (Kenya), probably the Apak Member of the Nachukui Formation.

Remarks Cercopithecoides kerioensis is the earliest known species of its genus. The species shares a deep and relatively thin-bodied mandible with other representatives of the genus from the Lonyumun and Lokochot members of the Koobi Fora Formation, and it is likely that this morphology is primitive for the genus (Leakey, 1982).

  • CERCOPITHECOIDES KIMEUI Leakey, 1982
  • Figure 23.2

Diagnosis Larger than C. williamsi with a globular calvaria that is flatter than that of C. williamsi (Leakey, 1982). The mandible is more robust than that of C. williamsi, especially in the thickness of the mandibular corpus and symphysis. Upper molars lower crowned than those of other colobines.

Description This species is represented by the holotype male calvaria and maxillae from middle Bed II Olduvai Gorge, Tanzania, two partial female crania and a series of other cranial and postcranial specimens from the Upper Burgi and KBS members of the Koobi Fora Formation (Jablonski et al., 2008a), a female cranium and mandible from a latest Pliocene to earliest Pleistocene horizon at Hadar, Ethiopia (Frost and Delson, 2002), and a male face and mandible from Rawi Gulley, Kenya (Frost et al., 2003b; Figure 23.2). An isolated lower molar from Bed III at Olduvai Gorge, if it represents C. kimeui, would extend the known range up to as young as 1.2 Ma.

Age Plio-Pleistocene, 2.6–1.5 Ma.

Cercopithecoidea

Figure 23.2 Cercopithecoides kimeui. Lateral and basal views of female cranium KNM-ER 398. The heavy wear on the cheek teeth is characteristic of adults of this species. © National Museums of Kenya.

(p.401) African Occurrence Olduvai Gorge (Tanzania), East Turkana and Rawi Gulley (Kenya), Hadar (Ethiopia).

Remarks A very large colobine monkey with females and males estimated at approximately 25 and 50 kg, respectively (Delson et al., 2000; Frost and Delson, 2002). The muzzle is relatively narrow and inflated just below the infraorbital margin, as in Lophocebus. The mandible is shallow and thick, and supported broad and puffy molar crowns of low relief. The weakly columnar cusps of the molars were covered in thin enamel and wore down quickly to functional obsolescence (Jablonski et al., 2008a). Judging by the nature and degree of tooth wear in most specimens, C. kimeui ate a highly abrasive diet. Although its mandible is thick, it lacks the deep and strongly reinforced mandibular corpus and symphysis and large muscles of mastication found in monkeys that chew tough and highly fibrous vegetation or a lot of vegetation. It is possible that C. kimeui had a relatively soft but highly abrasive diet that has no analogue among living monkeys but that included high percentages of fruits and leaves covered with grit or containing high concentrations of phytoliths (Benefit, 2000). The elbow joint of C. kimeui suggests that the species was highly terrestrial but exhibited considerable forearm flexibility consistent with an adaptation in the species to manipulation of food objects with the hand. This intriguing species is described and discussed at greater length elsewhere (Jablonski et al., 2008a).

  • CERCOPITHECOIDES MEAVEAE Frost and Delson, 2002

Diagnosis Emended after Frost and Delson (2002). Smaller than either C. williamsi or C. kimeui, and comparable to the extant species Nasalis larvatus in body size. Similar to C. kerioensis, but different from C. kimeui and C. williamsi in the absence of a median mental foramen. The mandibular symphysis is more vertically oriented than that of C. kerioensis.

Description This species is known from the holotype partial skeleton from Leadu as well as a maxilla and male mandible from the Sidi Hakoma Member of the Hadar Formation (Frost and Delson, 2002). It exhibits the relatively shallow and robust mandible typical of the genus. The known postcrania (including a tentatively assigned distal humeral fragment from Hadar) exhibit features of the shoulder, elbow, and hip joints associated with terrestrial locomotion (Frost and Delson, 2002).

Age Middle Pliocene, 3.4–3.28 Ma.

African Occurrence Leadu and Hadar (Ethiopia).

Remarks This species is younger than C. kerioensis and generally older than most of the material allocated to C. williamsi and C. kimeui. It is generally similar to C. williamsi in many aspects of its cranial, dental, and postcranial morphology, although it is not as extreme in its adaptations to a terrestrial lifestyle as is C. williamsi from Koobi Fora (Frost and Delson, 2002). Several isolated teeth of similar size to C. meaveae are known from the Omo (Shungura Mbs. B–G), Ethiopia, as well as from the upper Laetolil Beds, Tanzania. These specimens might represent C. meaveae, but at this point are best considered of indeterminate affinity.

  • CERCOPITHECOIDES WILLIAMSI Mollett, 1947
  • Figure 23.3

Diagnosis Larger in body size than all members of the genus except for C. kimeui, being similar in cranial and dental size to Rhinocolobus. Molar teeth possess higher crowns than those of C. kimeui. Differentiated from C. meaveae and C. kerioensis by the presence of a medial mental foramen. Mandibular corpus is shallower and thicker than that of C. kerioensis.

Cercopithecoidea

Figure 23.3 Cercopithecoides williamsi. Selected elements of partial male skeleton KNM-ER 4420. A) Lateral view of right maxilla and mandible; B) dorsal view of humerus. © National Museums of Kenya.

Description Cercopithecoides williamsi is the only fossil colobine known from South Africa and occurs at many Plio-Pleistocene cave sites in the country. Among the most complete cranial specimens are an associated female cranium (p.402) and mandible from Bolt’s Farm (BF 56784) a female cranium from Sterkfontein (STS 394A), and two male crania from Makapan (MP 113 [= M2999], and BPI M3055)(Freedman, 1957; Maier, 1971; Jablonski, 2002). In East Africa, the species is recognized only from East Turkana from whence the most complete specimen of the species, the partial skeleton KNM-ER 4420 (Figure 23.3), has been recovered (Jablonski et al., 2008a).

Age Plio-Pleistocene, 3.5–1.5 Ma.

African Occurrence Lokochot, upper Burgi, and KBS members of the Koobi Fora Formation, East Turkana (Kenya); Leba (Angola); and Taung, Sterkfontein, Makapansgat, Swartkrans, Kromdraai faunal site, Coopers, Swartkrans II, Graveyard, Bolt’s Farm, and Haasgat (South Africa). In South Africa, C. williamsi co-occurs with all fossil papionin species (Heaton, 2006; Jablonski et al., 2008a).

Remarks Cercopithecoides williamsi is a colobine with a large and rounded calvaria, a short, relatively narrow and rounded muzzle, a wide face, large widely spaced rectangular orbits, and a thick supraorbital torus. Sexual dimorphism in cranial shape is apparent in the relatively long and narrow crania of the males that contrast to the females with shorter crania and more rounded calvariae. The shoulder and elbow joint show features (including a massive, superiorly projecting greater tuberosity of humerus, a broad, flange-bearing humeral trochlea and retroflexed olecranon) associated with stability that are characteristic of terrestrial cercopithecoids (Jablonski et al., 2008a).

The skeleton of C. williamsi presents an interesting mixture of features, some of which are similar to living species and others that are not. The cranium and dentition of the species are quite unlike those of other colobines, particularly in the construction of the masticatory apparatus. The gracile construction of the jaws suggests that the species may have subsisted on foods that did not require strong occlusal forces or highly repetitive chewing to be processed, such as unripe fruits and young leaves. The postcranium of C. williamsi exhibits similarities to modern large-bodied colobines and cercopithecines that spend most of their time on the ground, but forage and sleep in trees.

A comparative study of the South and East African morphs of the species is long overdue, in order to determine whether they represent distinct species or members of one widespread and geographically variable species such as the modern temple langur, Semnopithecus entellus, from southern Asia.

  • CERCOPITHECOIDES ALEMAYEHUI Gilbert and Frost, 2008

Diagnosis Gilbert and Frost (2008). Smaller in size than C. williamsi and C. kimeui. Supraorbital torus more projecting than than of C. kerioensis or C. meaveae. Nasal bones longer than those of all other species of Cercopithecoides, extending inferior to the orbital rim.

Description This species is known from a single adult male calvaria and maxilla. In cranial size it is comparable to C. kerioensis and C. meaveae, but it has relatively larger and squarer upper molars. The holotype shows some evidence of healed cranial trauma.

Age Pleistocene, 1.0 Ma.

African Occurrence Daka Member of the Bouri Formation, Middle Awash, Ethiopia.

Remarks This taxon represents the youngest member of this long-lived genus and possibly the smallest. It may represent a cranially autapomorphic relict.

  • cf. CERCOPITHECOIDES

Diagnosis Jablonski et al. (2008a). Smaller in overall size and lacking the distinctly thick and shallow mandibular corpora of other species of Cercopithecoides, but referred to the genus because of the strong similarities in molar shape and cusp configuration. Postcrania share details of humeral and femoral morphology with C. williamsi.

Description A large number of isolated teeth, fragmentary mandibles, and isolated partial long bones, mostly deriving from exposures of the Lonyumun Member at Area 261–A in Allia Bay, east of Lake Turkana are referred to cf. Cercopithecoides.

Age Pliocene, 3.95–3.45 Ma.

African Occurrence Upper Lonyumun and lower Lokochot members of the Koobi Fora Formation (Kenya).

Remarks The specimens assigned to cf. Cercopithecoides were derived from animals of moderate size, probably closely comparable to modern black-and-white colobus monkeys based on mandibular and dental dimensions. The assemblage may include two species distinguished by male canine morphology, one of which bears a close resemblance to Cercopith-ecoides kerioensis from Lothagam.

  • Genus COLOBUS Illiger, 1811

Diagnosis Colobine monkeys with small heads and teeth typical of the subfamily. Unlike Procolobus, the cranial vault lacks an anterior sagittal crest, the supraorbital ridge is thin with small supraorbital foramina or notches, and the pterygoid fossae are not perforate. The distal lophid of the lower third molar is broader than the mesial. Limbs are relatively long, with greatly reduced or absent thumbs, and shortened tarsus. Body size is larger than Procolobus (Procolobus) and Presbytis, but smaller than Nasalis and larger subspecies of Semnopithecus.

Description Remains of Colobus similar or identical to living black-and-white colobus monkeys are abundant at several sites in the Afar region of Ethiopia, particularly in the middle Pleistocene (Kalb et al., 1982a; Frost, 2001a, 2001b; Frost and Alemseged, 2007).

Age Pliocene–present.

African Occurrence Northern and eastern Africa.

Remarks Most fossils of Colobus are found in Pleistocene strata of Africa where they sometimes co-occur with the mangabey, Lophocebus cf. albigena, the baboons Theropithecus oswaldi and Papio hamadryas, and the vervet Chlorocebus aethiops. The notable exception to this is the fragment of a right mandibular fragment with teeth from Kanam East, Kenya; the deposits may be of early Pliocene age (Harrison and Harris, 1996). Species of Colobus are common in forests in much of sub-Saharan Africa today, including riparian habitats within arid regions. Colobus guereza lives in the Afar region today and occurred throughout much of Ethiopia in modern times (Napier, 1985). As discussed, it is possible that Colobus descended from an early form of Cercopithecoides, on the basis of morphological similarities between the two in the mandible, and proximal and distal humerus and femur.

  • COLOBUS FREEDMANI Jablonski and Leakey, 2008
  • Figure 23.4

Diagnosis Swindler and Orlosky (1974); Jablonski and Leakey (2008b). Smaller than modern Colobus guereza and (p.403) distinguished from it by a narrower and slightly more sectorial lower fourth premolar with a small, distally offset lingual cusp. The size and position of the lingual cusp (metaconid) of the P4 distinguishes colobines from cercopithecines, and further distinguishes African from Asian colobines; in C. freedmani, the metaconid is small and distally offset, a condition which is uncommon in modern C. guereza.

Cercopithecoidea

Figure 23.4 Colobus freedmani. Lateral and occlusal views of probable female mandible KNM-ER 44224 (holotype). © National Museums of Kenya.

Description The species is best represented by the holotype mandible, KNM-ER 44224 (Figure 23.4), and by the partial skeleton, KNM-ER 5896, from Koobi Fora.

Age Early Pleistocene, 1.527–1.485 Ma.

African Occurrence Lower part of the Okote Member of the Koobi Fora Formation, East Turkana (Kenya).

Remarks The mandibular corpus and symphysis of C. freedmani are sexually dimorphic, to a slightly greater extent than in modern Colobus. In the postcranium, the clavicle is flatter and slightly less superiorly curved at its distal extremity, and the greater tuberosity of the humerus projects slightly above the level of the humeral head, indicating enhanced muscular stabilization of the shoulder than seen in the modern species (Jablonski and Leakey, 2008b). As in modern colobus, the thumb appears to have been markedly reduced. A complete description of this species is available elsewhere (Jablonski and Leakey, 2008b). Colobus freedmani was very similar in overall appearance to modern C. guereza and was probably an equally lithe and competent arborealist. Its upper limb anatomy suggests that it may have relied slightly less on overhead suspensory locomotion than its modern congener.

  • COLOBUS GUEREZA Rüppell, 1835

Diagnosis The modern black-and-white colobus monkey.

Description The species is best represented by a nearly complete fossil cranium of a young female individual, YPM 19063.

Age Presumed Pleistocene.

African Occurrence Near Wad (Wadi) Medani, central Sudan.

Remarks The cranial morphology of fossil C. guereza was similar to that of modern C. polykomos, with a short face and short nasal bones, well-marked supraorbital ridges, and pronounced postorbital constriction. Similar to C. polykomos in most features except for the buccally bowed cheek tooth rows and relatively small teeth, which more closely resemble C. polykomos polykomos.

The occurrence of modern black-and-white colobus monkeys indicates that during the Pleistocene the Blue Nile supported a lush riparian corridor capable of supporting arboreal monkey populations.

  • COLOBUS sp. indet.

Diagnosis Similar in size and morphology to modern Colobus, but not identifiable at the species level.

Description A heterogeneous group from of mostly Pleistocene age, Colobus sp. indet. is represented mostly by isolated mandibles. The sample from Asbole in the Afar Region of Ethiopia is by far the largest, consisting of many partial crania, mandibles, and fragmentary postcrania (Jablonski, 2002; Frost and Alemseged, 2007).

Age Plio-Pleistocene; late Pleistocene.

African Occurrence Plio-Pleistocene occurrences are from East Africa, including Kanam East (Kenya), the Omo Group, Asbole, Afar Region, and Middle Awash (Ethiopia); the late Pleistocene specimen is from Kazinga (Uganda)(Harrison and Harris, 1996; Jablonski, 2002).

Remarks Most specimens closely resemble modern black-and-white colobus monkeys, with some being slightly smaller and some somewhat larger. This group also probably includes forms more closely related to the modern red colobus, Piliocolobus badius (Frost, 2001b; Frost and Alemseged, 2007). It is interesting that the middle Pleistocene morph assigned to Colobus sp. indet. from the Asbole in the Afar region of Ethiopia is not C. guereza. The relationship of this morph to living species of Colobus and to other fossils of the genus, such as the roughly contemporaneous cranium from Wad Medani, Sudan, is currently unknown (Frost, 2001b). The fossil Afar species is within the size range of most extant Colobus, lacks the large female canines of extant C. guereza, and has relatively large central incisors.

  • Genus KUSERACOLOBUS Frost, 2001

Diagnosis Frost (2001a). The genus is characterized by a short face with anteriorly positioned zygomata and a mandibular corpus that is deep and robust, and deepens posteriorly. The interorbital region is broad, unlike Nasalis, Rhinocolobus, and Libypithecus. Unlike Cercopithecoides and distinguished from extant African colobines by well-developed protocones on the p3 and metaconids of the P4. Distal lophids of the M3 are approximately equal in breadth with the mesial lophids; this condition is similar to Procolobus but unlike Colobus, where the distal lophid is usually broader.

(p.404) Description The type species, K. aramisi, is known from deposits in the Middle Awash ranging in age from 5.2 to 4.4 Ma, with tentative identifications perhaps extending the range back to 5.7 Ma (Frost, 2001b). It is also known from the western margin at Gona dated to 4.5 Ma (Semaw et al., 2005). A second, larger species, K. hafu, has recently been described from Asa Issie and is approximately 4.1 Ma (Hlusko, 2006).

Age Latest Miocene and early Pliocene, 5.2–4.1 Ma.

African Occurrence Afar Region (Ethiopia).

Remarks The geologically younger K. hafu is considerably larger (Hlusko, 2006; Frost et al., 2009). The presence of Kuseracolobus species in the Mio-Pliocene fossil record of northeastern Africa indicates that the colobine radiation was more diverse at an earlier period in Africa than previously recognized. The probable arboreal proclivities of Kuseracolobus species (Hlusko, 2006) also indicate that previous generalizations about the mostly terrestrial locomotor preferences of early colobines need to be revised.

  • KUSERACOLOBUS ARAMISI Frost, 2001
  • Figure 23.5

Diagnosis Same as for genus and considerably smaller than K. hafu (Figure 23.5).

Description Described on the basis of a series of mandibles, maxillae, and dentition from the lower Aramis Member of the Sagantole Formation in the Middle Awash dated to 4.4 Ma (Frost, 2001b). A single mandible—originally thought to perhaps be Libypithecus (Kalb et al., 1982b)—and several isolated teeth from the 5.2 Ma old Kuseralee Member of the Sagantole Formation have been allocated to this species (Frost et al., 2009). A fragmentary series of fossils from the Adu Asa Formation in the Middle Awash may also represent this species and would extend the chronological range to 5.7 Ma (Frost, 2001b). Finally, a series of mandibles, maxillae, and dentition from Gona are also from this species (Semaw et al., 2005).

Age 5.2–4.4 Ma.

African Occurrence Middle Awash and Gona (Ethiopia).

Remarks Kuseracolobus aramisi is similar in size to Cerco-pithecoides meaveae and the extant proboscis monkey of Asia, Nasalis larvatus (Hlusko, 2006; Frost et al., 2009). Postcrania, especially of the forelimb, are similar in some aspects of their morphology to those of Paracolobus, Rhinocolobus, and extant arboreal colobines (Hlusko, 2006).

Cercopithecoidea

Figure 23.5 A) Kuseracolobus aramisi. Left: Occlusal and lateral views of maxilla ARA-VP-6/1686; right: Occlusal and lateral views of male mandible ARA-VP-1/87 (holotype), photographically reversed. B) Comparison of lateral views of partial mandibles of K. aramisi ARA-VP-1/87 (holotype) with K. hafu ASI BVP 2/100. Photograph courtesy of Leslea Hlusko.

(p.405)

  • KUSERACOLOBUS HAFU Hlusko, 2006
  • Figure 23.5

Diagnosis Distinguished from K. aramisi by its larger size (Figure 23.5).

Description The species is known from fragmentary jaws, isolated teeth, and mostly forelimb postcrania as described at length elsewhere (Hlusko, 2006).

Age 4.1 Ma.

African Occurrence Asa Issie area of the Middle Awash Region (Ethiopia).

Remarks Kuseracolobus hafu was larger than any living colobine and larger than most Plio-Pleistocene colobines, with an estimated male body mass between 30 and 40 kg (Hlusko, 2006). The forelimb morphology of the species indicates that it spent a large proportion of its time in the trees, despite its large size.

  • Genus LIBYPITHECUS Stromer, 1913
  • LIBYPITHECUS MARKGRAFI Stromer, 1913

Diagnosis A primitive colobine, lacking clear apomorphies with most other African and Asian colobines (Strasser and Delson, 1987). Libypithecus is also characterized by a maxillary sinus, a feature unknown in extant colobines (Rae et al., 2007). Its long and low cranium, projecting rostrum, and narrow interorbital distance may be symplesiomorphous for cercopithecoids in general, being shared with Victoriapithecus, Nasalis, and Rhinocolobus.

Description Libypithecus is primarily known by the holotype cranium of L. markgrafi and an isolated M1 from Wadi Natrun, Egypt (Stromer, 1914). In addition, a few isolated colobine molars from the late Miocene site of Sahabi, Libya (Meikle, 1987), have been tentatively allocated to L. markgrafi, largely on the basis of size. At both Wadi Natrun and Sahabi L. markgrafi occurs with the early papionin Macaca libyca (Delson, 1973, 1975).

Age Latest Miocene.

African Occurrence Gar Maluk, Wadi Natrun (Egypt).

Remarks The holotype male skull is nearly complete, except that damage renders the join between the middle and lower face and the upper face and vault tenuous, so that their relationship must be estimated (Szalay and Delson, 1979). The premaxilla of the male holotype cranium shows clear evidence of healed trauma. Related to its relatively long rostrum, the calvaria exhibits a marked sagittal crest which increases in height posteriorly. The dentition is typical of colobines with small incisors, the upper lateral incisor being caniniform, and the lowers show the presence of lingual enamel. The protocone on the p3 is reduced as in extant African colobines (Benefit and Pickford, 1986).

  • Genus MICROCOLOBUS Benefit and Pickford, 1986
  • MICROCOLUBUS TUGENENSIS Benefit and Pickford, 1986

Diagnosis A small colobine with a mandibular symphysis that lacks an inferior transverse torus below the genioglossal fossa and a median symphyseal foramen. The P3 exhibits a well-developed heel but lacks a mesiolingual sulcus; the P4 metaconid and protoconid are of almost equal height. The molar cusps are tall and anteriorly directed, and the lingual notches are deep, but the projection of the M1 and M2 cusps above the lingual notch is low compared to other colobines (Benefit and Pickford, 1986). Mandible slightly deeper below M3 than M1 as in Colobus, Rhinopithecus, Nasalis, and Mesopithecus, and absent median symphyseal foramen as in most other colobines. In its dentition, it is most similar to small examples of Mesopithecus pentelici, with moderately high molar cusps angled slightly forward, and well-developed mesial and distal shelves.

Description A rare colobine best known from the holotype, KNM-BN 1740, a nearly complete mandible from Ngeringerowa in the Baringo Basin of Kenya.

Age 9.5–9.0 Ma (Gundling and Hill, 2000).

African Occurrence Ngeringerowa (Kenya).

Remarks The morphological similarities between Microcolobus and the widespread Eurasian Mio-Pliocene colobine Mesopithecus suggest a close phyletic relationship between the two.

  • Genus PARACOLOBUS Leakey, 1969

Diagnosis Based on Hlusko (2007). Paracolobus is a medium to large monkey distinguished from Rhinocolobus by its moderately long cranium, broad muzzle, and wide face. The nasal bones are short but longer than those of Rhinocolobus, and the nasal aperture is long with relatively thick lateral margins. Differs notably from Cercopithecoides in its deep and slender mandibular corpus and the absence of a median mental foramen at the symphysis. The premolars are relatively large, and the p3 has a small protocone, lacking in Cercopithecoides. The molars are tall with angular cusps separated by deep valleys; the maxillary molars are wide relative to length and flare at the cervix. Most features of the postcranium are typical of arboreal colobines, but some are intermediate between those and the terrestrial cercopithecine condition.

Description Paracolobus enkorikae from the terminal Miocene site of Lemudong’o, Kenya, is represented by many gnathic remains and some forelimb postrcrania. Paracolobus chemeroni and P.mutiwa are of late Pliocene age, the former being recognized from a partial skeleton from Chemeron (Kenya) and possibly a mandible and humerus from the Middle Awash (Ethiopia). Paracolobus mutiwa is known from sites within the Omo–Lake Turkana Basin of Kenya and Ethiopia (Leakey, 1982). Examples of the genus not assignable to species are also known from Laetoli, Tanzania (Leakey and Delson, 1987).

Age Terminal Miocene and late Pliocene.

African Occurrence East and northeast Africa.

Remarks Species of Paracolobus are some of the most intriguing fossil monkeys to ever have been recovered because they exhibit suites of postcranial characteristics that have no close modern equivalents. They exhibit a range of body sizes from that of modern black-and-white colobus monkeys (P. enkorikae) to much larger than any living colobine (P. chemeroni). Paracolobus enkorikae and P.chemeroni were probably mostly arboreal, but P.mutiwa may have been far more terrestrial. The recognition of the terminal Miocene species P.enkorikae greatly expands the temporal span of the genus (Hlusko, 2007).

  • PARACOLOBUS CHEMERONI Leakey, 1969
  • Figure 23.6

Diagnosis Larger than P.enkorikae and lacking the squared rostrum, maxillary ridges, and expanded mandibular gonion of P.mutiwa.

(p.406)

Cercopithecoidea

Figure 23.6 Paracolobus chemeroni. Lateral view of male skull KNM-BC 3. Photograph courtesy of Gerald Eck. © National Museums of Kenya.

Description The species is best known from the holotype, a remarkable and nearly complete male skeleton, KNM-BC 3 (Figure 23.6), from Chemeron, Kenya (Leakey, 1969). A single left male mandibular corpus fragment from Matabaietu in the Middle Awash, dated to 2.5 Ma, has been referred to cf. P. chemeroni (Frost, 2001a, 2001b).

Age Pliocene, 3–2 Ma.

African Occurrence Chemeron (Kenya) and Middle Awash (Ethiopia).

Remarks The postcranial anatomy of the species was studied in detail by Birchette whose unpublished dissertation is a classic of descriptive paleontology (Birchette, 1982). Its unique features, including a poorly developed deltoid tuberosity of the humerus, shallow humeral trochlea, and anteriorly inclined olecranon process of the ulna, were interpreted as being consistent with a predominantly arboreal lifestyle. The body mass of the species was very great for a monkey, with an estimated range for males of 39–46 kg (Delson et al., 2000; Hlusko, 2007).

  • PARACOLOBUS ENKORIKAE Hlusko, 2007
  • Figure 23.7

Diagnosis Hlusko (2007). Distinguished from P.mutiwa and from Kuseracolobus, Microcolobus, and Rhinocolobus by the absence of significant mandibular gonial expansion, and from Cercopithecoides by a mandibular cross section that is less robust and rounded; differs from P.chemeroni and P.mutiwa mainly in its much smaller size.

Description Known from the holotype nearly complete mandible, KNM-NK 44770 (Figure 23.7), numerous partial jaws, and isolated teeth (Hlusko, 2007).

Age Terminal Miocene, 6 Ma.

African Occurrence Lemudong’o, Narok District (Kenya).

Remarks Paracolobus enkorikae exhibits close affinities with P.chemeroni (Leakey, 1982) and may be its ancestor. It shares overall dental proportions with Victoriapithecus macinnesi. On the basis of study of the mandibular morphology of the species, Hlusko has suggested that Paracolobus may have closer evolutionary affinities to modern Colobus than do the Plio-Pleistocene species of Rhinocolobus, Cercopithecoides, and Kuseracolobus.

  • PARACOLOBUS MUTIWA Leakey, 1982

Diagnosis Distinguished from other species of Paracolobus by a high muzzle, maxillary fossae and ridges, wide frontal process of the zygoma, narrower interorbital region, and less sharply converging temporal lines. The gonion is greatly expanded.

Description The species is known from the holotype female fragmentary cranium from East Turkana, KNM-ER 3843, and numerous gnathic fragments and isolated teeth (Leakey, 1982). A partial skeleton from West Turkana has not been fully described (Harris et al., 1988).

Age Pliocene, 3.36–1.88 Ma.

African Occurrence East and West Turkana (Kenya), and the Omo Valley (Ethiopia).

Remarks Preliminary study of the partial skeleton from West Turkana indicates that the species shows strong positive allometry of the skull and teeth relative to the postcranium and that it may have been strongly terrestrial (Jablonski, unpublished observations).

  • PARACOLOBUS sp. indet.

Diagnosis Distinguished from P.chemeroni and P.mutiwa by the smaller size of the teeth, but remains are insufficient to allow assignment to species.

Description A large number of fragmentary mandibular and maxillary specimens from Laetoli, Tanzania, the best being LAET 247, 259, and 4596, and two femoral fragments, LAET 247 and LAET 327, and several isolated teeth (Leakey and Delson, 1987); isolated molars and a distal humerus from the Western Rift (Senut, 1994); and, possibly, three fragments, including an isolated M3 from Makapansgat (Eisenhart, 1974).

(p.407)

Cercopithecoidea

Figure 23.7 Paracolobus enkorikae. Views of male mandible KNM-NK 44770 (holotype). A) Lingual view of right mandible; B) buccal view of right mandible; C) occlusal view of right and left mandibles; D) lingual view of left mandible; E) buccal view of left mandible. Photograph courtesy of Leslea Hlusko. © National Museums of Kenya.

Age Pliocene, 3.8–?2.5 Ma.

African Occurrence Laetoli (Tanzania), and possibly Western Rift (Uganda), and Makapansgat (South Africa).

Remarks The morphology of the teeth and femur indicate affinities with Paracolobus, but it is possible that at least the Laetoli assemblage represents a different taxon altogether (Leakey, 1982; Leakey and Delson, 1987; Jablonski et al., 2008a). The occurrences of the genus in Uganda and South Africa must be viewed with doubt pending further discoveries and study.

  • Genus RHINOCOLOBUS Leakey, 1982
  • RHINOCOLOBUS TURKANAENSIS Leakey, 1982
  • Figure 23.8

Diagnosis After Jablonski et al. (2008b). A large colobine, which shares with Libypithecus, Dolichopithecus, and modern Nasalis but not other colobines a long braincase and muzzle, narrow interorbital distance, marked postorbital constriction, and relatively small orbits. The mandibular corpus is thin and deep and the gonion expanded; a median symphyseal foramen is present. Distinguished from Libypithecus by its larger overall size, larger and more rounded calvaria, longer muzzle, and lack of a large sagittal crest, and from Nasalis by short nasal bones, wide malar region, postglabellar sulcus, and nuchal crests. The near absence of nasal bones in Rhinocolobus is remarkable and distinguishes it from all other colobines save the Asian odd-nosed monkey genus, Rhinopithecus. In the postcranium, Rhinocolobus is distinguished from other large colobines by its large and medially protuberant medial humeral epicondyle and medially inwardly curved distal humeral shaft.

Description The species is represented by abundant remains, including a well-preserved female skull (KNM-ER 1485; Figure 23.8), and a partial male skeleton (KNM-ER 1542), which are fully described and reconstructed elsewhere (Jablonski et al., 2008a). Several fragmentary gnathic remains and an isolated humerus from the Sidi Hakoma and Denen Dora members of the Hadar Formation (3.4–3.2 Ma) have been tentatively allocated to R. turkanaensis (Frost and Delson, 2002).

Age Plio-Pleistocene, 3.4–1.5 Ma.

African Occurrence Shungura and Hadar Formations (Ethiopia) and the Koobi Fora Formation, East Turkana (Kenya).

Remarks Rhinocolobus was one of the largest known colobines, exceeding extant African colobines and the widespread fossil species, Cercopithecoides williamsi, in body size, but smaller in tooth and body size than C. kimeui, Paracolobus chemeroni, and P.mutiwa. It was highly sexually dimorphic in body mass, with males being an estimated 31 kg and females 17 kg (Delson et al., 2000); its canines and P3 were also highly sexually dimorphic. Rhinocolobus was predominantly arboreal, as judged by the similarities of its postcranium to that of large extant species such as the equally sexually dimorphic odd-nosed Asian colobines Nasalis larvatus and Rhinopithecus brelichi.

(p.408)

Cercopithecoidea

Figure 23.8 Rhinocolobus turkanaensis. Lateral and vertical views of female skull KNM-ER 1485. © National Museums of Kenya.

  • Subfamily CERCOPITHECINAE Gray, 1821
  • Tribe CERCOPITHECINI Gray, 1821
  • Genus CERCOPITHECUS Brunnich, 1772
  • CERCOPITHECUS sp. indet.

Diagnosis Small cercopithecines comparable in size and morphology to living species of Cercopithecus, and characterized by relatively arboreal locomotor behavior compared to Chlorocebus. Like all members of the tribe, the M3 lacks a hypoconulid.

Description Cercopithecus has been recognized from gnathic fragments and isolated teeth from the Omo (Eck and Howell, 1972; Eck and Jablonski, 1987), from a left fragmentary mandible from Kanam East (M 15923)(Harrison and Harris, 1996), from fragmentary jaws, isolated teeth, an ulna and a femur as two morphs (Cercopithecus sp. indet. A and B) from Koobi Fora (Jablonski et al., 2008b), a jaw fragment from Kuguta (Napier, 1985), isolated teeth from late Pleistocene levels at Olduvai Gorge (Tanzania) and Loboi (Kenya)(Leakey, 1988), and a series of isolated teeth from a later Pliestocene deposit near Taung (South Africa)(Delson, 1984).

Age Pliocene and Pleistocene.

African Occurrence The Omo–Lake Turkana Basin (Ethiopia and Kenya); Kuguta and Kanam East (Kenya); later Pleistocene deposits near Taung (South Africa).

Remarks The scarcity of Cercopithecus fossils may be due to their genuine rarity in the past but is equally likely to be due to their small size, which renders them susceptible to destruction by carnivores or scavengers or to rapid decomposition by the elements. For whatever reason, the fossil record of Cercopithecus is sparse (Jablonski et al., 2008b). The smaller morph (Cercopithecus sp. indet. B) recognized at Koobi Fora may represent the Pliocene ancestor of the modern talapoin, the smallest extant guenon (Jablonski et al., 2008b). Several of the fragmentary specimens allocated to this genus may in fact represent Chlorocebus as they are craniodentally similar, and only recently have species (C. aethiops, and the C. lhoesti species group) previously included in Cercopithecus been referred to Chlorocebus (Tosi et al., 2002a, 2003b, 2004, 2005; Xing et al., 2007).

(p.409)

  • Genus CHLOROCEBUS Gray, 1870

Diagnosis Cercopithecin monkeys of average to large size for the tribe. Characterized by adaptations for terrestrial locomotion. Sexual swellings are absent.

Description Best known from a series of fossils from middle Pleistocene deposits from Asbole and the Middle Awash (Ethiopia).

Age Middle Pleistocene, 0.6 Ma and younger.

African Occurrence Eastern Africa.

Remarks Recent molecular analyses have consistently grouped the patas monkeys (formerly Erythrocebus patas) with the more terrestrially adapted species traditionally included in Cercopithecus: C. aethiops, C. lhoesti, C. solatus, and C. preussi (Tosi et al., 2002a, 2002b, 2003b, 2004, 2005). Following the recommendations of Tosi and colleagues (Tosi et al., 2004), these taxa are included in the genus Chlorocebus, which has priority over Erythrocebus and Allochrocebus. Thus, all of the guenon species that are more terrestrially adapted (Gebo and Sargis, 1994) and that occur in more open habitat types, such as Ch. aethiops and Ch. patas (Napier, 1981), are grouped in this genus. To varying degrees, this arrangement has also received some support from karyotypic analyses and vocalizations (Dutrillaux et al., 1988; Gautier, 1988). Molecular estimates indicate that Chlorocebus diverged from the Miopithecus + Cercopithecus group approximately 8 Ma (Tosi et al., 2005).

Thus far, the only fossil material allocated to this genus derives from the middle Pleistocene of the Afar (Ethiopia) (Kalb et al., 1982b; Frost, 2001a; Frost and Alemseged, 2007), but fragmentary specimens from eastern and southern Africa that have been allocated to Cercopithecus in the past are likely to represent this genus as well.

  • Cf. CHLOROCEBUS aff. AETHIOPS

Diagnosis A guenon similar in size to the extant vervet monkey, larger than Miopithecus and smaller than Ch. patas. Rostrum shorter and less squared than that of Ch. patas. The i2 is larger relative to the i1 than is the case in Miopithecus, Cercopithecus or Ch. lhoesti. The molar cusps are also not as tall and sharp as are those of Ch. lhoesti.

Description This species is best represented by a series of gnathic remains from Asbole, dated to approximately 600 Ka, as well as the younger site of Andalee in the Middle Awash (Ethiopia)(Frost, 2007b; Frost and Alemseged, 2007).

Age Middle Pleistocene, 0.6 Ma and younger.

African Occurrence Asbole and Middle Awash (Ethiopia).

Remarks The material assigned to this taxon shows affinities with the extant vervet monkey, present throughout diverse African habitats. The fossil assemblages derive from middle Pleistocene sites in the Afar region that were possibly closer to a major stream, such as the paleo-Awash, than other contemporary sites, such as Bodo and the other Dawaitoli Formation sites (Kalb et al., 1982b; Frost and Alemseged, 2007).

  • Cf. CHLOROCEBUS cf. PATAS

Diagnosis Comparable in size to extant Ch. patas, but larger than other known guenons. Rostrum is relatively long and narrow, and the palate is relatively deep.

Description This species is known from a few cranial fragments and an os coxae and femur from Asbole (Ethiopia). A few specimens from Andalee (Ethiopia) may also represent this taxon (Frost, 2007b).

Age Middle Pleistocene, 0.6 Ma and possibly younger.

African Occurrence Asbole and Middle Awash (Ethiopia).

Remarks If this material belongs to the patas monkey, then it would represent an eastward extension of the species’ known range. The femur, tentatively allocated to this taxon, has a relatively low neck-shaft angle and tall greater trochanter, both indicating a relatively terrestrial locomotor mode.

  • Tribe PAPIONINI Burnett, 1828
  • Subtribe MACACINA Owen, 1843
  • Genus MACACA Lacépède, 1799

Diagnosis Small to large size monkeys with narrow interorbital regions, rounded muzzles of moderate length, molars with flared sides and relatively short crowns, and moderate to great sexual dimorphism in the canine-premolar complex, and postcranium. Distinguished from other papionins by the general absence of suborbital fossae and maxillary ridges, presence of a maxillary sinus, and a lack of extreme lateral flare of the molars.

Description The representation of this genus in Africa is small compared to that in Asia, where it is the dominant papionin of the past and present. The African fossil species are similar in morphology to the modern Barbary macaque, Macaca sylvanus.

Age Late Miocene—Recent.

African Occurrence Northern Africa.

Remarks Today, Macaca is the most widely distributed nonhuman primate genus, with M. sylvanus occurring in North Africa and between 14 and 19 species distributed across southern and eastern Asia. It also spans the widest range of ecosystems including temperate forests in Japan, high altitude areas of the Himalayan foothills, as well as tropical forests and woodland (Fooden, 1980; Szalay and Delson, 1979; Jablonski, 2002). The genus has an extensive fossil record throughout the Pliocene and Pleistocene of Europe and Asia (Delson, 1980; Jablonski, 2002). Delson proposed that the North African and Eurasian Macaca became isolated from the sub-Saharan papionins in the late Miocene, perhaps due to the Sahara becoming more of a biogeographic barrier (Delson, 1975, 1980). The timing and biogeography of this scenario has essentially been corroborated by molecular analyses (Morales and Melnick, 1998; Tosi et al., 2000, 2002b, 2003b; Jablonski, 2002; Xing et al., 2005). Most morphological and molecular analyses agree on the position of this genus as the sister to all other extant papionins, and it is often placed in its own subtribe Macacina, with the remaining genera in the subtribe Papionina (Delson, 1973; Strasser and Delson, 1979, 1987; Jablonski, 2002).

The oldest material that may represent this genus is a series of isolated teeth from Menacer (formerly Marceau, Algeria), where it is found in association with a relatively large species of colobine. This population was initially named Macaca flandrini, but the holotype was in fact a specimen representing the co-occurring colobine. Therefore, the papionin material has remained unnamed pending discovery of more diagnostic morphology. Menacer has been faunally dated to the late Miocene (Geraads, 1987). Delson tentatively allocated this material to Macaca largely on the basis of geography but noted that it lacks any features distinguishing it from a stem papionin (Delson, 1975, 1980; Szalay and Delson, 1979).

(p.410) Three isolated teeth from the middle Pliocene site of Ahl al Oughlam (Morocco) have been tentatively assigned to Macaca, again based largely on biogeography (Alemseged and Geraads, 1998), as has an isolated distal humeral fragment from Garaet Ichkeul (Tunisia)(Delson, 1975, 1980), but the latter interpretation is not universally accepted (Alemseged and Geraads, 1998).

  • MACACA LIBYCA (Stromer, 1920)

Diagnosis A medium-sized papionin similar to extant M. sylvanus in both size and the relatively few preserved aspects of its morphology.

Description The sample from Wadi Natrun consists of a few mandibular fragments and isolated teeth (Stromer, 1920; Delson, 1975, 1980; Szalay and Delson, 1979). Additional mandibular fragments from Sahabi may also represent this species (Meikle, 1987).

Age Late Miocene—earliest Pliocene.

African Occurrence North Africa, Wadi Natrun (Egypt), and Sahabi (Libya).

Remarks Macaca libyca co-occurs with the colobine Libypithecus markgrafi (discussed earlier) at Wadi Natrun and possibly Sahabi. Due to the ambiguous nature of the morphology preserved by the relatively fragmentary specimens, it has generally been included in Macaca for biogeographic reasons but considered distinct from M. sylvanus due to its age, which approximates molecular estimates for the last common ancestor of the genus (Delson, 1975, 1980; Szalay and Delson, 1979; Tosi et al., 2003a).

  • MACACA SYLVANUS (Linnaeus, 1758)

Diagnosis Medium-sized papionin, with robust supraorbital torus, lacking maxillary or mandibular corpus fossae. Dentition is typical of the tribe. Limbs are relatively robust, and the external tail is reduced to a stub. Lacks the derived reproductive anatomy of many Asian species.

Description Fragmentary jaws and teeth from several sites in North Africa have been assigned to this species.

Age Middle and late Pleistocene, and possibly Pliocene.

African Occurrence Macaca sylvanus is known from Ain Mefta and Tamar Hat (Algeria), as well as from two isolated teeth tentatively included from the Pliocene site from Ain Brimba (Tunisia), as Macaca aff. sylvanus (Delson, 1980).

Remarks In Europe, this species has a much more extensive chronological range than in Africa, extending back to the Ruscinian, and is recognized in three chronological subspecies: M. s. prisca, M. s. florentina, and M. s. pliocena (Delson, 1980), but the relationship of the mostly younger African material to these European forms is unclear.

  • Subtribe PAPIONINA Burnett, 1828
  • Genus CERCOCEBUS Geoffroy Saint-Hilaire, 1812
  • CERCOCEBUS sp. indet.

Diagnosis Medium-sized monkeys distinguished from Cercopithecus and Macaca by the presence of suborbital fossae and large incisors relative to molar size; distinguished from Lophocebus by relatively shallow maxillary fossae and mandibular molars strongly laterally flared at the cervix.

Description The fossil evidence for the modern genus of Cercocebus mangabeys is fragmentary and comprises only a partial cranium from Makapansgat (M3057/8/9, M218), fragmentary jaws from Kromdraai (Eisenhart, 1974), and possibly some other gnathic remains previously assigned to female Parapapio jonesi from Swartkrans, such as SK 414, SK 543, and SK573a and b (Gilbert, 2007b). East African specimens previously referred to Cercocebus (Jablonski, 2002) are now considered Lophocebus cf. albigena (Jablonski et al., 2008b) and are described later in this chapter.

Age Late Pliocene.

African Occurrence Makapansgat, Kromdraai, and ?Swartkrans (South Africa).

Remarks The Cercocebus lineage has recently been recognized in South Africa, from material originally assigned to Parapapio antiquus (Gilbert, 2007b). (See later discussion of Procercocebus antiquus.) Molecular and morphological evidence has conclusively demonstrated that the mangabeys are diphyletic and that Cercocebus belongs to the Cercocebus/ Mandrillus clade, while Lophocebus belongs to the Lophocebus/ Papio/Theropithecus clade (Cronin and Sarich, 1976; Page and Goodman, 2001; Gilbert, 2007b). The existence of a fossil representative of the Cercocebus lineage in southern Africa suggests that modern Cercocebus mangabeys achieved their current equatorial distribution following a Pleistocene dispersal from southern Africa (Gilbert, 2007b), but other biogeographic interpretations are possible, as discussed later.

  • Genus DINOPITHECUS Broom, 1937
  • DINOPITHECUS INGENS Broom, 1937
  • Figure 23.9

Diagnosis Distinguished from other papionins by its very large size, broad interorbital region, the robustness and rugosity of cranial surfaces associated with the masticatory and nuchal musculature, the strength of the temporal lines in both sexes (and sagittal crest in males), strong nuchal crests, and large, broad molars that often show accessory cuspules and short P3s with large anterior foveae in males (Freedman, 1957). Distinguished from Papio by its general lack of maxillary and mandibular corpus fossae. Dinopithecus ingens was sexually dimorphic.

Description Remains of the species are known from two sites only, the type locality of Schurweberg (Skurweberg; 1 specimen, SB 7) and Swartkrans (over 30 specimens). Among the collection from Swartkrans are three nearly complete crania of females (SK 553, SK 600, and SK 603; Figure 23.9) and a fragmentary cranium of a male (SK 599) lacking the muzzle (Simons and Delson, 1978; Szalay and Delson, 1979; Delson and Dean, 1993; Heaton, 2006).

Age Late Pliocene.

African Occurrence Schurweberg (Skurweberg) and Swartkrans (South Africa).

Remarks The phyletic affinities, distribution, and classification of Dinopithecus have been a subject of some controversy for many years, partly because the most complete specimens referred to the taxon are female, and the majority of diagnostic papionin apomorphies are expressed only in males. Delson proposed that Dinopithecus was best considered an extinct subgenus of Papio and that several large fossil papionins from eastern and southwestern Africa could be accommodated within it; this view has been adopted by Frost and Heaton but is not followed here as these similarities may be primitive retentions. Several papionin fossils from Leba, Angola, considered possibly referable to Dinopithecus, have been argued by one of us (N.G.J.) to belong to an early, large representative of Theropithecus (Jablonski, 1994), as discussed later. The other author (S.F.) does not concur with this allocation. Similarities between the molar teeth of D. ingens and Gorgopithecus major noted in an early study (Freedman, 1957) (p.411) may indicate phyletic propinquity between these two large and unusual papionins, but the lack of comparable facial remains precludes necessary study.

Cercopithecoidea

Figure 23.9 Dinopithecus ingens. Lateral view of female cranium SK 553. Photograph courtesy of Gerald Eck.

  • Genus GORGOPITHECUS Broom and Robinson, 1949
  • GORGOPITHECUS MAJOR (Broom, 1940)

Diagnosis Distinguished from other papionins by its relatively short, high, and narrow muzzle, deep maxillary and mandibular fossae, great interorbital breadth, and long calvaria.

Description This species is recognized with confidence only from Kromdraai and is best known from a single specimen of crushed male cranium, KA 192, a partial female cranium, KA 153, and two badly damaged mandibles (KA 150 and KA 152). A single palate from Swartkrans has also been tentatively allocated to this species (Delson, 1984).

Age Plio-Pleistocene.

African Occurrence Kromdraai (South Africa).

Remarks Gorgopithecus major was one of two Plio-Pleistocene papionins (along with Papio angusticeps) recognized only at Kromdraai; it is probably also present at Coopers A and possibly Coopers B (Delson, 1984). The distinctive facial skeleton of this species features maxillae dropping steeply inferiorly from the sides of the nasal bones and nasal aperture to the alveolar margin. The short nasals are oriented almost horizontally to the posterior edge of the nasal aperture; the muzzle drops steeply from there to the anterior margin of the aperture on the premaxilla (Freedman, 1957). The zygomatic arch in both sexes is heavily built and the bizygomatic breadth is great. As mentioned earlier, the molars of G. major exhibit similarities to Dinopithecus ingens and may denote a close phyletic relationship between the two.

  • Genus LOPHOCEBUS Palmer, 1903

Description Lophocebus is recognized from a large collection of jaws and some postcrania from the Koobi Fora Formation, from a small but diagnostic collection of teeth and a temporal bone fragment from Kanam East, and tentatively from Olduvai and Omo.

Age Plio-Pleistocene.

African Occurrence Kanam East and East Turkana (Kenya), and possibly Olduvai (Tanzania) and Omo (Ethiopia).

Remarks Recognition of the diphyly of the mangabeys, discussed in connection with Cercocebus earlier, has led to renewed interest in the fossil history of both mangabey lineages. Lophocebus, as attested by the assemblages at East Turkana and Kanam East, diverged from the common ancestor of Lophocebus/Papio/Theropithecus in the late Miocene or early Pliocene in eastern Africa, probably from a species of Parapapio. Lophocebus mangabeys occupied the eastern Rift Valley through the middle Pleistocene, apparently favoring the riparian and forest habitats there. When those habitats deteriorated in the face of increasing Pleistocene seasonality, the mangabeys shifted their distribution westward. Today, Lophocebus is found only in central and western equatorial Africa, from the western Rift westward. It is significant that Lophocebus and Pan share this pattern of biogeographic history (McBrearty and Jablonski, 2005).

  • LOPHOCEBUS cf. ALBIGENA (Gray, 1850)
  • Figure 23.10

Diagnosis Larger in size than the modern gray-cheeked mangabey, Lophocebus albigena, and morphologically distinguished from it only in its consistently large and broad M3 hypoconulid.

Description The most diagnostic examples of this morph are from the Koobi Fora Formation, where they comprise mostly gnathic remains (Figure 23.10), the best being female left partial maxillae KNM-ER 595 and 44260, male maxillae KNM-ER 827 and 3090, and many mandibles or parts thereof, including female specimens KNM-ER 898 and 6014 and partial male specimens KNM-ER 594 and 6063. A humerus and proximal femur are also included in the sample. A mandible from Upper Bed II at Olduvai (Tanzania) and another mandible, originally identified as possibly Parapapio (Leakey and Leakey, 1976) from Shungura Member K (Ethiopia), Omo K6 ‘70 C146, may also represent this species (Eck, 1976).

Age 2.0–1.38 Ma.

(p.412)

Cercopithecoidea

Figure 23.10 Lophocebus cf. albigena. A) Lateral and occlusal views of partial left maxilla KNM-ER 40459; B) lateral and occlusal views of male partial right mandible KNM-ER 594. © National Museums of Kenya.

African Occurrence KBS and Okote members, Koobi Fora Formation, East Turkana (Kenya); Upper Bed II, Olduvai (Tanzania); and, possibly, Shungura Formation, Omo Group (Ethiopia).

Remarks This species was originally identified as Cercocebus sp., but at that time, Lophocebus was a junior synonym of Cercocebus, and the Koobi Fora material was suggested to be most similar to the “albigena-group” (Leakey and Leakey, 1976). Like modern L. albigena, the fossil form exhibits moderate sexual dimorphism in canine and cranial dimensions. The molars of the species denote a frugivorous diet similar to that of the modern gray-cheeked mangabey, which uses its large incisors for preparing thick-husked fruits and seeds (Hylander, 1975). The postcranial remains of L. cf. albigena indicate that the species was an arboreal climber, with a hindlimb adapted for stability at the hip joint (Jablonski et al., 2008b). The co-occurrence of the gray-cheeked mangabey and an early form of black-and-white colobus monkey (Colobus freedmani) in the Lake Turkana Basin in the early Pleistocene was the first step in the emergence of two of the modern cercopithecoid fauna in East Africa.

  • LOPHOCEBUS sp. indet.

Diagnosis Same as for genus.

Description A small assemblage from Kanam East, consisting of associated and heavily worn upper central incisors and M2 (M15922) and a fragment of right temporal bone (M18800; Harrison and Harris, 1996), has been referred to Lophocebus.

Age Plio-Pleistocene.

African Occurrence Kanam East, Kenya.

Remarks The distinctively robust and convexly curved incisors and the pronounced buccal flare of the isolated molar indicate a probable attribution to Lophocebus (Harrison and Harris, 1996).

  • Genus PAPIO Müller, 1773

Diagnosis A papionin of moderate to large body size with elongated muzzles in males; a strong supraorbital torus with a prominent glabella; extreme levels of canine-premolar and somatic sexual dimorphism; and shoulder, elbow, and hip joints strongly adapted for terrestriality. Following Heaton, the genus is distinguished from Parapapio by a sharp anteorbital drop near the glabella, leading to a muzzle that slopes gradually toward alveolare, by maxillary fossae in both sexes (which also distinguishes it from Dinopithecus), and by a flattened muzzle dorsum and sharp maxillary ridges in males (Heaton, 2006).

Description Taung and Sterkfontein have yielded examples of the small and short-muzzled P.izodi, including the type specimen TP 7. Heaton concluded that most of the specimens of Papio from late Pliocene sediments at Sterkfontein previously allocated to P. hamadryas robinsoni, including female SWP 2946, and male SWP Un2, were in fact P. izodi (Heaton, 2006). The fossil morph of the modern baboon, P.hamadryas robinsoni, appears to be a valid and widespread form present at most South African Plio-Pleistocene sites between 2.0 and 1.0 Ma except Schurweberg (Heaton, 2006). The modern savanna baboon, Papio hamadryas, is represented at the 600 Ka site of Asbole, Ethiopia (Alemseged and Geraads, 2000) and is probably also present at Bodo, in the Middle Awash as attested by two isolated molars (Frost et al., 2009). It is also known by a juvenile cranium from probable middle Pleistocene levels at Olduvai (Remane, 1925).

Age Plio-Pleistocene–Recent.

African Occurrence Northeast and South Africa.

Remarks Classification of extinct and extant species within Papio has been unstable for decades due to problems of species recognition. The assignment of all living forms of the genus into several subspecies within the single species P. hamadryas, following Groves (Groves, 1989, 2001; Frost et al., 2003a), is advocated by most scholars and is followed here.

The widespread presence of fossil members of the genus in Africa over space and time was assumed by many early paleontologists in light of the ubiquity of modern Papio baboons. Recent molecular and paleontological studies have cast doubt on this interpretation, however. Papio appears to have arisen in the terminal Pliocene, possibly first in South Africa (Newman et al., 2004; Wildman et al., 2004). Fossils of Papio hamadryas do not appear in eastern and northeastern Africa until the middle Pleistocene (Jablonski and Leakey, 2008a; Jablonski et al., 2008b).

Most of the fossil evidence for true Papio derives from South Africa, where the history of discovery and naming of fossil representatives of the genus has been long and tortured, partly because of the absence of morphological and (p.413) metrical distinctions between the molars of Papio and Parapapio (Freedman, 1957; McKee, 1993; Heaton, 2006). Heaton’s recent study has resulted in significant clarification of the morphological distinctions between the two genera, and has shed light on their probable chronologies in South Africa (Heaton, 2006).

Controversy surrounds the presence of Papio species outside of South Africa prior to the Pleistocene, partly because most examples identified as such have been fragmentary or immature. A relatively small species of this genus was identified in Ethiopia from the 2.5 Ma Hatayae Member of the Bouri Formation based on a partial female cranium. A relatively large morph from Members E–G of the Shungura Formation is known from two female partial crania and a male rostrum (Eck, 1976; Delson and Dean, 1993; de Heinzelin et al., 1999; Frost, 20 01b). This series has been attributed by Delson and Dean to Dinopithecus and associated with the significantly older holotype of Theropithecus quadratirostris from the Usno Formation (Delson and Dean, 1993). Eck and Jablonski considered the Usno holotype to be an unquestioned Theropithecus and did not discuss the status of the other large papionin from the Shungura Formation (Eck and Jablonski, 1984). In this chapter, the Usno holotype is discussed under Theropithecus, but the large Shungura papionin is considered to be a large species of Papio or, possibly, Dinopithecus. A distal humerus and isolated deciduous premolar from Laetoli, Tanzania were referred tentatively to Papio (Leakey and Delson, 1987). In the absence of clear Papio synapomorphies, all of these cases are more parsimoniously considered as Parapapio. Specimens from high in the Koobi Fora succession reported as close in size to modern Papio (Harris et al., 1988) have been referred to Parapapio, as discussed later in this chapter and elsewhere (Jablonski et al., 2008b).

  • PAPIO HAMADRYAS (Linnaeus, 1758)

Diagnosis The modern savanna baboon, distinguished from other species of the genus by sharp maxillary ridges in males.

Description This heterogeneous group of modern Papio baboons comprises two morphs from South Africa: P.hamadryas robinsoni Freedman, 1957 and P.hamadryas ursinus Kerr, 1782, and at least two from eastern Africa: P.hamadryas subsp. indet., and P.h.hamadryas or P. h. anubis. None save P. h. robinsoni are known from significant samples.

Age Latest Pliocene and Pleistocene.

African Occurrence Papio hamadryas robinsoni: Sterkfontein Member 5, Kromdraai A and B, Drimolen, Swartkrans, and Bolt’s Farm; Papio hamadryas ursinus: Pretoria, Transvaal; Papio hamadryas ssp. indet.: Olduvai Gorge (Tanzania); Asbole, Afar Region, (Ethiopia).

Remarks The South African origin of Papio hamadryas in the late Pliocene is attested to by molecular evidence (Newman et al., 2004; Wildman et al., 2004), and by the absence of any unambiguous fossils assignable to the taxon before that time. The middle Pleistocene fossils of the species from Asbole is probably either P. h. hamadryas or P. h. anubis (Frost and Alemseged, 2007). The specimen of Papio from an unknown level at Olduvai (Remane, 1925) appears to be a modern Papio because, despite its juvenile status, the concave profile of the orbital region and sloping muzzle clearly identify the specimen as Papio as opposed to Parapapio and its bulbous and low-crowned molars distinguish it from Theropithecus.

  • PAPIO IZODI Gear, 1926

Diagnosis Following Heaton, the species exhibits well-developed supraorbital tori in both sexes and a sharp anteorbital drop from glabella, and is distinguished from other Papio species and Parapapio by its lightly developed maxillary ridges, and well-defined maxillary fossae sited over the in fraorbital foramina (Heaton, 20 06). Delson showed that it had larger orbits and teeth than either modern P.h.kindae or fossil P. [h.] angusticeps of similar size (Delson, 1988).

Description Represented by the lectotype TP 7 (formerly AD 992) and numerous other good specimens from Taung and from many mostly fragmentary cranial remains from Sterkfontein, including the partial male skull SWP 29a and b, and the female SWP 2946 (Freedman, 1965; McKee, 1993; Heaton, 2006).

Age Plio-Pleistocene.

African Occurrence Taung, Sterkfontein Members 2 and 4, Kromdraai, and Coopers, (South Africa).

Remarks Papio izodi appears to be the most ancient species of true Papio, and may be ancestral or at least phyletically close to P.hamadryas. Papio izodi is conceived here as including most specimens originally assigned to P.angusticeps (Szalay and Delson, 1979), but Heaton (2006) recognizes the latter species as distinct and endemic to Kromdraai, along with Gorgopithecus major.

  • Genus PARAPAPIO Jones, 1937

Diagnosis Freedman (1957); Eisenhart (1974); Heaton (2006); Gilbert (2007b). A papionin of medium to large size distinguished by a straight or only slightly concave facial profile from nasion to rhinion, a lightly built and nonprojecting supraorbital torus, weak or absent maxillary ridges, poorly excavated or absent maxillary and mandibular fossae, and moderate sexual dimorphism in the cranium and caninepremolar complex.

Description Many morphs of this genus are known, with the earliest being those in eastern Africa. The greatest diversification of Parapapio took place in southern Africa, after a presumed southward dispersal event. Species of the genus were probably ancestral to all of the papionins that emerged in the Pliocene and Pleistocene—that is, to the earliest forms of Theropithecus, Lophocebus, Papio, Mandrillus, and Cercocebus. The precise nature and timing of this diversification have not been illumined by the fossil record, but molecular evidence for the timing of the major cladogenetic events within the Papionina leaves little doubt that the African radiation of the subtribe derived from Parapapio ancestry.

Age Late Miocene–early Pleistocene.

African Occurrence Eastern and southern Africa.

Remarks The lack of unambiguous and well-defined apomorphies has resulted in the repeated reassessment and reallocation of species between and among Parapapio morphs, and between Parapapio and Papio. This has resulted in a confusing literature and multiple conflicting synonymies (Leakey and Delson, 1987; Jablonski et al., 2008b). Recent studies have shed light on the diversity of Parapapio in southern and eastern Africa, respectively, but Pan-African comparisons are urgently needed in order to determine which species are shared between regions and the timing and nature of dispersal or vicariant events.

The earliest and most primitive members of the genus are known from East Africa, in the form of the late Miocene (p.414) species, P.lothagamensis, and the early Pliocene species P.ado from Laetoli and P. cf. ado from Allia Bay at Koobi Fora and Kanapoi. Parapapio appears to have undergone its first diversification event in the Mio-Pliocene of eastern Africa. One possible scenario is as follows: In the early to middle Pliocene, an East African Parapapio species, possibly P. jonesi, dispersed to southern Africa, where it or a descendant form underwent regional diversification to give rise to the many species of Parapapio known from the Plio-Pleistocene cave sites of South Africa. The ancestor of modern Papio almost certainly arose from Parapapio, but the fossil record is not informative as to whether that evolutionary step occurred in northeastern or southern Africa. The molecular evidence suggests the latter (Newman et al., 2004).

  • PARAPAPIO ADO (Hopwood, 1936)

Diagnosis Leakey and Delson (1987). A small species of Parapapio distinguished from Papio and larger species of Parapapio by its more sloping mandibular symphysis, with a projecting alveolar margin, straight-sided molars, an absence of cuspules in the median lingual clefts of the upper molars, and slight buccal flexures between the M3 lophids that slightly kink the tooth.

Description Most of the specimens referred to this species are fragmentary jaws, the most complete being the mandible of a young adult female, LAET 1209 (Leakey and Delson, 1987). A mandible from Kanapoi, originally identified as possibly P. jonesi (Patterson, 1968), was tentatively reassigned to this species (Leakey and Delson, 1987; Frost, 2001b), and collections of recent mandibles and dentition have confirmed this (Harris et al., 2003). A collection of isolated molars and fragmentary jaws including the male partial maxilla KNM-ER 37118 and partial mandible KNM-ER 37060 from East Turkana has been identified tentatively as Parapapio cf. ado (Jablonski et al., 2008b).

Age Early Pliocene, 4.1–3.49 Ma.

African Occurrence Laetoli (Tanzania); Kanapoi, and Lokochot and Lonyumun members of the Koobi Fora Formation, East Turkana (Kenya).

Remarks The poor preservation of many of the remains referred to this species, and—especially—the absence of diagnostic facial material, precludes the clear morphological definition of the taxon. As discussed in connection with Cercopithecus, the lack of relevant fossils is probably due to taphonomic bias adversely affecting the preservation of small-bodied monkeys.

Diagnosis Heaton (2006). A species of Parapapio of moderate size distinguished from Parapapio jonesi by more strongly developed maxillary ridges and maxillary fossae, from Parapapio whitei by smaller size, and shorter rostrum, and from Papio izodi by less marked development of the same features; shares with Parapapio jonesi but not with P.izodi anterolaterally “fleeting” zygomatic arches.

Description The species is known from a large number of partial crania (Figure 23.11) from Sterkfontein including the female STS 255 and the STS 253, as well as a slightly larger morph from Bolt’s Farm, BF 43.

Age Plio-Pleistocene.

African Occurrence Members 2 and 4, Sterkfontein; Members 2–4 at Makapansgat; and Bolt’s Farm (South Africa).

Remarks Heaton’s research has suggested that P.whitei (discussed later) is a junior synonym of P.broomi, with the expanded concept of the species being more sexually dimorphic. If his analysis is correct, this would result in significant expansion of the sample size the specimens assigned to P. broomi (Heaton, 2006).

Diagnosis Following Heaton (2006), a small Parapapio morph distinguished from Parapapio broomi and Papio izodi by a straight nasal profile and the least marked development of maxillary ridges and fossae (Frost, 2001b; Frost and Delson, 2002).

Description Best known from South Africa, where it is represented by cranial and abundant gnathic remains including female cranium STS 565 and male cranium SWP 2947, and craniodental remains from Hadar and the Middle Awash (Frost, 2001b; Frost and Delson, 2002).

Age Middle Pliocene.

African Occurrence Makapansgat and Members 2 and 4, Sterkfontein (South Africa); tentatively from Kada Hadar Member, Hadar Formation (Ethiopia), and below the Sidi Hakoma Tuff in the Middle Awash (Ethiopia).

Cercopithecoidea

Figure 23.11 Parapapio broomi. Lateral view of male cranium MP 2 (M 202). Photograph courtesy of Leonard Freedman.

Remarks The identification of P. jonesi from the Hadar Formation (ca. 3.0 Ma) and from Middle Awash sediments (3.5 Ma) is based on a nearly complete male skull, female face, and several mandibular fragments (Figure 23.12; Frost and Delson, 2002). Morphologically, this material is similar to that from (p.415) Makapansgat and Sterkfontein Member 4, but it differs in the prominent and rounded nasal bones and robust and thickened brow ridge of the male cranium. If the remains assigned to P. jonesi from northeastern and southern Africa are conspecific or closely related, it would establish the species as the earliest papionin with a nearly Pan-African distribution. If, as is argued later, Parapapio is originally a northeastern or eastern African genus, then P. jonesi or a closely related morph may represent the base of the genus’ radiation in South Africa (Heaton, 2006).

Cercopithecoidea

Figure 23.12 Parapapio jonesi. Comparison of specimens allocated or tentatively allocated to P. jonesi from different parts of Africa. A) Lateral and occlusal views of female mandible STS 390A from Sterkfontein; photograph courtesy of Leonard Freedman. B) Lateral and occlusal views of male mandible KNM-KP 286 from Kanapoi. © National Museums of Kenya. C) Vertical and lateral views of male cranium A.L.363-1a from Hadar.

  • PARAPAPIO LOTHAGAMENSIS Leakey et al., 2003

Diagnosis Leakey et al. (2003). Distinguished from all other Parapapio species by its small size; long, narrow, and proclined mandibular symphysis; broad P3; and deciduous P4 lacking a transverse crest. Shares with Victoriapithecus but not most other cercopithecoids considerable molar flare, distally constricted m3, and other characteristics.

Description Known from mostly fragmentary gnathic and postcranial remains and isolated teeth, the most complete specimen of the species is the holotype mandible, KNM-LT 23091.

Age Late Miocene, 7.4–ca. 5 Ma.

African Occurrence Lower and Upper members, Nawata Formation, Lothagam (Kenya).

Remarks This species is the oldest, smallest, and most primitive of the recognized papionins. Its presence at Lothagam, and the existence of other Mio-Pliocene morphologically similar forms of Parapapio at nearby sites in the Omo–Lake Turkana Basin, suggests that the region was a center of diversification for Parapapio.

  • PARAPAPIO WHITEI Broom, 1940

Diagnosis Larger than other species of Parapapio. Rostrum is relatively longer than that of P.broomi.

Description The species is known from a series of crania from Makapansgat and more fragmentary remains from Sterkfontein.

Age Plio-Pleistocene.

African Occurrence Members 2 and 4, Sterkfontein, and Members 2–4 Makapansgat (South Africa).

Remarks Freedman (1957) recognized three species of Parapapio at Sterkfontein and Makapansgat, largely on the basis of dental size. In response to the poorly defined boundaries among these species, Heaton undertook an important reevaluation of Parapapio (Heaton, 2006). He synonymized P.broomi and P.whitei, and if this is correct, it would result in the definition of a more sexually dimorphic P.broomi.

  • PARAPAPIO sp. indet.

Diagnosis Includes small-, medium-, and large-sized examples of the genus that are too fragmentary or that are represented by too few specimens to diagnose to species.

Description This sample includes partial and fragmentary jaws, and a large number of isolated papionin postcrania that lack the apomorphies of Papio or Theropithecus.

(p.416) Age Plio-Pleistocene.

African Occurrence Apak and Kaiyumung members, Nachukui Formation, Lothagam (Kenya); Lonyumun, Lokochot, Upper Burgi, and KBS members, Koobi Fora Formation, East Turkana (Kenya)(Leakey et al., 2003; Jablonski et al., 2008b).

Remarks This collection almost certainly includes one or more new species, but the parlous nature of the material has precluded the erection of formal taxa to date. Prior to 3 Ma, Parapapio was the dominant papionin in the Turkana Basin. After that time, the genus slips into the background of the Turkana Basin monkey fauna, seemingly having been eclipsed by species of Theropithecus, while continuing to thrive in southern Africa. Parapapio does not disappear altogether from East Africa, however, because it continues to be represented by a series of morphologically intriguing, but poorly known morphs that are distinct from their Theropithecus contemporaries or from modern Papio baboons (Frost, 2001b).

  • Genus PLIOPAPIO Frost 2001
  • PLIOPAPIO ALEMUI Frost, 2001

Diagnosis Frost (2001a). A medium-sized papionin similar in cranial and dental size to larger species of Macaca but smaller than Mandrillus, most subspecies of modern Papio, Gorgopithecus, Paradolichopithecus, Dinopithecus, or extinct species of Theropithecus. Distinguished from Papio by a rounded muzzle dorsum and weak or absent maxillary ridges and facial fossae, and from Parapapio by a clear anteorbital drop and ophryonic groove.

Description Pliopapio alemui is best known from the male holotype cranium, ARA-VP-6/933, and a large sample of mandibles, maxillae, and dentition from Aramis and contemporary sites (Frost, 2001b); also present at Gona (Semaw et al., 2005), and known from a female maxilla and mandible, along with more fragmentary remains from the 5.2-Ma Kuseralee Member of the Sagantole Formation, and several isolated teeth from the Adu Asa Formation may extend its range back to 5.7 Ma (Frost et al., 2009).

Age Latest Miocene–early Pliocene, 5.2–4.2 Ma.

African Occurrence Aramis and Kuseralee members of the Sagantole Formation, Middle Awash; and Gona (Ethiopia).

Remarks Pliopapio is a medium-sized papionin from the Afar region of Ethiopia. Its phylogenetic position is not known, but Frost (2001b) hypothesized that it may represent a stem member of the Papio, Lophocebus, Theropithecus clade, although a position closer to Parapapio or a stem African papionin cannot be ruled out. The obliquely oriented (proclined) morphology of the mandibular symphysis that Pliopapio shares with early species of Parapapio such as P. ado and P. lothagamensis suggests either a close phyletic relationship or similar patterns of ingestion and mastication, or both.

  • Genus PROCERCOCEBUS Gilbert, 2007
  • PROCERCOCEBUS ANTIQUUS (Haughton, 1925)

Diagnosis Gilbert (2007b). A small- to medium-sized papionin distinguished from other papionins by an extremely straight nasal profile, widely divergent anterior temporal lines, and upturned nuchal crest, and other features; and from Cercocebus primarily in its more widely divergent temporal lines and smaller premolars.

Description Recognized only from Taung, the best specimens of the species are the lectotype, SAM 5384, a partial male cranium, a nearly complete adult male cranium, UW-AS TP9, and a partial adult female cranium, UW-AS TP8 (Gilbert, 2007b).

Age Plio-Pleistocene.

African Occurrence Taung (South Africa).

Remarks As mentioned in connection with Lophocebus earlier, the recognition of Procercocebus in South Africa lends weight to the hypothesis that the two lineages of extant mangabeys evolved from geographically distant forebears in eastern and southern Africa.

  • Genus THEROPITHECUS I. Geoffroy Saint-Hilaire, 1843

Diagnosis Delson (1993); Jablonski (2002); Jablonski et al. (2008b). Large, heavily built, and highly sexually dimorphic papionins distinguished from other papionins by highcrowned and columnar-cusped cheek teeth with deep foveae and pronounced infoldings of thick enamel, mandibular teeth arranged in an anteroposteriorly convex curve (Curve of Spee) in most species, anterior union of temporal lines and long sagittal crest, a high opposability index produced by its elongated pollex and abbreviated index finger, and many other features.

Description Following Delson, Theropithecus is recognized here as consisting of two subgenera, T.(Omopithecus) and T.(Theropithecus), which represent the two major lineages within the genus as they are now understood (Delson, 1993). An early, if not the earliest Theropithecus, is recognized from early Pliocene sequences of the Koobi Fora Formation in the Omo–Lake Turkana Basin (described later under Theropithecus sp. indet.) and appears to represent an early member of the T.(Omopithecus) lineage. Both subgenera may appear at similar times in the fossil record, however, with T.(Omopithecus) in early Pliocene sequences of the Koobi Fora Formation, and T.(Theropithecus) potentially from Wee-ee in the Middle Awash. The T.(Omopithecus) lineage was associated with well-watered environments, including riparian forests, in the Omo–Lake Turkana and Baringo basins during the Pliocene. The T.(Theropithecus) lineage, by contrast, dominated more open, grassland-dominated environments throughout the Pleistocene, and it is known from localities in northern, northeastern, eastern, and southern Africa. The sole living representative of the genus, T.(T.) gelada, is found only in the grass-covered highlands of central Ethiopia.

Age Pliocene–Recent.

African Occurrence Pan-African, except for equatorial rain forests.

Remarks Fossils of Theropithecus occur more widely and in larger numbers than those of any other primate genus in Africa, and the genus appears to have been one of the most successful primates of all time. This was due to a remarkable combination of anatomical features of the hand, dentition, and masticatory apparatus that permitted theropiths to harvest, ingest, and chew large quantities of vegetation, especially grass. These specializations allowed open-country-dwelling forms of the genus, especially T.(T.)oswaldi, to successfully compete in savanna and savanna-woodland environments against hooved mammals until the middle Pleistocene, when a combination of factors, notably increasing environmental seasonality and an inability to engage in seasonal migrations, led to the extirpation of the genus from all but the most remote and competition-free grassland environments. The genus is represented today by only one relict species in the Ethiopian highlands, T.gelada. The subgeneric (p.417) definitions advanced by Delson for division of extinct Theropithecus species (Delson, 1993) are followed here, as in a previous review (Jablonski, 2002). The first comprehensive description of fossil Theropithecus by Jolly (1972) is a classic work in vertebrate paleontology, to which modern studies of fossil primate functional anatomy and ecomorphology owe their inspiration.

  • Subgenus THEROPITHECUS I. Geoffroy Saint-Hilaire, 1843

Diagnosis Distinguished from Theropithecus (Omopithecus) by tendencies toward reduction of muzzle length, weak development of maxillary ridges and corresponding rounding of the muzzle cross section, reduction of incisors, and molarization of premolars.

Description After the tentatively identified material from Wee-ee, Middle Awash, already mentioned, the earliest members of the subgenus, represented by T. (T.) darti, are known from abundant remains at Hadar and the Middle Awash (including Maka and contemporary sites) in Ethiopia, and Makapansgat in South Africa. Theropithecus (T.) oswaldi is recognized from almost all Plio-Pleistocene fossil sites in Africa, with the largest samples deriving from sites in the Omo–Lake Turkana Basin and Kanjera and Olorgesailie in Kenya and Swartkrans in South Africa.

Age Plio-Pleistocene.

African Occurrence North, northeastern, eastern, and southern Africa (including Algeria, Ethiopia, Kenya, Tanzania, and South Africa).

Remarks The fossils of T.(Theropithecus) form a geographically and temporally extensive array of medium- to large-bodied papionins. Some students have lumped constituent taxa into a single species, T.oswaldi, with three slightly morphologically differentiated chrono-subspecies: T. oswaldi darti, T. oswaldi oswaldi, and T.oswaldileakeyi (Leakey, 1993). Theropithecus (Theropithecus) darti is here retained as a separate species, following Eck and Jablonski (1987), but questions remain over the validity of this species and its certain identification from widely geographic distant sites in northeastern, eastern, and southern Africa. One of us (S.F.) considers the darti morph to be the earliest subspecies of T.(T).oswaldi.

  • THEROPITHECUS (THEROPITHECUS) DARTI
  • Broom and Jensen, 1946
  • Figure 23.13

Diagnosis Distinguished from T.(T.)oswaldi, by its smaller overall size, narrow and ovoid piriform aperture, a large infratemporal fossa contained by a broadly bowed and smoothly curved zygomatic arch, and a deeply excavated triangular depression on the mandibular ramus.

Description The largest sample of this species is from Hadar, which has produced a partial skull of a male (AL205-1a–1c; Figure 23.13) as well as many partial crania of juveniles and subadults (Eck, 1993). The species was first recognized from Makapansgat in South Africa, where a male mandible with broken cheek teeth, MP 1 (M201), represents the holotype (Freedman, 1957; Maier, 1972). Makapansgat has also produced a complete female juvenile skull with occluded cranium and mandible, M3073, and the adult female cranium MP 222. Fragmentary specimens of T. (T.). darti are also known from lower Omo Group and Middle Awash deposits (Eck, 1987, 1993; Frost, 2001b), and from East Turkana, where the species is represented by a fragmented male cranium, KNM-ER 3025 (Leakey, 1993).

Cercopithecoidea

Figure 23.13 Theropithecus (Theropithecus) darti. Lateral and basal views of male cranium AL 205-1. Photographs courtesy of Gerald Eck.

Age Pliocene, 3.5–2.4 Ma.

African Occurrence Upper Lokochot Member, Koobi Fora Formation, East Turkana (Kenya); lower members of the Shungura Formation, Omo Group (Ethiopia), Hadar, Formation “W” below the Sidi Hakoma Tuff, Middle Awash (Ethiopia); and Makapansgat (South Africa).

Remarks Theropithecus (T.) darti was geographically widespread, but was only reasonably common in northeastern Africa. Although the taxonomic equivalence of the different geographic representatives of the species is still debated, the occurrence of T.(T.) darti in South Africa appears to be the result of a dispersal event near the end of the species’ history. Like T.(T.)oswaldi, T.(T.) darti appeared to enjoy limited success in southern Africa probably because of competition from species and descendants of Parapapio. As this species grades into T.(T.)oswaldi, it is often regarded as an early chrono-subspecies T. (T.) oswaldi darti (Leakey, 1993; Frost, 2001a; Frost and Delson, 2002; Frost and Alemseged, 2007).

(p.418)

  • THEROPITHECUS (THEROPITHECUS) OSWALDI
  • Andrews, 1916
  • Figure 23.14

Diagnosis Same as for genus and subgenus. Distinguished from other papionins, especially T. darti, by its larger size, robust postglenoid processes and greater relative reduction of incisors and canines. This long-lived species exhibited considerable variation through time.

Description Most students recognize at least two subspecies, an earlier and smaller T. (T.) oswaldi oswaldi and a later and larger T.(T.)oswaldileakeyi. Both morphs are represented by abundant remains, including partial skeletons, which are enumerated elsewhere (Eck, 1987; Delson et al., 1993; Frost, 2001b; Frost and Delson, 2002; Frost and Alemseged, 2007). Occurrences of the former subspecies include partial crania from the Middle Awash, material from the upper part of the Hadar Formation, Konso, and large numbers of specimens from upper members of the Shungura Formation from Ethiopia (Jablonskietal.,2008b); fromplentiful cranial and postcranial remains from the upper Burgi and KBS members of the Koobi Fora Formation (Delson et al., 1993), West Turkana and Kanjera in Kenya; and from Olduvai Gorge in Tanzania (Freedman, 1970; Delson et al., 1993; Heaton, 2006; Frost and Alemseged, 2007; Gilbert, 2007a; Frost et al., 2009; Figure 23.14). Theropithecus (T.) oswaldi leakeyi is known from the Daka Member of the Bouri Formation, the Dawaitoli Formation, Andalee in the Middle Awash, Asbole in the Afar, the southern Ethiopian site of Konso, and Member L of the Shungura Formation. It is also recognized from the Okote Member of the Koobi Fora Formation, West Turkana, and Olorgesailie in Kenya, from Olduvai Gorge and Peninj in Tanzania, and from several South African cave sites (Delson and Hoffstetter, 1993). It is also known from the northern African sites of Ain Jourdel and Ternifine, Algeria, and Thomas Quarries, Morocco (Delson et al., 2000). The largest and probably last representative of the species appears to have occurred at Kapthurin in the Baringo Basin.

Age Plio-Pleistocene, 2.5–0.25 Ma.

African Occurrence Ain Jourdel and Ternifine (Algeria); Thomas Quarries (Morocco); Upper Kada Hadar Member, Hadar Formation (Ethiopia); Matabaietu Formation, and Hata and Daka members, Bouri Formation, Dawaitoli Formation, Middle Awash (Ethiopia); Asbole, Afar Region (Ethiopia); Melka Kontoure (Ethiopia); Konso (Ethiopia); Members D–L, Shungura Formation (Ethiopia); upper Burgi, KBS, and Okote members, Koobi Fora Formation, East Turkana (Kenya); Nachukui Formation, West Turkana (Kenya); Olorgesailie (Kenya); Kapthurin (Kenya); Beds I–IV and Masek Beds, Olduvai Gorge and Peninj (Tanzania); Kaiso (Uganda); and Swartkrans, Sterkfontein (Member 5), Gladysvale, Hopefield, Coopers, and Bolt’s Farm (South Africa).

Cercopithecoidea

Figure 23.14 Theropithecus (Theropithecus) oswaldi. A) Lateral and basal views of male cranium KNM-ER 18925; B) lateral and occlusal views of associated mandible KNM-ER 18925; C) occlusal view of partial left mandible KNM-ER 880. Note the crown height and complex infoldings of enamel that characterize the late examples of this species.

Remarks Theropithecus oswaldi was a chronospecies, and the subspecies recognized by some workers represent specimen allocations based on size, enamel folding complexity, anterior dental reduction, or occurring on either side of depositional (p.419) hiatuses. Through the long tenure of the species, the animals became considerably larger, with estimates for male body mass ranging from 42 kg in early representatives of the species to 〉85 kg by the time the species went extinct (Delson et al., 2000). Pari passu, the postcanine dentition underwent increases in occlusal surface area and in the length and complexity of molar enamel ridges, while the anterior dentition underwent significant reduction (Jolly, 1972; Jablonski et al., 2008b). Theropithecus oswaldi was one of the most highly specialized primates that ever lived. The species was large bodied, highly sexually dimorphic, mostly—if not exclusively—terrestrial, and capable of chewing prodigious amounts of manually harvested vegetation (mostly grass) with its powerful jaws and ungulate-like teeth (Benefit and McCrossin, 1990; Jablonski, 1993). Theropithecus oswaldi was the only primate other than Homo known to have dispersed out of Africa in the Plio-Pleistocene; fragmentary but convincing fossil remains are known from Spain and India (Delson et al., 1993).

  • Subgenus OMOPITHECUS Delson, 1993

Diagnosis Jablonski (1994). Distinguished from Theropithecus (Theropithecus) by an elongated muzzle with a flat dorsum and well-developed maxillary ridges, a large and anteriorly expanded zygoma, a robust zygomatic arch that is triangular in cross section, a robust mandibular symphysis bearing sinusoidal mental ridges, and features of the postcranial skeleton that reflect adaptations for elbow stability and shoulder flexibility.

Description This subgenus contains three recognized species, T.(O.) baringensis, T.(O.) brumpti, and T. (O.) quadratirostris, from the Omo–Lake Turkana Basin of Kenya. Remains referred to T.(O.) baringensis have also been described from Angola (Jablonski, 2002). All species are represented by complete crania (Jablonski et al., 2002), and T.(O.) brumpti from extensive fossils including a partial skeleton (Jablonski et al., 2008b)

Age Pliocene, 3.94–2.0 Ma.

African Occurrence Chemeron (Kenya); Tugen Hills (Kenya); Lonyumun, Lokochot and Tulu Bor members, Koobi Fora Formation, East Turkana (Kenya); Nachukui Formation, West Turkana (Kenya), Members B–G, Shungura Formation, Omo Group (Ethiopia); Usno Formation, Omo Group (Ethiopia).

Remarks Theropithecus (Omopithecus) contains the earliest recognized fossils of Theropithecus, as represented by isolated molar teeth (Benefit and McCrossin, 1990). Theropithecus (O.) quadratirostris and T.(O.) baringensis exhibit broad, boxy muzzles that lack well-defined maxillary ridges and zygomatic arches that show anterior thickening, not flare. Their molar teeth are low crowned and lack the pinched, columnar cusps typical of most T.(O.).brumpti. The dietary preferences of the species in the T.(Omopithecus) lineage are not well-known but do not appear to be closely comparable to those of living primates (Jablonski, 1986; Jablonski et al., 2002).

Postcranial fossils are only known from T.(O.)brumpti, and these indicate that the species was mainly terrestrial but that it had a high opposability index and was capable of undertaking the same kind of dexterous manipulation of food and other items that the gelada does today (Jablonski et al., 2002). Theropithecus (Omopithecus) brumpti may have been quite similar to the living mandrill in appearance and behavior (Jablonski, 1994).

  • THEROPITHECUS (OMOPITHECUS) BARINGENSIS
  • (Leakey, 1969)
  • Figure 23.15

Diagnosis Same as for the subgenus. Theropithecus (Omopithecus) baringensis shows the most conservative facial morphology of the subgenus, with a broad muzzle lacking well-defined maxillary ridges and zygomatic arches showing anterior thickening but no anterior flare. The molars are somewhat lower crowned and exhibit less pinching of the cusps than in T.(O.)brumpti.

Description The species is best known from the holotype, a complete skull, KNM-BC 2, from Chemeron (Figure 23.15). It is also known from a mandibular specimen, KNM-BC 1647, from the same site, and a series of cranial remains from the Angolan site of Leba including a complete juvenile cranium, TCH 38 ‘90, and a partial cranium of a male, TCH 25 ‘90 (Delson and Dean, 1993). Other remains referable to this species are discussed and illustrated as Papio quadratirostris by Delson and Dean (1993).

Age Pliocene, 3–2 Ma (for Chemeron)(Gundling and Hill, 2000).

African Occurrence Chemeron (Kenya); Leba (Angola).

Remarks Originally classified as Papio baringensis (Leakey, 1969), the classification and phyletic position of this species continues to be debated in the literature (Eck and Jablonski, 1984, 1987; Delson and Dean, 1993; Leakey, 1993; Jablonski et al., 2002). The holotype and paratype are best accommodated within Theropithecus (Omopithecus) because of the relatively small size and weakly developed columnar cusp morphology of the molars that presage the conditions seen in T. (O.) brumpti.

  • THEROPITHECUS (OMOPITHECUS) BRUMPTI
  • (Arambourg, 1947)
  • Figure 23.16

Diagnosis Same as for the subgenus, with accentuation of facial features, specifically those of the maxillae and zygomatic arch. Theropithecus (O.) brumpti is distinguished from other species of the subgenus by very high-crowned, straight-sided, and columnar-cusped molars; more deeply excavated fossae of the mandibular corpus; more pronounced maxillary ridges; and anterolaterally flaring zygomatic arches present in both sexes.

Description Good examples of this species (Figure 23.16) have been retrieved from deposits of the Omo and Turkana basins and include a partial skeleton, KNM-WT 39368, two nearly complete crania of adult males (L345-287 and KNM-WT 16828), partial crania of females (L32-155 and L122-34), and nearly complete mandibles of males (L576-8, KNM-ER 2015) (Eck and Jablonski, 1987).

Age Pliocene, 3.4–2.0 Ma.

African Occurrence Lokochot and Tulu Bor members, Koobi Fora Formation, East Turkana (Kenya); Nachukui Formation, West Turkana (Kenya); Members B–G, Shungura Formation, Omo Group (Ethiopia).

Remarks This species would have been one of the most extraordinary-looking monkeys that ever lived. Its large and anterolaterally flaring zygomatic arches are unique among mammals and supported the attachment of a greatly enlarged superficial masseter muscle, which permitted a wide gape for canine displays (Jablonski, 1986; Jablonski et al., 2002). The shape of the maxillary ridges and the shape and orientation (p.420) of the zygomatic flare vary considerably between individuals of the same sex. Remains of the hand skeletons of two individuals exhibit the elongated pollex and abbreviated index digit that contributed to excellent opposability, as seen in extant Theropithecus gelada (Iwamoto, 1982). The discovery of this manual architecture in T.(O.)brumpti indicates that the configuration probably was primitive for the genus and that it may have played an important role facilitating food harvesting and manipulation.

Cercopithecoidea

Figure 23.15 Theropithecus (Omopithecus) baringensis. Views of male skull, KNM-BC 2 (holotype). A) Lateral, vertical, and basal views of cranium; B) lateral and occlusal views of mandible (lateral is a mirror image). © National Museums of Kenya.

  • THEROPITHECUS (OMOPITHECUS) QUADRATIROSTRIS (Iwamoto, 1982)

Diagnosis Same as for the subgenus, except that diagnostic features of the cranium appear intermediate in state between those of T.(O.)baringensis and T.(O.)brumpti. The broad, long muzzle bears rounded maxillary ridges, the robust zygomatic arches are triangular in cross section at the zygomaticomaxillary suture and thickened anteriorly, and the broad frontal process of the zygoma lends depth to the malar region, as in other Theropithecus. The species is distinguished from T.(O.) baringensis by its elongated neurocranium, more posteriorly oriented temporalis musculature, and posterior union of the temporal lines and formation of sagittal crest posterior to the bregma in males.

Description The species is known only from the holotype, a nearly complete cranium of a male (unnumbered; Delson and Dean, 1993)

Age Pliocene, 3.3 Ma.

African Occurrence Usno Formation, Omo Group (Ethiopia).

Remarks This species is only recognized with certainty from the type specimen; specimens allocated by Delson and Dean (Iwamoto, 1982) to Papio quadratirostris from Angola are assigned to T.(O.)baringensis (Jablonski, 1994). The material from the Shungura Formation is discussed under Papio. As in the case of T.(O.)baringensis, this species was originally assigned to Papio (Eck and Jablonski, 1984) and was subsequently referred to Theropithecus (Delson and Dean, 1993). This referral has been questioned (including by S.F.) (Eck and Jablonski, 1984) but is retained here because of the synapomorphies that unite it with both T.(O.)baringensis and T.(O.)brumpti, as discussed elsewhere (Jablonski et al., 2008b).

  • THEROPITHECUS (OMOPITHECUS) sp. indet.

Diagnosis Molars with moderately pinched, columnar cusps covered with thick enamel; distinguished from Theropithecus (Theropithecus) by molars with lower crowns, lower cusp relief, and less pronounced enamel infoldings.

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Cercopithecoidea

Figure 23.16 Theropithecus (Omopithecus) brumpti. A) Lateral and vertical views of male cranium KNM-WT 16828. Note strongly anteriorly expanded and flaring zygomatic arches. © National Museums of Kenya. B) Dorsal view of the hand skeleton of T.(O.)brumpti(L865-2) showing the derived condition of elongated metacarpals and abbreviated proximal phalanges that contribute to a high opposability index.

Description Specimens assigned to this morph include mostly isolated teeth and a few highly weathered jaw and postcranial fragments that have been described from Allia Bay at Koobi Fora and that were recently assigned to Theropithecus sp. indet. or cf. Theropithecus (Kalb et al., 1982b).

Age Pliocene, 3.94 Ma.

African Occurrence Lokochot and Lonyumun members, Koobi Fora Formation, East Turkana (Kenya).

Remarks These remains constitute one of the oldest, if not the oldest, occurrences of the genus. At Allia Bay, Theropithecus appears to have been the rarest of the monkeys, with its remains greatly outnumbered by those of Parapapio and Cercopithecoides.

  • THEROPITHECUS subgen. et sp. indet.

Diagnosis This small group comprises fragmentary specimens probably belonging to Theropithecus, but lacking sufficient apomorphies to permit more specific diagnosis.

Description A small female mandible from the Afar has been tentatively assigned to Theropithecus (Frost, 2001a). A male mandible from the Middle Awash may also belong to Theropithecus but is is more equivocal (Frost, 2001a; Benefit and McCrossin, 2002; Benefit, 2009).

Age Pliocene, 3.9 Ma.

African Occurrence Wee-ee in the Middle Awash, Afar Region (Ethiopia).

Remarks These occurrences of Theropithecus, if confirmed, would be the earliest known and would point to an origin of the genus in northeastern Africa. An isolated molar from Kanapoi dated to 4.1 has also been tentatively included in Theropithecus (Frost, 2001a; Harris et al., 2003).

General Discussion

The African fossil record of the Cercopithecoidea defines the history of the superfamily from its origins in the middle Miocene through the latest Pleistocene. From the late Miocene onward, monkeys were a major element of the African mammalian fauna, but the composition of the monkey fauna was not stable through time. Changes in the taxonomic and morphological composition of the monkey fauna occurred as a consequence of climatic and environmental change, and because of competition with other mammals. This discussion will touch on only a small number of the most important topics brought to light by the fossil record of the African Cercopithecoidea. These are, first, the nature and meaning of the fossil record of the Victoriapithecidae and of the earliest representatives of the modern subfamilies Colobinae and Cercopithecinae. The second topic to be explored is that of the Pliocene radiations of Cercopithecoides and Parapapio. This will pave the way for discussions of the evolution of the large, terrestrial colobines and Theropithecus, and for examinations of the origin of the modern cercopithecoid fauna of Africa that highlight our state of knowledge concerning, especially, the evolution of the mangabeys and Papio baboons.

The earliest clearly defined Old World monkeys belong to the family Victoriapithecidae, with the northeastern African species Prohylobates tandyi generally considered the most pr imitive known cercopithecoid species. The circum-Mediterranean (p.422) region has long been considered a geographic focus for early cercopithecoid evolution (Delson, 1973, 1974, 1975). The presence of the middle Miocene P. tandyi in Egypt and of the earliest representatives of the Colobinae and Cercopithecinae in late Miocene and earliest Pliocene deposits of Greece, Algeria, Libya, and Kenya considerably strengthens this surmise. Primate paleontologists have generally discounted the possibility that the ancestors of any African late Miocene or PlioPleistocene cercopithecids dispersed from Eurasia, but this possibility cannot be excluded at least for colobines because of the strong craniodental morphological similarities between Eurasian Mesopithecus and the African Mio-Pliocene genera Libypithecus, Paracolobus, and Rhinocolobus (Jablonski, 1998; Stewart and Disotell, 1998).

The nature of the phyletic relationships of victoriapithecids to later cercopithecids is still a topic of much debate (Benefit and McCrossin, 2002), because the constituent species do not display patterns of synapomorphies that permit their convincing assignment to one or another of the modern cercopithecid subfamilies. The conditions leading to the emergence of the Colobinae and Cercopithecinae thus remain unclear but were no doubt related to the evolution of divergent dietary preferences. The earliest colobines presumably exhibited specializations for gut fermentation and allelochemical detoxification consistent with a diet consisting mostly of seeds and leaves (Lucas and Teaford, 1994). Many such foods, especially leaves, are not patchily distributed and are not usually contested. On the other hand, the earliest cercopithecines would have possessed cheek pouches, which afforded the animals the ability to temporarily store highquality and highly contestable food items that might require incisal or manual preparation before ingestion (Lambert, 2005; Smith et al., 2008).

The Cercopithecoides of the latest Miocene and earliest Pliocene in Africa included two large and idiosyncratic genera endemic to Ethiopia, Kuseracolobus and Pliopapio, as well as early representatives of the colobine genera Paracolobus and Cercopithecoides and the papionin genus Parapapio. These fossils have been recorded mostly from closed environments, and the animals have been interpreted as being exclusively arboreal or at least not exclusively terrestrial in their modes of locomotion (Hlusko, 2006, 2007). These findings denote that arboreality was the rule, not the exception, for late Miocene and early Pliocene monkeys, and that the evolution of predominantly terrestrial forms occurred only later in the history of both cercopithecid subfamilies in Africa.

Major changes in African environments and mammalian faunas occurred by the middle Pliocene. Marine and terrestrial paleoclimatic records indicate that a shift from warmer and wetter conditions to more seasonally contrasted, cooler, drier, and more variable conditions occurred after about 3 Ma (deMenocal, 2004; Feakins and deMenocal, this volume, chap. 4). From this time onward, the predominant trend was toward increased seasonality of rainfall, intensification of seasonal pulses of ecosystem productivity, and increasing climatic variability, with steplike increases in savanna vegetation apparent at 1.8 Ma, 1.2 Ma, and 0.6 Ma (deMenocal, 2004). These changes impacted the hydrological regimes of most of the continent and the vegetation on which mammalian herbivores, including the monkeys, depended (Bobe et al., 2002; Bobe and Behrensmeyer, 2004; deMenocal, 2004). From the middle Pliocene onward, the African cercopithecoid fauna underwent marked changes in numbers and kinds of species, distributions of body sizes, and dietary and locomotor specializations (Elton, 2007). Monkeys are particularly sensitive indicators of ecosystem productivity because they require foods of relatively high nutritional yield with respect to amino acid, fatty acid, and sugar content. Monkeys are not as narrowly restricted as apes in their dietary preferences (Jablonski et al., 2000), but they require higher-quality foods than other mammals of similar body size because of their relatively large and metabolically costly brains. They are also limited in their physical ability to range widely for preferred foods because their prehensile hands and feet are no match for wear-resistant hooves when it comes to covering long distances. Thus, monkeys—like other primates, but unlike many ungulates—cannot and do not undertake long-distance migrations in order to track seasonally available food and water resources. For these and other reasons, monkeys were vanguard indicators of environmental change in the African Plio-Pleistocene. They were sensitive to environmental perturbations and were among the first to suffer during periods of climatic deterioration. There is no evidence, however, that they underwent significant pulses of speciation and extinction in coordination with specific climatic swings (Frost, 2007a).

By the middle Pliocene the geographic center for cercopithecid lineage diversification had shifted from northern and northeastern Africa to eastern Africa. Against the backdrop of prevailing environmental change, species of the colobine Cercopithecoides and the papionin Parapapio appear to have been the most successful, at least in those habitats preserved in the fossil record.

The fossil record of the Omo–Lake Turkana Basin is particularly instructive in shedding light on cercopithecid evolution from the middle Pliocene through middle Pleistocene (Jablonski and Leakey, 2008a). With the onset of increasingly seasonal rainfall regimes in the middle Pliocene, the fauna of this region became dominated by one terrestrial cercopithecine apparently restricted to riparian forest floors (Theropithecus [O.]brumpti) and to large-bodied colobines capable of exploiting ecotonal woodland savanna habitats. The latter included one mostly arboreal species, Rhinocolobus turkanaensis, and two highly terrestrially adapted forms, Cercopithecoides williamsi and C. kimeui (Jablonski et al., 2008a). The success that large-bodied colobines enjoyed from the middle Pliocene through early Pleistocene relative to cercopithecines probably had much to do with their capacity for fermentative, ruminant digestion, which would have permitted them to subsist on vegetation of lower quality and with lower requirements for fresh drinking water (Van Soest, 1982). Their command of these niches was short-lived, however, as competition from more highly mobile and better dentally equipped ruminant artidactyls intensified. By the Plio-Pleistocene boundary, environments were considerably more heterogeneous than in the Pliocene, and pronounced differences in habitat quality and ecosystem productivity existed between areas adjoining permanent sources of water and those not. Under these conditions, monkeys probably suffered from increasing competition with ruminant artiodactyls and suids, which were becoming ever-more taxonomically and ecologically diverse (Gagnon and Chew, 2000; Cerling et al., 2003).

The earliest cercopithecoids in South Africa are from the middle Pliocene. At that time, the monkey fauna included Cercopithecoides williamsi, several species of Parapapio and Theropithecus (T.) darti. By the later Pliocene, Papio izodi was present in southern Africa. Although the details of latest (p.423) Tertiary and early Quaternary climatic and environmental change are less well-known for southern than for eastern Africa, available records indicate progressive cooling since 3.2 Ma and increasing dominance of arid-adapted vegetation (deMenocal, 2004). For reasons that are still not clear, Parapapio and its putative regional descendants were more diverse in southern Africa than were theropiths and colobines. Parapapio underwent considerable regional diversification and gave rise to the first species of Papio and Procercocebus, the probable ancestor to the Cercocebus lineage of mangabeys. At the same time, colobines and theropiths in South Africa continued to be represented by one ecological generalist species each: Cercopithecoides williamsi and Theropithecus (T.) darti (and later T.[T.]oswaldi), respectively. During the late Pliocene and early Pleistocene, Papio and the Cercocebus mangabeys appear to have remained confined to southern Africa. Judging from its Pleistocene distribution in southern Africa, Papio evolved in markedly seasonal environments where it developed the ecological opportunism that was eventually to propel it to greater success and continental hegemony by the late middle and late Pleistocene.

In the late Pliocene environments of eastern Africa, Theropithecus (O.) brumpti disappeared from its riparian forest-floor niche, probably supplanted by suines (such as Kolpochoerus spp.) and dry-adapted tragelaphine bovids, which colonized their habitats and more successfully exploited subcanopy food resources (Flagstad et al., 2001; Cerling et al., 2003). Theropithecus (T.) oswaldi became the dominant cercopithecine by the Plio-Pleistocene boundary, not by ecologically displacing T.(O.)brumpi but by establishing a successful niche as a terrestrial, primarily graminivorous habitué of ecotonal and open habitats (Bobe et al., 2002). In this environment, T.(T.)oswaldi joined the large colobine, Cercopithecoides kimeui, while Rhinocolobus turkanaensis maintained a more arboreal niche. By the early middle Pleistocene, woodland environments became rarer, the trend toward increasing seasonality of precipitation had intensified, habitats had become highly heterogeneous, and monkeys had become less common and less taxonomically diverse. Theropithecus (T.) oswaldi appears to have been the most successful of the monkeys in competing with ungulates and suids for grazing niches in mostly open habitats, largely because of its large, high-crowned, and occlusally complex molars. Most of the other monkey species recognized at that time were species closely comparable to modern forms and include close relatives of the gray-cheeked mangabey, Lophocebus albigena, colobus monkeys (Colobus spp.) and various guenons (Cercopithecus and Chlorocebus spp.). These species occupied uniquely primate niches, which were unassailable by hoofed competitors (Jablonski and Leakey, 2008a).

In eastern Africa, the middle and late Pleistocene were characterized by inexorably increasing seasonality of rainfall and exaggerated habitat heterogeneity. This period saw the extinction of the last of the large Plio-Pleistocene monkeys, epitomized by the demise of the colobine Cercopithecoides kimeui and the giant papionin Theropithecus (T.) oswaldi. Representatives of Papio in eastern Africa begin to be detected by the later middle Pleistocene. There are few sites in which Theropithecus (T.) oswaldi and Papio appear to have coexisted, at least until the very end of the middle Pleistocene, and it is unlikely that it was ecological competition with Papio that drove T (T.)oswaldi to extinction. The largely graminivorous theropith became extinct because it could not survive as a highly encephalized and relatively immobile ecological specialist. Papio did not take over this niche but succeeded in a completely different one, that of the intensive, highly opportunistic, and omnivorous forager.

Through time, the centers of diversification of the Cercopithecoidea in Africa shifted from the north and northeast in the middle and late Miocene to east Africa in the middle Pliocene to southern Africa in the terminal Pliocene and Pleistocene. Mostly endemic monkey faunas evolved in the these regions, but generalist forms did succeed in dispersing, first from northeast to eastern Africa in the latest Miocene, then from eastern to southern African in the later Pliocene. The enormous latitudinal expanse of Africa meant that the monkeys evolving in different regions faced markedly different climatic and environmental challenges. It is telling that, by the end of the Pleistocene, the dominant cercopithecids of open African environments—baboons of the genus Papio—underwent their early evolution under the highly seasonal conditions at the southernmost extremity of the continent. With few exceptions, the remaining elements of the modern African monkey fauna are committed arborealists who established and maintained highly folivorous or frugivorous niches in woodlands and forests, far from the hoofbeats and claws of the savanna.

Summary

All evidence at hand indicates that Old World monkeys originated in Africa in the early Miocene. The earliest cercopithecoids were recovered from sites in Egypt, Libya, and Kenya and have been assigned to species of Victoriapithecidae, a family lacking the anatomical specializations of later Cercopithecidae. Although one site, Maboko Island, preserves large numbers of Victoriapithecus fossils, victoriapithecids appear to have been genuinely rare elements of the African mammalian fauna. Until around 10 mya, hominoids were the dominant catarrhines throughout the Old World. The lack of diversity of early cercopithecoids can readily be appreciated in Figure 23.17, which depicts the temporal ranges of the genera of Africa fossil Cercopithecoidea.

In the interpretation of the history of Old World monkeys in Africa, it is difficult to differentiate taphonomic effects from biogeographic trends. The fossil record indicates that the prevailing direction of dispersal of cercopithecoids in Africa was from north (or northeast) to south and began in the middle Miocene. By the late Miocene, species representing the two modern cercopithecid subfamilies, Colobinae and Cercopithecinae, were present in the fossil records of Ethiopia and Kenya; by the early Pliocene, colobine and cercopithecine fossils were plentiful in the Omo–Lake Tur kana Basin. The plentiful and well-preserved monkey fossils from the basin have been tacitly considered to represent the archetypal fossil monkeys of Africa and putative ancestors for later monkey lineages. Evidence provided by detailed studies of the northeastern and southern African monkey faunas suggests, however, that the Omo–Lake Turkana Basin was geographically isolated during intervals of the Pliocene and Pleistocene and that some of its most famous fossil monkeys (e.g., Rhinocolobus turkanaensis and Theropithecus brumpti) were strictly endemic. With respect to overall biogeographic trends, the most important south to north dispersal of monkeys was that of Papio in the middle Pleistocene.

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Cercopithecoidea

Figure 23.17 The temporal ranges of African fossil monkey genera. Shading at ends of range bars indicates uncertainty about dates of first and last appearances.

Morphological and molecular evidence indicates that the earliest true colobines possessed foregut fermentation (Stewart et al., 1987; Stewart, 1999), a key innovation that allowed members of the subfamily to evolve a variety of herbivore niches in forests, ecotonal woodland-grasslands, and open savannas through the Pliocene and Pleistocene. The Pliocene colobines were large bodied (〉10 kg), and many were terrestrial or semiterrestrial. Species of the genus Cercopithecoides were particularly numerous and widespread. They competed favorably with ungulates in woodland-grassland and ecotonal woodland ecosystems through the Plio-Pleistocene, and they only became extinct in these habitats when increased environmental seasonality throughout Africa led to deterioration of food quality and critical shortfalls of food at important milestones in animal life histories. The modern colobine fauna of Africa consists of exclusively arboreal species, and probably includes descendants of some semiterrestrial or terrestrial Plio-Pleistocene forms.

(p.425) Three genera, Parapapio, Theropithecus, and Cercopithecus (sensu lato) dominated cercopithecine evolution in Africa through the Pliocene and Pleistcene. The radiation of Parapapio species is still not well understood because few complete fossils are known, but most species appear to have been macaque-like in size, morphology, and habitus. Regional species or populations of Parapapio were probably the ancestors of Theropithecus and Lophocebus in eastern Africa, and of Papio and Cercocebus in southern Africa; in due course, the taxonomy of the genus may have to be revised to accommodate these cladogenetic events. The evolution of Theropithecus is well documented, with the species T.oswaldi being its most important representative. This widespread and highly adaptable grass eater was the only primate other than early Homo that dispersed out of Africa in the Plio-Pleistocene, and continues to be a well-deserved subject of study. Its extinction occurred later than that of the large-bodied colobines but was probably precipitated by a similar course of events. The evolution of the guenons (Cercopithecus and close relatives) is the least well documented in the African fossil record probably because of taphonomic factors that mostly prevented the preservation of forest-dwellers of smaller body size (5–10 kg). Nonetheless, the group’s radiation rivaled that of papionins with regard to the total number of species produced and the total area of the continent they occupied.

The most visible and widespread of the nonhuman primates of Africa today, the baboons of the genus Papio, are relative newcomers whose unquestioned fossil record began only in the middle Pleistocene. These baboons have achieved success because their eclectic, opportunistic foraging strategies made it possible for them to create intensivist niches that were different from those of most of the open-country-dwelling primates who preceded them. In this way, Papio baboons were similar to another remarkable primate lineage, that of Homo sapiens.

Acknowledgments

We thank Bill Sanders and Lars Werdelin for inviting us to contribute to this volume and for being extremely patient while we prepared this chapter. Discussions with Brenda Benefit, Eric Delson, Todd Disotell, Leslea Hlusko, Cliff Jolly, Meave Leakey, Ellen Miller, and Tony Tosi, especially in the context of the Cercopithecoid Analytical Working Group of the Revealing Hominid Origins Initiative, were useful in helping us organize our thoughts and keeping us current on new fossil discoveries. Eric Delson’s comments on the original version of this chapter greatly improved the text. We are extremely grateful to Brenda Benefit, Gerald Eck, Leonard Freedman, and Leslea Hlusko for providing us with photos of various fossil monkey species. Bonnie Warren of the Department of Anthropology of the California Academy of Sciences and Tess Wilson of the Department of Anthropology of The Pennsylvania State University prepared the figures for publication. Tess Wilson is thanked for maintaining the bibliographic database and for preparing the final draft for submission.

Literature Cited

Bibliography references:

Alemseged, Z. and D. Geraads. 1998. Theropithecus atlanticus (Thomas, 1884)(Primates: Cercopithecidae) from the late Pliocene of Ahl al Oughlam, Casablanca, Morocco. Journal of Human Evolution 34:609–621.

———. 2000. A new Middle Pleistocene fauna from the BusidimaTelalak region of the Afar, Ethiopia. Comptes Rendus de l’Académie des Sciences, Série IIA, 331:549–556.

Barnicot, N. A. and D. Hewtt-Emmett. 1972. Red cell and serum proteins of Cercocebus, Presbytis, Colobus, and certain other species. Folia Primatologica 17:442–457.

Barry, J. C. 1987. The history and chronology of Siwalik cercopithecids. Human Evolution 2:47–58.

Benefit, B. R. 1993. The permanent dentition and phylogenetic position of Victoriapithecus from Maboko Island, Kenya. Journal of Human Evolution 25:83–172.

———. 1999. Victoriapithecus: The key to Old World monkey and catarrhine origins. Evolutionary Anthropology 7:155–174.

———. 2000. Old World monkey origins and diversification: An evolutionary study of diet and dentition; pp. 133–179 in P. F. Whitehead and C. J. Jolly (eds.), Old World Monkeys. Cambridge University Press, Cambridge.

———. 2009. The biostratigraphy and paleontology of fossil cercopithecoids from eastern Libya; pp. 247–266 in M. J. Salem et al. (eds.) Geology of East Libya, Vol. 3. Tripoli, Libya. Geology of East Libya.

Benefit, B. R. and M. L. McCrossin. 1990. Diet, species diversity and distribution of African fossil baboons. Kroeber Anthropological Society Papers 71–72:77–93.

———. 1997. Earliest known Old World monkey skull. Nature 388:368–371.

———. 2002. The Victoriapithecidae, Cercopithecoidea; pp. 241–253 in W. C. Hartwig (ed.), The Primate Fossil Record. Cambridge University Press, Cambridge.

Benefit, B. R. and M. Pickford. 1986. Miocene fossil cercopithecoids from Kenya. American Journal of Physical Anthropology 69:441–464.

Birchette, M. G. 1982. The postcranial skeleton of Paracolobus chemeroni. Unpublished PhD dissertation, Harvard University, Cambridge, 494 pp.

Bobe, R. and A. K. Behrensmeyer. 2004. The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeography, Palaeoclimatology, Palaeoecology 207:399–420.

Bobe, R., A. K. Behrensmeyer and R. E. Chapman. 2002. Faunal change, environmental variability and late Pliocene hominin evolution. Journal of Human Evolution 42:475–497.

Broom, R. 1937. On some new Pleistocene mammals from limestone caves of the Transvaal. South African Journal of Science 33:750–768.

———. 1940. The South African Pleistocene cercopithecid apes. Annals of the Transvaal Museum 20:89–100.

Broom, R. and J. T. Robinson. 1949. A new type of fossil baboon, Gorgopithecus major. Proceedings of the Zoological Society of London 119:379–387.

Brunet, M., F. Guy, D. Pilbeam, H. T. Mackaye, A. Likius, D. Ahounta, A. Beauvilain, C. Blondel, H. Bocherens, J.-R. Boisserie, L. De Bonis, Y. Coppens, J. Dejax, C. Denys, P. Duringer, V. Eisenmann, G. Fanone, P. Fronty, D. Geraads, T. Lehmann, F. Lihoreau, A. Louchart, A. Mahamat, G. Merceron, G. Mouchelin, O. Potero, P. P. Campomanes, M. Ponce de Leon, J.-C. Rage, M. Sapanet, M. Schuster, J. Sudre, P. Tassy, X. Valentin, P. Vignaud, L. Viriot, A. Zazzo and C. Zollikofer. 2002. A new hominid from Upper Miocene of Chad, Central Africa. Nature 418:145–151.

Cerling, T. E., J. M. Harris and B. H. Passey. 2003. Dietary preferences of East African Bovidae based on stable isotope analysis. Journal of Mammalogy 84:456–471.

Cronin, J. E. and V. M. Sarich. 1976. Molecular evidence for dual origin of mangabeys among Old World monkeys. Nature 260:700–702.

(p.426) Dechow, P. P. C. and R. R. Singer. 1984. Additional fossil Theropithecus from Hopefield, South Africa: A comparison with other African sites and a reevaluation of its taxonomic status. American Journal of Physical Anthropology 63:405–35.

de Heinzelin, J., J. D. Clark, T. White, W. Hart, P. Renne, G. WoldeGabriel, Y. Beyene and E. Vrba. 1999. Environment and behavior of 2.5-million-year-old Bouri hominids. Science 284:625–635.

Delson, E. 1973. Fossil colobine monkeys of the Circum-Mediterranean region and the evolutionary history of the Cercopithecidae (Primates, Mammalia). Unpublished PhD dissertation, Columbia University, 856 pp.

———. 1974. Preliminary review of cercopithecid distribution in the circum-Mediterranean region. Mémoires du Bureau des Recherches Géologiques et Minières (France) 78:131–135.

———. 1975. Evolutionary history of the Cercopithecidae. Contributions to Primatology. 5:167–217

Delson, E. 1979. Prohylobates (Primates) from the Early Miocene of Libya: A new species and its implications for cercopithecid origins. Geobios 12:725–733.

Delson, E. 1980. Fossil macaques, phyletic relationships and a scenario of deployment; pp. 10–30 in D. G. Lindburg (ed.), The Macaques: Studies in Ecology, Behavior and Evolution. Van Nostrand Reinhold, New York.

———. 1984. Cercopithecid biochronology of the African PlioPleistocene: Correlation among eastern and southern hominidbearing localities. Courier Forschungs-Institut Senckenberg 69: 199–218.

———. 1988. Chronology of South African australopith site units; pp. 317–324 in F. E. Grine (ed.), Evolutionary History of the “Robust” Australopithecines. Aldine de Gruyter, New York.

———. 1993. Theropithecus fossils from Africa and India and the taxonomy of the genus; pp. 157–189 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Delson, E. and D. Dean. 1993. Are Papio baringensis R. Leakey, 1969, and P. quadratirostris Iwamoto, 1982, species of Papio or Theropithecus? pp. 125–156 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Delson, E., G. G. Eck, M. G. Leakey and N. G. Jablonski. 1993. A partial catalogue of fossil remains of Theropithecus; pp. 499–525 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Delson, E. and R. Hoffstetter. 1993. Theropithecus from Ternifine, Algeria; pp. 191–208 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Delson, E., C. J. Terranova, W. L. Jungers, E. J. Sargis, N. G. Jablonski and P. C. Dechow. 2000. Body mass in Cercopithecidae (Primates, Mammalia): Estimation and scaling in extinct and extant taxa. Anthropological Papers of the American Museum of Natural History 83:1–159.

deMenocal, P. B. 2004. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters 220:3–24.

Disotell, T. R. and R. L. Raaum. 2002. Molecular timescale and gene tree incongruence in the Guenons; pp. 27–36 in M. E. Glenn and M. Cords (eds.), The Guenons: Diversity and Adaptation in African Monkeys. Kluwer Academic Publishers, New York.

Dutrillaux, B., M. Muleris and J. Couturier. 1988. Chromosomal evolution of Cercopithecinae; pp. 150–159 in A. Gautier-Hion, F. Bourlière, J. P. Gautier, and J. Kingdon (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge University Press, New York.

Eck, G. G. 1976. Cercopithecoidea from Omo Group deposits; pp. 332–344 in Y. Coppens, F.C. Howell, G.L.Isaac, and R.E.F. Lea key (eds.), Earliest Man and Environments in the Lake Rudolf Basin. University of Chicago Press, Chicago.

———. 1987. Theropithecus oswaldi from the Shungura Formation, Lower Omo Basin, southwestern Ethiopia; pp. 123–140 in Les Faunes Plio-Pleistocenes de la Vallée de l’Omo (Ethiopie): Cercopithecidae de la Formation de Shungura. Centre National de la Recherche Scientifique, Paris.

———. 1993. Theropithecus darti from the Hadar Formation, Ethiopia; pp. 15–83 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Eck, G. and F. C. Howell. 1972. New fossil Cercopithecus material from the Lower Omo Basin, Ethiopia. Folia Primatologica 18:325–355.

Eck, G. G. and N. G. Jablonski. 1984. A reassessment of the taxonomic status and phyletic relationships of Papio baringensis and Papio quadratirostris (Primates: Cercopithecidae). American Journal of Physical Anthropology 65:109–134.

———. 1987. The skull of Theropithecus brumpti as compared with those of other species of the genus Theropithecus; pp. 11–122 in Les Faunes Plio-Pleistocenes de la Vallée de l’Omo (Ethiopie): Cercopithecidae de la Formation de Shungura. Centre National de la Recherche Scientifique, Paris.

Eisenhart, B. 1974. The Fossil Cercopithecoids of Makapansgat and Sterkfontein. Unpublished senior honors thesis, Harvard University, Cambridge.

Elton, S. 2007. Environmental correlates of the cercopithecoid radiations. Folia Primatologica 78:344–364.

Flagstad, Ø., P. O. Syvertsen, N. C. Stenseth and K. S. Jakobsen. 2000. Environmental change and rates of evolution: The phylogeographic pattern within the hartebeest complex as related to climatic variation. Proceedings of the Royal Society of London, B 268:667–677.

Fooden, J. 1980. Classification and distribution of living macaques (Macaca Lacepede, 1799); pp. 1–9 in D. Lindburg, G. (ed.), The Macaques: Studies in Ecology, Behavior and Evolution. Van Nostrand Reinhold, Los Angeles.

Freedman, L. 1957. The fossil Cercopithecoidea of South Africa. Annals of the Transvaal Museum 23:8–262.

———. 1965. Fossil and subfossil primates from the limestone deposits at Taung, Bolt’s Farm and Witkrans, South Africa. Palaeontologia Africana 9:19–48.

———. 1970. A new check-list of fossil Cercopithecoidea of South Africa. Palaeontologia Africana 13:109–110.

———. 1976. South African fossil Cercopithecoidea: A re-assessment including a description of new material from Makapansgat, Sterkfontein and Taung. Journal of Human Evolution 5:297–315.

Frost, S. R. 2001a. Fossil Cercopithecidae of the Afar Depression, Ethiopia: Species systematics and comparison to the Turkana Basin. Unpublished PhD dissertation, City University of New York, New York, 463 pp.

———. 2001b. New Early Pliocene Cercopithecidae (Mammalia: Primates) from Aramis, Middle Awash Valley, Ethiopia. American Museum Novitates 3350:1–36.

———. 2007a. Fossil Cercopithecidae from the Middle Pleistocene Dawaitoli Formation, Middle Awash Valley, Afar Region, Ethiopia. American Journal of Physical Anthropology 134:460–467.

———. 2007b. African Pliocene and Pleistocene cercopithecid evolution and global climatic change; pp. 51–76 in R. Bobe, Z. Alemseged, and A. K. Behrensmeyer (eds.), Hominid Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, New York.

Frost, S. R. and Z. Alemseged. 2007. Middle Pleistocene fossil Cercopithecidae from Asbole, Afar Region, Ethiopia. Journal of Human Evolution 53:227–259.

Frost, S. R. and E. Delson. 2002. Fossil Cercopithecidae from the Hadar Formation and surrounding areas of the Afar Depression, Ethiopia. Journal of Human Evolution 43:687–748.

Frost, S. R., Y. Haile-Selassie and L. G. Hlusko. 2009. Cercopithecidae; pp. 135–158 in Y. Haile-Selassie (ed.), Ardipithecus kadabba. Late Miocene evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley.

Frost, S. R., L. F. Marcus, F. L. Bookstein, D. P. Reddy and E. Delson. 2003a. Cranial allometry, phylogeography, and systematics of large-bodied papionins (Primates: Cercopithecinae) inferred from geometric morphometric analysis of landmark data. The Anatomical Record Part A 276A:1048–1072.

Frost, S. R., T. Plummer, L. C. Bishop, P. Ditchfield, J. Ferraro and J. Hicks. 2003b. Partial cranium of Cercopithecoides kimeui Leakey, 1982 from Rawi Gully, southwestern Kenya. American Journal of Physical Anthropology 122:191–199.

Gagnon, M. and A. E. Chew. 2000. Dietary preferences in extant African Bovidae. Journal of Mammalogy 81:490–511.

Gautier, J. P. 1988. Interspecific affinities among guenons as deduced from vocalizations; pp. 194–226 in A. Gautier-Hion, F. Bourlière, J. P. Gautier, and J. Kingdon (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge University Press, New York.

Gebo, D. L. and E. J. Sargis. 1994. Terrestrial adaptations in the postcranial skeletons of guenons. American Journal of Physical Anthropology 93:341–371.

Geraads, D. 1987. Dating the Northern African cercopithecid fossil record. Human Evolution 2:19–27.

(p.427) Gilbert, C. C. 2007a. Craniomandibular morphology supporting the diphyletic origin of mangabeys and a new genus of the Cercocebus/Mandrillus clade, Procercocebus. Journal of Human Evolution 53:69–102.

———. 2007b. Identification and description of the first Theropithecus (Primates: Cercopithecoidae) material from Bolt’s Farm, South Africa. Annals of the Transvaal Museum 44:1–10.

Gilbert, W. H. and S. R. Frost. 2008. Cercopithecidae; pp. 115–132 in W. H. Gilbert and B. Asfaw (eds.), Homo erectus: Pleistocene Evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley.

Groves, C. P. 1989. A Theory of Human and Primate Evolution. Clarendon Press, Oxford, 384 pp.

———. 2001. Primate Taxonomy. Smithsonian Institution Press, Washington, D.C., 350 pp.

Gundling, T. and A. Hill. 2000. Geological context of fossil Cercopithecoidea from eastern Africa; pp. 180–213 in P. F. Whitehead and C. J. Jolly (eds.), Old World Monkeys. Cambridge University Press, Cambridge.

Harris, J. M., F. H. Brown and M. G. Leakey. 1988. Stratigraphy and paleontology of Pliocene and Pleistocene localities west of Lake Turkana, Kenya. Contributions in Science 399:1–128.

Harris, J. M., M. G. Leakey and T. E. Cerling. 2003. Early Pliocene tetrapod remains from Kanapoi, Lake Turkana Basin, Kenya. Contributions in Science, Natural History Museum of Los Angeles County, Los Angeles 498:39–114.

Harrison, T. 1989. New postcranial remains of Victoriapithecus from the middle Miocene of Kenya. Journal of Human Evolution 18:3–54.

Harrison, T. and E. E. Harris. 1996. Plio-Pleistocene cercopithecids from Kanam, western Kenya. Journal of Human Evolution 30:539–561.

Heaton, J. L. 2006. Taxonomy of the Sterkfontein fossil Cercopithecinae: The Papionini of members 2 and 4 (Gauteng, South Africa). Unpublished PhD dissertation, Indiana University, 503 pp.

Hlusko, L. J. 2006. A new large Pliocene colobine species (Mammalia: Primates) from Asa Issie, Ethiopia. Geobios 39:57–69.

———. 2007. A new late Miocene species of Paracolobus and other Cercopithecoidea (Mammalia: Primates) fossils from Lemudong’o, Kenya. Kirtlandia 56:72–85.

Hylander, W. L. 1975. Incisor size and diet in anthropoids with special reference to Cercopithecidae. Science 189:1095–1098.

Iwamoto, M. 1982. A fossil baboon skull from the lower Omo basin, southwest Ethiopia. Primates 23:533–541.

Jablonski, N. G. 1986. The hand of Theropithecus brumpti; pp. 173–182 in Selected Proceedings of the Tenth Congress of the International Primatological Society: Volume 1. Primate Evolution. Cambridge, Cambridge University Press.

———. 1993. The evolution of the masticatory apparatus in Theropithecus; pp. 299–329 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

———. 1994. New fossil cercopithecid remains from the Humpata Plateau, southern Angola. American Journal of Physical Anthropology 94:435–64.

———. 1998. Primate evolution—in and out of Africa: Comments from Nina G. Jablonski. Current Biology 9:119–122.

———. 2002. Fossil Old World monkeys: The late Neogene radiation; pp. 255–299 in W. C. Hartwig (ed.), The Primate Fossil Record. Cambridge University Press, Cambridge.

Jablonski, N. G. and M. G. Leakey. 2008a. The importance of the Cercopithecoidea from the Koobi Fora Formation in the context of primate and mammalian evolution; pp. 397–416 in N. G. Jablonski and M. G. Leakey (eds.), Koobi Fora Research Project: Volume 6. The Fossil Monkeys. California Academy of Sciences, San Francisco.

———. 2008b. Systematic paleontology of the small colobines; pp. 12–30 in N. G. Jablonski and M. G. Leakey (eds.), Koobi Fora Research Project: Volume 6. The Fossil Monkeys. California Academy of Sciences, San Francisco.

Jablonski, N. G., M. G. Leakey and M. Antón. 2008a. Systematic paleontology of the cercopithecines; pp. 103–300 in N. G. Jablonski and M. G. Leakey (eds.), Koobi Fora Research Project: Volume 6. The Fossil Monkeys. California Academy of Sciences, San Francisco.

Jablonski, N. G., M. G. Leakey, C. Kiarie and M. Antón. 2002. A new skeleton of Theropithecus brumpti (Primates: Cercopithecidae) from Lomekwi, West Turkana, Kenya. Journal of Human Evolution 43:887–923.

Jablonski, N. G., M. G. Leakey, C. V. Ward and M. Antón. 2008b. Systematic paleontology of the large colobines; pp. 31–102 in N. G. Jablonski and M. G. Leakey (eds.), Koobi Fora Research Project: Volume 6. The Fossil Monkeys. California Academy of Sciences, San Francisco.

Jablonski, N. G., M. J. Whitfort, N. Roberts-Smith and Q. Xu. 2000. The influence of life history and diet on the distribution of catarrhine primates during the Pleistocene in eastern Asia. Journal of Human Evolution 39:131–157.

Jolly, C. J. 1970. The seed-eaters: A new model of hominid differentiation based on a baboon analogy. Man 5:5–26.

———. 1972. The classification and natural history of Theropithecus (Simopithecus)(Andrews, 1916), baboons of the African Plio-Pleistocene. Bulletin of the British Museum (Natural History), Geology 22:1–123.

Jones, T. R. 1937. A new fossil primate from Sterkfontein, Krugersdorp, Transvaal. South African Journal of Science 33:709–728.

Kalb, J. E., M. Jaegar, C. J. Jolly and B. Kana. 1982a. Preliminary geology, paleontology and paleoecology of a Sangoan site at Andalee, Middle Awash Valley, Ethiopia. Journal of Archaeological Science 9:349–363.

Kalb, J. E., C. J. Jolly, S. Tebedge, A. Mebrate, C. Smart, E. B. Oswald, P. F. Whitehead, C. B. Wood, T. Adefris and V. Rawn-Schatzinger. 1982b. Vertebrate faunas from the Awash Group, Middle Awash Valley, Afar, Ethiopia. Journal of Vertebrate Paleontology 2:237–258.

Lambert, J. E. 2005. Competition, predation, and the evolutionary significance of the cercopithecine cheek pouch: The case of Cercopithecus and Lophocebus. American Journal of Physical Anthropology 126:183–192.

Leakey, M. G. 1982. Extinct large colobines from the Plio-Pleistocene of Africa. American Journal of Physical Anthropology 58:153–172.

———. 1985. Early Miocene cercopithecids from Buluk, northern Kenya. Folia Primatologica 44:1–14.

———. 1988. Fossil evidence for the evolution of the guenons; pp. 7–12 in A. Gautier-Hion, F. Bourlière, J.-P. Gautier, and J. Kingdon (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge University Press, Cambridge.

———. 1993. Evolution of Theropithecus in the Turkana Basin; pp. 85–123 in N. G. Jablonski (ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge.

Leakey, M. G. and E. Delson. 1987. Fossil Cercopithecidae from the Laetolil Beds; pp. 91–107 in M. D. Leakey and J. M. Harris (eds.), Laetoli: A Pliocene Site in Northern Tanzania. Clarendon Press, Oxford.

Leakey, M. G. and R. E. F. Leakey. 1976. Further Cercopithecinae (Mammalia, Primates) from the Plio/Pleistocene of East Africa. Fossil Vertebrates of Africa 4:121–146.

Leakey, M. G., M. F. Teaford and C. V. Ward. 2003. Cercopithecidae from Lothagam; pp. 201–248 in M. G. Leakey and J. M. Harris (eds.), Lothagam: The Dawn of Humanity in Eastern Africa. Columbia University Press, New York.

Leakey, R. E. F. 1969. New Cercopithecidae from the Chemeron Beds of Lake Baringo, Kenya. Fossil Vertebrates of Africa 1:53–69.

Lucas, P. W. and M. F. Teaford. 1994. Functional morphology of colobine teeth; pp. 173–203 in A. G. Davies and J. F. Oates (eds.), Colobine Monkeys: Their Ecology, Behaviour and Evolution. Cambridge University Press, Cambridge.

Maier, W. 1971. Two new skulls of Parapapio antiquus from Taung and a suggested phylogenetic arrangement of the genus Parapapio. Annals of the South African Museum 59:1–16.

———. 1972. The first complete skull of Simopithecus darti from Makapansgat, South Africa, and its systematic position. Journal of Human Evolution 1:395–405.

McBrearty, S. and N. G. Jablonski. 2005. First fossil chimpanzee. Nature 437:105–108.

McKee, J. K. 1993. Taxonomic and evolutionary affinities of Papio izodi fossils from Taung and Sterkfontein. Palaeontologia Africana 30:43–49.

Meikle, W. E. 1987. Fossil Cercopithecidae from the Sahabi Formation; pp. 119–127 in N. T. Boaz, A. El-Arnauti, A. W. Gaziry, J. de Heinzelin, and D. D. Boaz (eds.), Neogene Paleontology and Geology of Sahabi. Liss, New York.

Miller, E. R., B. R. Benefit, M. L. McCrossin, J. M. Plavcan, M. G. Leakey, A. N. El-Barkooky, M. A. Hamdan, M. K. Abdel Gawad, S. M. Hassan and E. L. Simons. 2009. Systematics of early and middle Miocene Old World monkeys. Journal of Human Evolution 57:195–211.

(p.428) Morales, J. C. and D. J. Melnick. 1998. Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. Journal of Human Evolution 34:1–23.

Napier, P. H. 1981. Catalogue of Primates in the British Museum (Natural History) and Elsewhere in the British Isles: Part II. Family Cercopithecidae, Subfamily Cercopithecinae. British Museum (Natural History), London, 203 pp.

———. 1985. Catalogue of Primates in the British Museum (Natural History) and Elsewhere in the British Isles: Part III. Family Cercopithecidae, Subfamily Colobinae. British Museum (Natural History), London, 111 pp.

Newman, T. K., C. J. Jolly and J. Rogers. 2004. Mitochondrial phylogeny and systematics of baboons (Papio). American Journal of Physical Anthropology 124:17–27.

Page, S. L. and M. Goodman. 2001. Catarrhine phylogeny: Noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Molecular Phylogenetics and Evolution 18:14–25.

Patterson, B. 1968. The extinct baboon, Parapapio jonesi, in the early Pleistocene of northwestern Kenya. Breviora 282:1–4.

Raaum, R. L., K. N. Sterner, C. M. Noviello, C.-B. Stewart and T. R. Disotell. 2005. Catarrhine primate divergence dates estimated from complete mitochondrial genomes: Concordance with fossil and nuclear DNA evidence. Journal of Human Evolution 48:237–257.

Rae, T. C., O. Rohrer-Ertl, C.-P. Wallner and T. Koppe. 2007. Paranasal pneumatization of two late Miocene colobines: Mesopithecus and Libypithecus (Cercopithecidae: Primates). Journal of Vertebrate Paleontology 27:768–771.

Remane, A. 1925. Der Fossile Pavian (Papio Sp.) von Oldoway nebst Bemerkungen über die Gattung Simopithecus C. W. Andrews; pp. 83–90 in H. Reck (ed.), Wissenschaftliche Ergebnisse der OldowayExpedition 1913, vol. 2.

Semaw, S., S. W. Simpson, J. Quade, P. R. Renne, R. F. Butler, W. C. McIntosh, N. Levin, M. Dominguez-Rodrigo and M. J. Rogers. 2005. Early Pliocene hominids from Gona, Ethiopia. Nature 433:301–305.

Senut, B. 1994. Cercopithecoidea Neogénes et Quaternaires du Rift Occidental (Ouganda); pp. 195–205 in M. Pickford and B. Senut (eds.), Geology and Palaeobiology of the Albertine Rift Valley, UgandaZaire: Vol. II. Palaeobiology. CIFEG, Orléans.

Simons, E. L. 1967. A Fossil Colobus Skull from the Sudan (Primates, Cercopithecidae). Postilla 111:1–12.

Simons, E. L. and E. Delson. 1978. Cercopithecidae and Parapithecidae; pp. 100–119 in V. J. Maglio and H. B. S. Cooke (eds.), Evolution of African Mammals. Harvard University Press, Cambridge.

Smith, L. W., A. Link and M. Cords. 2008. Cheek pouch use, predation risk, and feeding competition in blue monkeys (Cercopithecus mitis stuhlmanni). American Journal of Physical Anthropology 137:334–341.

Sterner, K. N., R. L. Raaum, Y.-P. Zhang, C. -B. Stewart and T. R. Disotell. 2006. Mitochondrial data support an odd-nosed colobine clade. Molecular Phylogenetics and Evolution 40:1–7.

Stewart, C.-B. 1999. The colobine Old World monkeys as a model system for the study of adaptive evolution at the molecular level; pp. 29–38 in P. Dolhinow and A. Fuentes (eds.), The Nonhuman Primates. Mayfield, London.

Stewart, C.-B. and T. R. Disotell. 1998. Primate evolution—in and out of Africa. Current Biology 8:R583–R588.

Stewart, C.-B., J. W. Schilling and A. C. Wilson. 1987. Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404.

Strasser, E. and E. Delson. 1987. Cladistic analysis of cercopithecid relationships. Journal of Human Evolution 16:81–99.

Stromer, E. 1914. Mitteilungen über Wirbeltierreste aus dem Mittelpliocän des Natrontales (Ägypten). Zeitschrift der Deutschen Geologischen Gesellschaft 65:350–372.

———. 1920. Mitteilungen über Wirbeltierreste aus dem Mittelpliocän des Natrontales (Ägypten) 5. Nachtrag zur Affen. Sitzungsberichte der Bayerischen Akademie der Wissenschaften 1920:345–370.

Swindler, D. R. and F. J. Orlosky. 1974. Metric and morphological variability in the dentition of colobine monkeys. Journal of Human Evolution 3:135–160.

Szalay, F. S. and E. Delson. 1979. Evolutionary History of the Primates. Academic Press, New York, 580 pp.

Tosi, A. J., P. J. Buzzard, J. C. Morales and D. J. Melnick. 2002a. Y-chromosomal window onto the history of terrestrial adaptation in the Cercopithecini; pp. 13–24 in M. E. Glenn and M. Cords (eds.), The Guenons: Diversity and Adaptation in African Monkeys. Kluwer Academic Publishers, New York.

Tosi, A. J., K. M. Detwiler and T. R. Disotell. 2005. X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini). Molecular Phylogenetics and Evolution 36:58–66.

Tosi, A. J., T. R. Disotell, J. C. Morales and D. J. Melnick. 2003a. Y-chromosome data provide a test of competing morphological evolutionary hypotheses. Molecular Phylogenetics and Evolution 27:510–521.

Tosi, A. J., D. J. Melnick and T. R. Disotell. 2004. Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). Journal of Human Evolution 46:223–237.

Tosi, A. J., J. C. Morales and D. J. Melnick. 2000. Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution 17:133–144.

———. 2002b. Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. International Journal of Primatology 23:161–178.

———. 2003b. Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution 57:1419–1435.

Van Soest, P. J. 1982. Nutritional Ecology of the Ruminant. Your Town Press, Salem, Mass., 476 pp.

Wildman, D. E., T. J. Bergman, A. al-Aghbari, K. N. Sterner, T. K. Newman, J. E. Phillips-Conroy, C. J. Jolly and T. R. Disotell. 2004. Mitochondrial evidence for the origin of hamadryas baboons. Molecular Phylogenetics and Evolution 32:287–296.

Xing, J., H. Wang, K. Han, D. A. Ray, C. H. Huang, L. G. Chemnick, C. B. Stewart, T. R. Disotell, O. A. Ryder and M. A. Batzer. 2005. A mobile element based phylogeny of Old World monkeys. Molecular Phylogenetics and Evolution 37:872–80.

Xing, J., H. Wang, Y. Zhang, D. A. Ray, A. J. Tosi, T. R. Disotell and M. A. Batzer. 2007. A mobile element-based evolutionary history of guenons (Tribe Cercopithecini). BMC Biology 5:5.

Zhang, J., Y.-p. Zhang and H. F. Rosenberg. 2002. Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nature Genetics 30:411–415.