Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007–2015)

Journal of Human Evolution xxx (xxxx) xxx

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Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015) Stephen R. Frost a, *, Carol V. Ward b, Fredrick K. Manthi c, J. Michael Plavcan d a

Department of Anthropology, 1218 University of Oregon, Eugene, OR 97403-1218, USA Department of Pathology and Anatomical Sciences, M263 Medical Sciences Building, University of Missouri, Columbia, MO 65212, USA c Department of Earth Sciences, National Museums of Kenya, P.O. Box 40658, Nairobi, Kenya d Department of Anthropology, 330 Old Main, University of Arkansas, Fayetteville, AR 72701, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 October 2017 Accepted 12 July 2019 Available online xxx

Recent fieldwork at Kanapoi has expanded the sample of fossil cercopithecids, facilitating a reappraisal of their taxonomy. The assemblage now includes at least one species of cercopithecin, two papionins, and two colobines. The guenon Nanopithecus browni is similar in dental size to extant Miopithecus. We tentatively re-affirm the identification of Parapapio cf. ado and confirm the presence of Theropithecus. The colobines include a small form tentatively attributed to Kuseracolobus and a second larger species. The Kanapoi fossils represent the oldest occurrences of guenons in Africa and of the important genus Theropithecus, the most abundant and widespread primate in the Neogene of Africa. In the assemblage, Parapapio cf. ado is the most abundant form, comprising the majority of specimens. All of the other taxa are comparatively rare. Colobines make up a small part of the Kanapoi fossil assemblage compared to most other contemporary sites, including Allia Bay, Kenya, where, like Kanapoi, Australopithecus anamensis has been found. The presence of Theropithecus is consistent with the presence of some relatively open habitat at Kanapoi. While the ecological preferences of the small cercopithecin are unknown, most guenons are associated with relatively wooded habitats, as are most colobines, suggesting the availability of at least some wooded areas. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Pliocene Theropithecus Cercopithecini Parapapio Kuseracolobus

1. Introduction The locality of Kanapoi, Kenya, yields some of the oldest known Australopithecus fossils to date, and thus constitutes an important locality for understanding the paleoenvironmental and faunal context of early hominin evolution (Leakey et al., 1995, 1998; Ward et al., 2001, 2013, in press; 2013, in press). Fossil non-hominin primates are an important element of most eastern African Neogene faunas, with the record of papionin fossils being particularly rich (Jablonski and Frost, 2010). The most recent review of the Kanapoi fauna noted that aside from one galago specimen, cercopithecids comprise the majority of the non-hominin primate sample, and identified Parapapio ado, cf. Theropithecus sp. indet., cf. Cercopithecoides sp. indet., and two colobine species of indeterminate genus in the non-hominin primate material (Harris et al., 2003). Expeditions conducted from 2007 to 2015 significantly expanded the sample of non-hominin primates, increasing the total

series to 156 specimens and allowing a re-assessment and refinement of the cercopithecid fossils from Kanapoi. The Kanapoi sites represent a composite record of three sedimentary sequences, the lower fluvial sequence, the lacustrine phase, and the upper fluvial sequence, dipping gently to the west (Leakey et al., 1995; Feibel, 2003). Most of the cercopithecids under discussion here derive from the lower fluvial and lacustrine/deltaic sequences, with only a handful from the upper fluvial sequence, and therefore date to between ~4.1 and 4.2 Ma, with most close to 4.2 Ma. We present here a summary of the new Kanapoi cercopithecid fossils, with a re-evaluation of previously described material. We recognize the newly described guenon Nanopithecus browni (Plavcan et al., 2019), along with Parapapio cf. ado, Theropithecus sp. indet., cf. Kuseracolobus sp. indet., and at least one larger colobine. We also evaluate the expanded sample in terms of taxonomic diversity, paleoecological and biological implications and compare it to those from other eastern African early Pliocene sites.

* Corresponding author. E-mail addresses: [email protected] (S.R. Frost), [email protected] (C.V. Ward), [email protected] (F.K. Manthi). https://doi.org/10.1016/j.jhevol.2019.102642 0047-2484/© 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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2. Systematic paleontology Order Primates Linnaeus, 1758 Suborder Haplorhini Pocock, 1918 Infraorder Catarrhini Geoffroy, 1812 Superfamily Cercopithecoidea Gray, 1821 Family Cercopithecidae Gray, 1821 Subfamily Cercopithecinae Gray, 1821 Tribe Cercopithecini Gray, 1821 Genus Nanopithecus Plavcan et al., 2019 Diagnosis: See Plavcan et al., 2019 Type species: Nanopithecus browni Plavcan et al., 2019 Nanopithecus browni Plavcan et al., 2019 (¼ or including: Cercopithecus sp. A, Leakey, 1976: Leakey, 1988; Cercopithecini gen. et sp. indet. Frost, 2001; Cercopithecus sp. indet. B, Jablonski et al., 2008a). Type specimen: KNM-KP 53150 right M3 and left M2 Other Kanapoi specimens included: (?) KNM-KP 58710 right distal humerus. Diagnosis: See Plavcan et al., 2019. Range: 4.2e3.3 Ma. Distribution: Kanapoi and Tulu Bor Member of the Koobi Fora Formation. Description: This species is known from just two craniodental specimens: the holotype from Kanapoi and the paratype KNMER 396, a right mandibular corpus fragment with M2-3 from the Tulu Bor Member (or below) of the Koobi Fora Formation (Jablonski et al., 2008: see their Fig. IV.6.). In size, the Kanapoi guenon is similar to extant species of Miopithecus. Morphologically, the molars are characteristically bilophodont and the third molars lack a hypoconulid, consistent with their identification as a guenon. Guenon molars are relatively uniform morphologically, making species identifications difficult. Though the molars are slightly smaller than the mean for extant Miopithecus, they are distinctly elongated mesiodistally by comparison to the extant species (Plavcan et al., 2019). The Kanapoi specimens show only light wear, allowing an assessment of relative shearing crest development. This demonstrates that N. browni falls outside the known range of variation of Miopithecus and other extant guenons, with the molars showing relatively low relief (Plavcan et al., 2019). KNM-KP 58710 is a distal fragment of a right humerus of a very small cercopithecid. In size, it is consistent only with N. browni among the Kanapoi cercopithecids. Although damaged (so its dimensions can only be estimated), the total bi-epicondylar breadth would have been under 17 mm. Morphologically, it is also similar to the distal humeri of most guenon species, and lacks some of the more marked terrestrial adaptations of most papionins. The bone is broken just proximal to the supraradial and supraulnar fossae with damage to the lateral condyle, lateral border of the olecranon fossa, and distal edge of the trochlea and medial epicondyle. The articular surface is smooth, lacking a prominent zona conoidea with a capitulum that is not well differentiated. Due to damage, it is difficult to gauge the morphology of the medial trochlear flange, but this flange is unlikely to have been very long or sharp. The medial epicondyle is only moderately retroflexed. Posteriorly, the olecranon fossa is shallow and relatively proximodistally short and mediolaterally broad. Remarks: In spite of its rarity, N. browni is of considerable importance in understanding guenon evolution as it marks the first appearance of the tribe in Africa proper. It is exceeded in age only

by the isolated molar from the latest Miocene Baynunah Formation Abu Dhabi (Gilbert et al., 2014). Nonetheless, the Kanapoi guenon is considerably younger than molecular estimates of 13e8 Ma for the origin of cercopithecins (e.g. Raaum et al., 2005; Tosi et al., 2005; Perelman et al., 2011; Springer et al., 2012), and younger even than the divergence dates for individual extant genera 4e8 Ma (e.g. Tosi et al., 2005; Perelman et al., 2011; Springer et al., 2012). At approximately 3.4 Ma, the last appearance of N. browni in the Tulu Bor Member at Koobi Fora nearly overlaps with the first appearance of other, larger guenon species from the Usno Formation, Omo River Valley, Ethiopia (Eck, 1987) establishing based on fossil evidence that the tribe was differentiated into at least two genera by the early Pliocene. The phylogenetic position of the small guenon from Kanapoi among cercopithecins is difficult to assess at this point given the fragmentary nature of the remains and a general lack of consensus about the polarity of morphological features within the tribe. That said, the lack of adaptations for terrestrial locomotion in the humerus suggests Nanopithecus is not closely related to the terrestrial guenon clade (Tosi et al., 2004; Xing et al., 2007). Tribe Papionini Burnett, 1828. Genus Parapapio Jones, 1937 Diagnosis: see Jablonski and Frost (2010) Type species: Parapapio broomi Jones, 1937 Other included species: Pp. ado (Hopwood, 1936), P. jonesi Broom, 1940; P. whitei Broom, 1940; P. lothagamensis Leakey et al. (2003). Remarks: Parapapio is most clearly diagnosed by slight or absent maxillary fossae and ridges as well as lack of anteorbital drop, thus requiring the presence of facial material to be definitive (Freedman, 1957). Three species are securely placed in the genus; from smallest to largest these are Parapapio jonesi, P. broomi, and P. whitei (e.g. Freedman, 1957; Szalay and Delson, 1979; Delson, 1984; Jablonski, 2002; Jablonski and Frost, 2010; Gilbert, 2013). Parapapio antiquus, known only from Taung, has been previously included in the genus (e.g. Freedman, 1957; Szalay and Delson, 1979; Delson, 1984; Frost, 2001b, 2007a; Jablonski, 2002; McKee and Kuykendall, 2016), but was recently named the type of a new genus Procercocebus (Gilbert, 2007, 2013; Jablonski and Frost, 2010). In South Africa, Parapapio is the most abundant cercopithecid during the Pliocene and early Pleistocene, but in eastern Africa it is only securely identified from Hadar based on a male partial cranium and female partial face of Parapapio cf. jonesi (Frost and Delson, 2002). Two additional species from eastern Africa are also often included in the genus, P. ado from Laetoli and possibly other sites (Leakey and Delson, 1987; Harrison, 2011), and Parapapio lothagamensis from the late Miocene Nawata Formation (Leakey et al., 2003). Diagnostic facial material is not known for P. ado making its inclusion in the genus less secure, but two isolated frontal fragments from Laetoli that likely derive from this species suggest it may have lacked an anteorbital drop (Harrison, 2011). This, along with the absence of mandibular corpus fossae, relatively small P4s, and molars with modest levels of flare (i.e. more than Theropithecus and most guenons, but less than Cercocebus and Lophocebus) are all consistent with its placement in Parapapio, although other identifications are still possible. P. lothagamensis shares the lack of anteorbital drop and absence of maxillary fossae with other species of the genus, but shares some features with Victoriapithecus and may be significantly more primitive than the better-known species of Parapapio and, therefore, may warrant generic distinction (Harrison, 2011; Gilbert, 2013).

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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Parapapio ado (Hopwood, 1936). (¼ or including: Cercocebus ado Hopwood, 1936. Papio (Simopithecus) serengetensis Dietrich, 1942, in part. P. jonesi Broom, 1940: Patterson, 1968. Papionini gen. et sp. indet (B), Leakey and Leakey, 1976. ?P. ado: Delson, 1978; Szalay and Delson, 1979; P. ado:Leakey and Delson, 1987; Frost, 2001a; Jablonski and Frost, 2010; Harrison, 2011.). Type specimen: NHMUK PV M14940 Diagnosis: Following Leakey and Delson (1987) and Harrison (2011), a small species of Parapapio, intermediate in size between P. jonesi and P. broomi, distinguished from other species by its more sloping mandibular symphysis, with a more projecting alveolar margin, molar teeth that are taller and less flaring, narrower, and lack cuspules in the median lingual clefts of the upper molars. Range: 4.2e3.6 Ma (more tentatively 4.2e2.6 Ma). Distribution: Upper Laetolil Beds, (cf.) Upper Ndolanya Beds, Tanzania; (cf.) Kanapoi, (cf.) Lonyumun and Tulu Bor Members, Koobi Fora Formation, Kenya. Parapapio sp., cf. P. ado. (¼ or including: P. jonesi Broom, 1940: Patterson, 1968. Papionini gen. et sp. indet. (B), Leakey and Leakey, 1976. ?P. ado: Delson, 1978; Szalay and Delson, 1979; P. ado (Hopwood, 1936): Leakey and Delson, 1987; Frost, 2001; Jablonski, 2002; Harris et al., 2003; Jablonski and Frost, 2010). Kanapoi specimens included: Table 1. Description: The Kanapoi sample includes a series of partial mandibles, cranial fragments, and isolated teeth, with the entire lower dentition and much of the upper represented. Little maxillary morphology is present. The most complete mandibles (see Fig. 1) include the reconstructed partial corpus of a male KNM-KP 286 (Patterson, 1968: Fig. 1), KNM-KP 29306 a left corpus fragment with P3-M3 of a male (Harris et al., 2003: Fig. 9); KNM-KP 53085 a fragment of a right corpus with I1-M2 of a male; KNM-KP 30230 partial mandible of a subadult female with right P3-M3 and left corpus and partial ramus with M1-3, with the M3s partially erupted bilaterally; KNM-KP 26942 right mandibular corpus fragment with M1-3 (Fig. 1). There are also several more fragmentary specimens and isolated teeth (Table 1). The mandible is characterized by a strongly sloping symphysis, considerably more so than that of the Theropithecus sp. specimen KNM-KP 58577, with a relatively projecting alveolar margin suggesting that the incisors would have been somewhat procumbent. Moderate mental ridges are variably present, especially in the male individuals KNM-KP 286 and KNM-KP 29306. The mandible is also pierced by a median mental foramen. In lateral view, the symphysis has the somewhat “sigmoidal” shape characteristic of some Laetoli mandibles as described by Frost (2001a). This is particularly so in KNM-KP 286 and KNM-KP 30147. The superior transverse torus extends posteriorly to the level of the P3 and the inferior to the P4. As is typical of papionins, the corpora of the males are distinctly deeper anteriorly and shallow posteriorly under the M3 (Table 2). The females are more even in depth, but are still moderately shallower posteriorly. The lateral surface lacks corpus fossae. The mental foramen is multiple, located approximately under the P4 and along the superior border of the mental ridges. In superior view, the corpora are not particularly broad, and the extramolar sulcus is relatively narrow. The one specimen that preserves any of the ramus, KNM-KP 30230, reveals it to be more vertically oriented compared to the corpus than it is in most Papio, and marked by a deep and distinct triangular fossa. The dentition of the Kanapoi Parapapio cf. ado is typical of most papionins. Dental dimensions are summarized in Table 3 with

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individual values in Supplementary Online Material (SOM) Table S1. In overall dental size, this material is comparable to P. jonesi from South Africa (Freedman, 1957; Eisenhart, 1974), somewhat smaller than P. ado from Laetoli (Leakey and Delson, 1987; Harrison, 2011, Fig. 3), and larger than Pliopapio alemui from Aramis (Frost, 2001a, Fig. 3). The I1 crown is relatively flaring and spatulate in morphology with its mesial border being more angled than the distal. It lacks the lingual cingulum typical of colobines. It is larger than the I2, but not as much as in many cercopithecins. The I2 is more mesially angled and mesiodistally narrower than the I1. The lower incisors are narrower and more equal in size than the uppers, and lack lingual enamel. Compared to the size of the molars, the incisors are fairly large, being relatively smaller than those of most cercopithecins and relatively larger than those of Theropithecus or colobines. The canines are sexually dimorphic and typical of the family. The upper premolars are typical bicuspid teeth. The P3 and P4are relatively close in size and generally lack the larger talonid or complexity of Theropithecus. The P3 is a relatively conical tooth possessing a narrow talonid. The mesiobuccal honing facet of the males is significantly longer than that of the females, but in relationship to overall crown size it is not as extended as in extant Papio or Mandrillus, being rather more similar to Parapapio from South Africa in this regard. The P4 generally lacks a mesiobuccal extension, and the lingual margin of the talonid is relatively high in comparison to the trigonid and lacks the deeply defined lingual notch of colobines. The P4 is essentially in line with the molars and is not obliquely oriented. Both the upper and lower P4s are relatively small in area by comparison to the M1s. In terms of crown height, basal flare and the position of the cusps relative to the crown margins, the molars are typical for papionins. They show less basal flare than extant Lophocebus and Cercocebus, but more than is present in Theropithecus, Pliopapio, most cercopithecins (other than Allenopithecus) and most colobines. In this regard, the molars of the Kanapoi Parapapio cf. ado are also more flaring than those of Pp. ado from Laetoli and P. alemui (Frost et al., 2009, Fig. 3). In terms of buccolingual crown breadth of mandibular molars, the M2 is the broadest tooth, which is typical of most papionins, but unlike Theropithecus. Using the prediction equations and methods from Delson et al. (2000) we estimated the population mean body masses for males and females using all of the P. cf. ado molars from Kanapoi attributable to sex. Males and females are estimated to have mean body masses of 14 kg (range 12e17 kg) and 10 kg (8e12 kg) respectively. These values are modestly larger than those for Pl. alemui from Aramis (12 and 7.5 kg for males and females; Frost, 2001) and smaller than those for P. ado from Laetoli (21 and 12 kg), and to a lesser extent, P. jonesi (17 and 11 kg) (Delson et al., 2000). These values also result in a relatively low level of sexual dimorphism for a papionin of approximately 1.4:1, although the sample sizes are quite small. Remarks: Taxonomic identification of the medium-sized papionins from Kanapoi is complex and their relationships to those from broadly contemporary sites are ambiguous. Consequently, the position of the Kanapoi material in this regard merits some discussion. The first primate specimen described from Kanapoi (KNM-KP 286, published as 122-66K) is a partial male mandible of a mediumsized papionin attributed to P. jonesi by Patterson (1968) largely based on size and a lack of corpus fossae1. Leakey and Leakey (1976) were more conservative and assigned this specimen to Papionini

1 The specimen was partially reconstructed with plaster (see Patterson, 1968: Fig. 1), which was intact as of 1999. Since then, the plaster (but not the fossil itself) in the area of the right corpus has been damaged displacing the portion of the corpus containing the M2-3 towards the left corpus.

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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Table 1 Specimens allocated to Parapapio cf. ado. Cat. No. KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP

Cat. No. Description

36969 26942 286 29295 29304 29305 29306 29310 29311 29312 30147 30149

KNM-KP 30213 KNM-KP 30230 KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP

Table 1 (continued )

30233 30399 30483 30531 30532 30535 30538a 30538b 30538c 30538d 30538e 30538f 30538h 30538i 30538j 30538k 30538l 30538m 30538n 30538 30538p 30538q 30539 30558 32520 32527 32534 32535 32572 32804 32805 32806 32811 32816 32817 32819 32819 32869 32878 36914 37374 37378 37379 37380 43122 50734 50743 50746 53085 53148 53156 56929 57004 57010 58700 58733 59886

left P4, M frag., right female C1 right mandible with M1-3 male mandible with left C,P4-M1,M3 and right C, M2-3 right M1 or 2 left mandible with M1-2, isolated M3 talonid fragment right M3 male left mandible with P3-M3 right MX, prob. M2 left I2 left mandible with M2-3 mandibular symphysis and left corpus, edentulous mandible with left dC-M1 and right di2-M1; left maxilla with dc-M1; right maxilla with dp3-M1; associated left di1, I1 and right di1, dc1, i1 right M2 female right mandible with P3-M3; left mandible with M1-3 male left mandilbe with M3, right edentulous mandible right M3 left M3 female mandibular symphysis with left P4 - right P4 left mandible with P4-M2 left M3 female right mandible with left I1, right I1-M1,3 left mandible with M2-3 left frontal mastoid process basioccipital rigth temporal left maxilla with I1eP3 left M3 M1 P3 left mandible with I2eP3 zygomatic fragments right I mandibular fragments fragments left female maxilla with I2eC roots right M1 or 2, prob. M1 right edentulous mandible left edentulous female mandible, right I2 dPX right M1 or 2 right M2 left dp4 left MX fragment right MX fragment M3 right M3 fragment right I1 right M3 right maxilla with P34 left edentulous premaxilla male left C1, and right M3 right dp3 left M1 or 2, prob. M2 and associated M fragment Tooth fragments MX fragments right M3 hypoconulid, I1 I2 right dp4 maxillary fragments with left P3,M23, right I2, P4, M12 left I2 right M3 male right mandible with I1-M2 left M1 or 2, male right P3 P4 right M3 left MX right M1 or 2, prob. M1 right MX fragment, prob. M1 left M1 or 2, prob. M1 left MX

KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP

Description 59887 59891 59896 59898 59899

left M1 or 2 right mandible with dp4-M1 left P4 right M3 right M3

genus et species indet. B, but noted its similarity to material from Laetoli (which they recognized as Cercocebus ado Hopwood, 1936). Szalay and Delson (1979) tentatively recognized KNM-KP 286 and the Laetoli material together as ?P. ado. Leakey and Delson (1987), based on an expanded sample, recognized KNM-KP 286 along with most of the Laetoli papionin material as P. ado. Their attribution of this material to Parapapio was based on the absence of mandibular corpus fossae and molars that show a level of crown flare typical of the tribe, but less flare than found in extant Cercocebus (and presumably Lophocebus, which was generally considered a junior synonym of Cercocebus at the time). Harris et al. (2003) also included the greatly expanded Kanapoi series within P. ado, as have most authors, at least tentatively (Frost, 2001a,b; Frost, 2007a; Jablonski et al., 2008; Jablonski and Frost, 2010). Harrison (2011), however, suggested the Kanapoi material was specifically distinct from the type series of P. ado from Laetoli. He based this distinction on the smaller size, narrower and more sloping mandibular symphysis, shallower and more gracile mandibular corpus with more distinct fossae, as well as broader and more low-crowned molars with different relative proportions than specimens in the Laetoli sample. Instead, he argued that the Kanapoi (and Koobi Fora Lonyumun Member) material showed more affinities with the much older P. lothagamensis, and suggested that together they may represent a distinct taxon (Harrison, 2011). Here we include the Kanapoi medium-sized papionin material within Parapapio for the same reasons (lack of mandibular corpus fossae and typical papionin dentition) as most previous authors, but confirmation of this diagnosis will require more complete facial material. Several other genera can also be ruled out or seem unlikely. The Kanapoi medium-sized papionin specimens lack the distinctive dental morphology of Theropithecus, even in primitive form (e.g. Szalay and Delson, 1979; Frost et al., 2014). The symphysis is more sloping and the molars are lower crowned, more flaring, and broader than those of Pliopapio (Frost, 2001a). Biogeography suggests Macaca would be an unlikely attribution, but there are few morphological reasons to exclude it. The lack of mandibular corpus fossae makes Papio, Mandrillus, Lophocebus, and to a lesser extent Cercocebus, unlikely as well (e.g. Szalay and Delson, 1979; Jablonski and Frost, 2010). Molar morphology also makes Cercocebus and to a lesser extent Lophocebus unlikely, though the Kanapoi specimens do overlap the latter in lateral flare. The relative size of the P4 also argues against Mandrillus or Cercocebus (Fleagle and McGraw, 2002). Thus, pending the discovery of more complete facial material, Parapapio is the most reasonable diagnosis. The specific affinities of the Kanapoi Parapapio cf. ado material also require caution. While similar to P. ado from Laetoli (especially the lectotype of P. ado M14940) in symphyseal morphology, lack of mandibular corpus fossae, and broadly in overall size (Leakey and Leakey, 1976; Leakey and Delson, 1987; Delson et al., 2000; Frost, 2001a; Harris et al., 2003, Fig. 2), there are also a number of differences. The Kanapoi material is smaller on average, although with overlap, and has molars that are lower-crowned, broader, and more flaring (Frost, 2001a; Harrison, 2011, Fig. 3; SOM Table S2). In fact, Parapapio cf. ado from Kanapoi is more similar in these last features to the three Parapapio species from South Africa. In summary, given the overall resemblance of Kanapoi Parapapio cf. ado to the type

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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Figure 1. Parapapio cf. ado. KNM-KP 286 male mandible with left I1eC1 roots, P4-M1, M3, and right I1eC1 roots, M2-3, superior and lateral views; KNM-KP 29306 male left mandible with P3-M3, superior and lateral views; KNM-KP 53085 right male mandible with I1-M2, superior and lateral views; KNM-KP 30230 left and right female corpora with left M1-3 and right P4-M3, superior left and right lateral views; KNM-KP 26942 right corpus with M1-3, occlusal and lateral views.

material from Laetoli, Tanzania, in corpus morphology in general, and symphyseal morphology in particular, we tentatively retain identification as P. cf. ado for this series, but recognize differences in molar size, relative breadth and crown flare. Moreover, it is currently unclear whether these differences from the type series are chronological between the 4.2 Ma Kanapoi sample and that from Laetoli at ~3.7 Ma (with the Allia Bay papionins possibly bridging the two at 3.9 Ma) or truly indicate separate lineages (Jablonski et al., 2008; Harrison, 2011). There is also the possibility

that some specimens allocated to P. ado from Laetoli may be primitive Theropithecus (personal observation, Frost et al., 2014; Frost et al., 2018), which may alter our understanding of P. ado and affect these comparisons. Papionins of similar size from a range of early Pliocene localities have also been tentatively identified as P. ado. These include a sizeable sample of isolated teeth and a few very fragmentary gnathic elements from the Lonyumun (3.9 Ma) and Lokochot (3.6 Ma) Members at Koobi Fora (Jablonski et al., 2008), a relatively

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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Table 2 Mandibular dimensions in millimeters.a Catalog Number

Taxon

Sex

Width C1

Width M2/M3

KNM-KP 29255 KNM-KP 286 KNM-KP 29306 KNM-KP 53085 Laetoli Range Laetoli Range

cf. Kuseracolobus sp. Parapapio cf. ado Parapapio cf. ado Parapapio cf. ado Parapapio ado Parapapio ado

F M M M F M

15 24

39

Symphysis Height

Depth P4/M1 19

37

28 23

34 37 39e45

45

27 28 23e29 28e31

Depth M1/M2

Depth M2/M3

Breadth M2/M3

20 27 27 27 24e30 29e31

22 27 25 27 23e32

13 12 10 (11) 10e14 13e14

a

Width C1 ¼ width from left to right alveolar margin at the canines, Width M2/M3 ¼ width at the M2 e M3 contact, Symphysis Height ¼ depth from between I1s to the inferior margin in the midline, Depth P4/M1 ¼ depth from alveolar margin to inferior margin at the P4 e M1 contact, Depth M1/M2 ¼ depth from alveolar margin to inferior margin at the M1 e M2 contact, Depth M2/M3 ¼ depth from alveolar margin to inferior margin at the M2 e M3 contact, Breadth M2/M3 ¼ corpus breadth at the M2 e M3 contact. Values in parentheses ( ) are estimates. Table 3 Summary of dental dimensions in millimeters for Parapapio cf. ado.a Tooth

N

I1 I2 P3 P4 M1 M2 M3 MX di1 dc1 dp3 dp4 I1 I2 C1(F) C1(M) P3(F) P3(M) P4 M1 M2 M3 MX dc1 dp3 dp4

1 1 3 3 1 1 1 7 1 1 1 3 4 4 2 3 2 2 7 9 7 19 9 1 1 5

Widtha

Other measuresb

Lengthc

Mean

Min.

Max.

Mean

Min.

Max.

Mean

Min.

Max.

5.8 5.4 6.8 7.0 7.9 10.9 9.6 9.6 3.7 3.8 5.7 6.4 5.6 6.2 6.6 9.7 4.1 4.7 5.5 7.2 8.8 8.9 7.5 3.1 4.4 5.5

e e 6.0 6.6 e e e 8.8 e e e 5.9 4.7 5.5 6.1 8.8 3.6 4.6 4.9 5.9 7.9 7.8 6.0 e e 4.9

e e 7.2 7.4 e e e 10.3 e e e 6.9 6.4 6.8 7.1 10.5 4.7 4.8 6.1 8.4 9.8 10.1 9.1 e e 6.1

11.3 6.9 e e 7.3 9.1 8.3 7.9 3.7 5.2 6.2 6.0 5.7 7.8 8.9 14.9 8.4 15.2 e 7.2 8.4 7.8 7.0 4.5 4.7 5.4

e e e e e e e 6.9 e e e 5.5 5.3 5.2 6.7 e e 14.8 e 6.1 7.2 6.5 6.0 e e 5.1

e e e e e e e 9.1 e e e 6.6 6.2 12.0 11.1 e e 15.5 e 8.4 9.2 8.6 7.9 e e 5.7

7.5 4.1 5.3 5.6 9.2 10.8 9.6 9.2 6.2 5.0 7.1 7.5 4.9 5.2 3.5 6.2 6.7 8.2 6.4 8.2 10.2 12.4 9.2 4.4 7.3 7.1

e e 5.1 5.6 e e e 7.8 e e e 7.3 4.3 4.8 3.4 6.3 e 7.8 5.8 7.3 9.3 10.9 8.2 e e 6.9

e e 5.4 5.7 e e e 10.7 e e e 7.7 6.1 5.7 3.7 6.3 e 8.6 7.0 9.1 11.1 14.3 10.4 e e 7.6

a All widths are buccolingual and in the case of molars widthis measured across the mesial moiety. Other measures include: crown height for incisors and canines; for lower third premolars flange height is taken from the protoconid to the inferior tip of the mesiobuccal honing flange; for the molars distal width across the distal moiety is presented. Dental dimensions for individual specimens are given in the Supplementary Online Material (SOM) Table S1. Min. ¼ minimum, Max. ¼ maximum.

complete mandibular corpus from the lower Lomekwi Member (3.3 Ma), Nachukui Formation (Harris et al., 1988), as well as a partial lower third molar from Ekora (unknown age, but likely close to Kanapoi) (Leakey and Delson, 1987). The material from Koobi Fora is broadly similar to fossils from both Kanapoi and Laetoli. In shape the molars of the Lonyumun Member material are generally closer to those from Kanapoi being relatively broad, but are less flaring. In size, they encompass the ranges of both Laetoli and Kanapoi. A well-preserved mandible, KNM-WT 16752, comes from the lower Lomekwi Member of the Nachukui Formation and was assigned to cf. Pp. ado by Harris et al. (1988). In both the size of the corpus and dentition it is close to P. cf. ado from Kanapoi, but the symphysis is shorter and more vertical than P. cf. ado from Kanapoi, especially KNM-KP 286, and the molars are buccolingually narrower in proportion. The tooth from Ekora is non-diagnostic beyond being similar in size to the Kanapoi papionin. The same can be said for other similarly-sized isolated papionin teeth from other sites throughout eastern Africa.

Within the Pp. cf. ado material from Kanapoi there is a considerable size range, even within sexes. For example, the male mandibles KNM-KP 29306 and KNM-KP 53085 differ markedly in size (with KNM-KP 286 being closer to KNM-KP 53085), possibly suggesting the presence of two species within the Kanapoi Pp. cf. ado series. That said, the range of variation in molar size does not exceed that within most extant papionin species. Only additional specimens will clarify this issue. Genus Theropithecus I. Geoffroy, 1843 Diagnosis: see Frost and Delson (2002) Type species: Theropithecus gelada (Rüppell, 1835) Other included species: T.oswaldi (Andrews, 1916), ?T. brumpti (Arambourg, 1947), ?T. baringensis (Leakey, 1969). Remarks: There are two well-known lineages of Theropithecus in the fossil record, T. oswaldi and T. brumpti, often separated at the sub-generic level with T. brumpti in T. (Omopithecus) and T. oswaldi together with extant T. gelada in T. (Theropithecus) (e.g. Delson, 1993; Delson et al., 1993; Jablonski, 1993; Frost, 2001b; Jablonski, 2002; Jablonski and Frost, 2010; Gilbert, 2013). Following Leakey (1993a,b), T. oswaldi includes three chronosubspecies, from oldest to youngest: T. o. darti, T. o. oswaldi, and T. o. leakeyi (e.g. Frost and Delson, 2002; Frost, 2007b; Gilbert, 2013). While nearly indistinguishable in molar morphology, the T. oswaldi lineage is distinguished from T. brumpti by a lack of maxillary fossae, maxillary ridges, and mandibular corpus fossae, as well as several evolutionary trends in dental and body size (e.g., Eck and Jablonski, 1987; Delson, 1993; Jablonski, 1993; 2002; Jablonski and Frost, 2010; Gilbert, 2013). The two forms are also similar in postcranial morphology (Guthrie, 2011). The T. oswaldi lineage is pan-African, and spans from at least 3.7 Ma to less than 0.5 Ma whereas T. brumpti is only known from the Turkana Basin and Tugen Hills, and ranges from at least 3.6 Ma to 2.0 Ma (Jablonski et al., 2008; Jablonski and Frost, 2010; Gilbert et al., 2011; Frost et al., 2014). An additional species, ?T. baringensis from the Tugen Hills, Kenya, is tentatively placed as a primitive member of the genus (Eck and Jablonski, 1984, 1987; Delson and Dean, 1993; Leakey, 1993a,b; Gilbert, 2013). Although at 3.2 Ma it is geologically younger than the earliest T. oswaldi or T. brumpti, it is nonetheless considered more primitive than the other forms, although its exact phylogenetic position is debated (Eck and Jablonski, 1984, 1987; Delson and Dean, 1993; Delson, 1993; Leakey, 1993a,b; Gilbert, 2013). Finally, there are fragmentary fossils assigned to the genus, but of unknown specific affinity. These include several isolated teeth from the Lonyumun Member of the Koobi Fora Formation (Jablonski et al., 2008) dated to 3.9 Ma and a right corpus fragment with P4-M3 of a female from Wee-ee in the Middle Awash, Ethiopia, also 3.9 Ma (Frost, 2001b). An isolated molar of Theropithecus from Lothagam was once thought to represent an early and possibly distinct member of the genus (Delson, 1993). Leakey et al. (2003)

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

7

Figure 2. Comparison of medium-sized papionin mandibles from Laetoli and Kanapoi. Laetoli material is on the left and Kanapoi on the right. Laetoli specimens include: NHML M14940 right female mandible with P3-M3, lectotype of Parapapio ado (Hopwood, 1936); MB Ma. 42441 (¼ MB, 1938.1) female mandible with left I1-M3 and right M1-3, type specimen of Papio (Simopithecus) serengentensis Deitrich, 1942 (usually considered a junior synonym of P. ado); NMT EP 700/00 male mandible with complete dentition except left C1. Kanapoi specimens include: KNM-KP 30230 left and right female corpora with left M1-3 and right P4-M3; KNM-KP 286 partially reconstructed male mandible with left I1eC1 roots, P4-M1, M3, and right I1eC1 roots, M2-3 (reversed); KNM-KP 53085 right male mandible with I1-M2.

subsequently discovered several additional specimens from the Kaiyamung Member of the Nachukui Formation (3.3 Ma), and argued they most likely represent an early sample of the T. brumpti lineage. Theropithecus sp. indet. (¼ or including cf. Theropithecus sp. Harris et al., 2003; Colobinae gen. et sp. indet. B Harris et al., 2003) Kanapoi specimens included: KNM-KP 29308 L. male corpus with erupting P3, roots C, P4-M1; KNM-KP 32879 rightM1 or 2, probably M2; KNM-KP 58577 male mandibular corpus with complete

dentition; KNM-KP 59888 right maxillary molar, probably M3; KNM-KP 59892 right P4; KNM-KP 59897 right M3. Description: This species is noticeably larger than P. cf. ado in both the mandible and dentition (Table 4), and it can be readily distinguished from that taxon on size grounds alone for most of the teeth. KNM-KP 58577 preserves nearly the entire corpus and lower dentition except for the tip of the left canine and the incisors which are heavily worn (Fig. 4). The corpus is also crushed and sheared rightward so that the left corpus is displaced inferiorly relative to the right. A considerable amount of the cortical bone is missing, and there is also cracking and crushing of the surface. A further complication is that the matrix surrounding the specimen can be

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

Figure 3. Box and whisker plots comparing M3 size and proportions among medium-sized papionins from the early Pliocene sites of Aramis (P. alemui dated to 4.4 Ma), Kanapoi (P. cf. ado dated to 4.2 Ma), Alia Bay (medium sized papionins allocated to P. cf. ado by Jablonski et al., 2008a dated to 3.9 Ma), and Laetoli (Pp. ado dated to 3.7 Ma). These compare occlusal area (upper left), relative breadth (lower left), basal flare of the crown (upper right) and relative relief of the metaconid (lower right). The central bar of each box represents the median, or 50th percentile. The bottom and top of each box represent the 25th and 75th percentiles respectively. The whiskers extend to the furthest observation. Aramis Pl. alemui data from Frost (2001b). Laetoli P. ado data from the Primate Morphometrics Online (PRIMO) database (https://primo.nycep.org/).

difficult to distinguish from fossilized bone. Unambiguous natural bone surface is preserved near the midline of the external surface of the symphysis to just inferior to the right canine root and the lateral surface of the inferior border of the left corpus, from P3 to M2 as well as the inferior edge of the right corpus, under the M2-3. A piece of fossilized bone attached to the posterior portion of the left corpus does not smoothly articulate with the remainder of the specimen and appears to be displaced, tilting anteriorly, inferiorly, and medially. The surface of this piece is cracked, but does not appear distorted or crushed. Given the preservation of KNM-KP 58577, much of the mandibular morphology is difficult to assess, and measurements of the corpus are unreliable. In overall size and robusticity, KNM-KP 58577 is close to the KNM-BC2b and KNM-BC 1647a mandibles attributed to ?T. baringensis (Leakey, 1969; Eck and Jablonski, 1984; Delson and Dean, 1993; Gilbert, 2013). The corpus of KNM-KP 58577 is somewhat shallower than those of ?T. baringensis. The lateral surfaces appear to lack corpus fossae, but this may be due to distortion. The exact position of the mental foramen is difficult to

judge due to the preservation. The symphysis is damaged such that it is impossible to tell if a median mental foramen was present. If mental ridges were present, they would not have been prominent. In lateral view, the symphysis appears fairly vertical making an angle of approximately 50e60 to the occlusal plane. If this is correct, then KNM-KP 58577 would also be similar in symphyseal slope to KNM-BC2, the type specimen of ?T. baringensis (Leakey, 1969) from the Chemeron Formation, Kenya. The dorsal surface of the superior transverse torus is concave and extends posteriorly to the level of the mesial part of the P3. The inferior torus reaches as far posteriorly as P4. The only Theropithecus incisors and canines preserved at Kanapoi are those of KNM-KP 58577. The incisors are small relative to the size of the molars, although they are heavily worn. They are otherwise typical of the tribe in morphology. They lack lingual enamel, and the crowns are slightly flaring in labial view. The lower canines are large and prominent as is typical of male cercopithecids. Both KNM-KP 29308 and KNM-KP 58577 preserve the P3, and their morphology is very similar. The P3 crown is tall relative to the

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

Subfamily Colobinae Jerdon, 1867 Genus Kuseracolobus Frost, 2001

Table 4 Dental dimensions in millimeters for Theropithecus sp.a Catalog Number KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP

32879 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 58577 59888 59892 59897

(l) (l) (l) (l) (l) (l) (l) (l) (r) (r) (r) (r) (r) (r) (r) (r)

Sex M M M M M M M M M M M M M M M M

Tooth

WS

Width

MX I1 I2 C1 P3 P4 M1 M2 M3 I1 I2 C1 P3 P4 M1 M2 M3 MX P4 M3

0

e 5.9 5.8 10.8 5.7 6.2 6.9 9.4 9.7 6.0 6.5 10.5 5.6 6.1 6.9 9.1 9.1 10.9 6.5 e

9 8

2 11 8 5 7

9

Other 8.5 4.2 4.5 18.6 e 7.8 9.7 8.8 4.4 6.9 19.1 19.9 e 7.1 9.4 8.8 10.4 e 9.6

Length 11.7 5.4 4.3 7.2 11.0 6.6 9.2 12.3 14.9 5.7 5.1 6.7 10.5 7.4 9.2 12.3 14.5 12.0 8.9 e

a Dimensions same as for Table 3. WS, dental wear stage (after Delson, 1973). Values in parentheses ( ) are estimates.

P3s of Parapapio cf. ado, largely due to the prominent conical protoconid. The paraconid is relatively distinct. The mesiobuccal honing flange is long and quite vertically oriented, as is typical of male papionins. It is relatively longer than that of Pp. cf. ado. The P4s of both KNM-KP 58577 and KNM-KP 59892 have well-developed talonids and show some of the enamel infoldings typical of Theropithecus. The molar teeth show the complexly folded enamel and columnar cuspal morphology typical of Theropithecus, although they are very primitive and low crowned (Fig. 4). In this regard, they are like molars from Woranso-Mille, Ethiopia, but simpler than younger members of the T. oswaldi lineage and T. brumpti (Frost et al., 2014). In occlusal shape, they are relatively elongate compared to those of most papionins, with the M2 being quite rectangular in outline. In size, the molars are similar to those of T. gelada and ?T. baringensis, but smaller than those of T. brumpti and T. oswaldi, although they do overlap the range from Woranso-Mille (Table 5). On KNM-KP 58577 the molars increase in mesial breadth from M1 to M3. In terms of occlusal area, the M1 is small compared to the M2, a feature shared with T. gelada, T. brumpti, and T. oswaldi, but not ?T. baringensis. The M3 is not as enlarged relative to the M2 as in other Theropithecus. Remarks: Harris et al. (2003) provisionally identified a single, isolated molar from Kanapoi (KNM-KP 32879) as possibly marking the earliest well-dated appearance of Theropithecus in the fossil record. The new material described here confirms their tentative identification, marking the Kanapoi series as the current first appearance datum for the genus. After Kanapoi, the earliest specimens attributed to Theropithecus are those mentioned above from the Lonyumun Member of the Koobi Fora Formation and from Wee-ee in the Middle Awash, both dated to 3.9 Ma (Frost, 2001b; Jablonski et al., 2008). The earliest specimens that can be assigned to one of the well-known fossil lineages is the large series of T. oswaldi cf. darti from Woranso-Mille spanning the 3.8e3.6 Ma interval (Frost et al., 2014) and fragmentary material that most likely represents T. brumpti from the Lokochot Mb., Koobi Fora Formation dated to approximately 3.5 Ma (Jablonski et al., 2008). In size and morphology, the Kanapoi material is similar to both ?T. baringensis and the indeterminate Theropithecus from 3.9 Ma and is therefore unclear in its specific affinities.

Diagnosis: See Frost, 2001a Type species: Kuseracolobus aramisi Frost, 2001 Other included species: Kuseracolobus hafu Hlusko 2006 Remarks: Kuseracolobus has been previously recognized only from the Afar region, Ethiopia. K. aramisi has been described from the Aramis and Kuseralee Members of the Sagantole Formation in the Middle Awash (Frost, 2001a; Frost et al., 2009), the As Duma and Segala Noumou Members of the Sagantole Formation in the Gona Project area (Semaw et al., 2005) and tentatively from the Adu Asa Formation in the Middle Awash (Frost et al., 2009). The significantly larger species K. hafu is known from Asa Issie, also in the Middle Awash and close in age to Kanapoi (Hlusko, 2006). The genus is distinguished from other fossil genera by several features (Frost, 2001a). It differs from Cercopithecoides by having a deeper more posteriorly sloping mandibular corpus, with an expanded gonial region. It is also different from Paracolobus and Rhinocolobus by having a much more robust corpus with well-developed prominentia laterales. It is distinguished from all three genera by its relatively shorter face. It differs from extant colobinans in having a relatively larger P4 protocone. The distal lophid of M3 is not broader than the mesial further distinguishing it from Colobus. Kuseracolobus differs from all colobines other than Libypithecus and Cercopithecoides by possessing a maxillary sinus. Finally, it differs from Cercopithecoides in that its postcrania appear more adapted for arboreal positional and locomotor behaviors (Hlusko, 2006; Frost et al., 2009; White et al., 2009). cf. Kuseracolobus sp. indet (¼ or including cf. Cercopithecoides sp. Harris et al., 2003) Kanapoi specimens included: KNM-KP 29255 mandibular corpus of a female with right P3-M3 and left P3-M1; KNM-KP 31741 right Mx; KNM-KP 32870 left P4; KNM-KP36967 left M3; KNM-KP 43120 right P3 talonid; KNM-KP 58701 fragment of a left maxilla with a molar, likely M3, and a small molar fragment mesial to it; KNM-KP 58702 right P3; KNM-KP 59885 left I1; KNM-KP 58823 edentulous mandibular symphysis fragment of a female. Description: The best specimen of this population by far is the well-preserved mandibular corpus KNM-KP 29255 described by Harris et al. (2003) as cf. Cercopithecoides sp. KNM-KP 58823 is an edentulous mandibular symphyseal fragment that is morphologically very similar to KNM-KP 29255 (Fig. 5). There is also a very small maxillary fragment with M3 and part of M2, KNM-KP 58701 (Fig. 5). All of the other material consists of isolated teeth. In overall size, Kanapoi Kuseracolobusis is slightly larger than extant Colobus and Procolobus (Piliocolobus), but smaller than Rhinopithecus, Nasalis, and extinct K. aramisi and Cercopithecoides meaveae (Table 6). KNM-KP 58701 preserves relatively little maxillary morphology, being broken just above the apices of the tooth roots. It is clear that the alveolar margins would have likely been relatively straight, but it is not possible to determine where the zygomatic arch would have been located, or how prognathic the maxilla was. On the dorsal aspect of the specimen, however, the smooth, submucosal surface of a maxillary sinus can be observed from the small portion preserved. The Kanapoi cf. Kuseracolobus mandible is best represented by KNM-KP 29255. The corpus is anterioposteriorly short relative to the overall width of the specimen, suggesting that this species would have been fairly short-faced. The corpus is quite robust. The symphysis is vertically oriented and relatively shallow. From what is preserved, it appears to lack a median mental canal, although

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

Figure 4. Theropithecus sp. indet. KNM-KP 58577 male mandible with complete dentition, showing occlusal, left and right lateral views. Occlusal, buccal, and lingual views of KNMKP 59892 right P4; KNM-KP 32879 right M1 or 2; KNM-KP 59897 right M3; and KNM-KP 59888 right upper M, prob. M3.

there is a small round area that appears to be surface damage on the outer face of KNM-KP 58823 that could possibly be a median mental foramen. The mental ridges would have been very slight at the most. The superior transverse torus extends back the level of the distal part of P3, inferior to the P3 e P4 contact. The corpus is deep and increases in depth posteriorly. Although the gonial area is

absent, the inferior margin of the right corpus can be observed to curve inferiorly at its distal extreme suggesting the presence of a relatively expanded gonial region. The inferior part of the corpus is thick and robust and marked by distinct prominentia laterales. The extramolar sulcus is wide, and the anterior border of the buccinator line extends up to the M2.

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx Table 5 Molar areas in mm2 for extant and fossil Theropithecus.a

KNM - KP 58577 KNM - BC 2 KNM - BC 1657 WEE-VP-1/1 T. o. cf. darti - Woranso-Mille T. o. cf. darti - Hadar T. o. oswaldi T. o. leakeyi T. brumpti T. gelada a

M1

M2

M3

Total

M1/M2

M3/M2

66 87 83 68 76 87 121 152 107 73

116 116 118 96 114 133 189 251 173 110

134 174 159 116 154 185 274 385 286 152

315 377 359 280 344 405 584 788 565 335

0.57 0.75 0.70 0.71 0.67 0.66 0.64 0.61 0.62 0.66

1.16 1.50 1.35 1.21 1.35 1.40 1.45 1.54 1.66 1.38

Molar areas calculated as length x (mesial breadth þ distal breadth)/2.

In general, the preserved dentition is typical for colobines. The P3 of the female KNM-KP 29255 is small and lacks a mesiobuccal extension. It has a prominent protoconid and a relatively narrow talonid. The P4 has a large metaconid and a well-developed talonid that is separated from the trigonid by a distinct lingual notch. The molars are clearly colobine with tall cusps linked by broad and sharp lophids. The distal lophid of the M3 is only slightly narrower than the mesial one. The wear differential between the molars suggests a relatively long amount of time between the eruptions of the M1 to M2 to M3. Remarks: While this material is fairly fragmentary and difficult to assign to genus, it does preserve enough morphology to make a preliminary taxonomic assessment. The presence of a maxillary

11

sinus as preserved in KNM-KP 58701 distinguishes this species from all extant colobines, but is consistent with Cercopithecoides, Libypithecus, and Kuseracolobus (Rae, 2008; S. Frost pers. observation). The robust corpus with well-developed prominentia laterales is consistent with Cercopithecoides and Kuseracolobusas well as extant Procolobus verus. The posterior deepening of the mandible, however, aligns it with Kuseracolobus, and differentiates it from Cercopithecoides and Procolobus (Fig. 6). If the gonial region could be established as being expanded, this would also further distinguish it from Cercopithecoides. While most species of Cercopithecoides have a clear median mental foramen, this foramen is lacking in both C. meaveae and C. kerioensis, and therefore in this case does not help determine the genus (Frost and Delson, 2002; Leakey et al., 2003). Colobinae genus et species indeterminate (¼ or including cf. Cercopithecoides sp. Harris et al., 2003, in part. Colobinae gen. et sp. indet. A Harris et al., 2003.) Kanapoi specimens included: KNM-KP29307 right mandibular corpus with dp3 and I1eP4 in crypts; KNM-KP 30408 left mandibular corpus with M1, P3-4 erupting; KNM-KP 32803 right M1 or M2, probably M2; KNM-KP 32821 left M2; KNM-KP 36830 left M1 or M 2; KNM-KP 37382 right I2; KNM-KP 53081 left di2; KNM-KP 53100 left M1 or M 2, probably M2; KNM-KP 53145 left M1 or 2; KNM-KP 56982 male mandibular symphysis with right I1 and roots of left I1eP3, right I2; KNM-KP 59884 left mandibular corpus with P4-M1; KNM-KP 59901 left M1 or 2, probably M2

Figure 5. cf. Kuseracolobus sp. KNM-KP 29255 female mandible with left P3-M3 and right P3-M1, superior and lateral views; KNM-KP 58823 female mandibular symphysis with roots of left I1 to right C1, superior and lateral views; KNM-KP 58701 left maxillary fragment with M3?; KNM-KP 36967 left M3, occlusal, buccal, and lingual views; KNM-KP 59885 left I1, labial and lingual views; KNM-KP 31741 right Mx, occlusal and lingual views.

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S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

Table 6 Dental dimensions in millimeters for cf. Kuseracolobus sp.a Cat. No. KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP a

29255 29255 29255 29255 29255 31741 32870 36967 58701 58702 59885

Sex

Tooth

F F F F F

P3 P4 M1 M2 M3 MX P4 M3 M3 P3 I1

WS 5 14 10 8 7 6 8 1

Width

Other

Length

4.2 5.0 5.8 6.7 7.2 e 4.7 7.9 8.2 5.3 4.7

6.3 e 6.1 7.1 6.3 e e 6.5 e e 4.6

7.1 6.1 7.3 8.1 10.8 7.8 6.5 8.1 e 5.8 4.4

Dimensions same as for Table 4.

Description: This sample is a collection of isolated teeth and broken mandibular fragments that are all clearly colobine, but significantly larger than cf. Kuseracolobus sp. (Fig. 7; Table 7). They

overlap the size ranges for K. aramisi, C. meaveae, Cercopithecoides williamsi, and cf. Cercopithecoides sp. from Laetoli (Delson et al., 2000; Frost, 2001a; Frost and Delson, 2002; Harrison, 2011), but are on average smaller than the larger colobine from Laetoli (i.e. cf. Paracolobus sp. or cf. Rhinocolobus sp. [Leakey and Delson, 1987; Harrison, 2011]) and other Pliocene forms including K. hafu, Rhinocolobus turkanaensis, and Cercopithecoides kimeui (Delson et al., 2000; Frost et al., 2003; Hlusko, 2006). Remarks: It is possible that this series represents multiple species, but currently there is no morphological or size variation present to justify such an interpretation. Due to the fragmentary nature of the specimens, only a few aspects of mandibular morphology can be determined. The symphysis of KNM-KP 56982 is vertically oriented in lateral view and the superior transverse torus extends posteriorly to the level of the P3. Anteriorly, it appears to lack a median mental foramen. The corpus of KNM-KP 30408 is robust and lacks any evidence for a corpus fossa. The corpus is also not very deep superoinferiorly for its size, but given that it is from a subadult it is difficult to assess how much this would have changed on maturity. Dentally, this material is typical for the subfamily. The incisors are small in proportion to the molars. The upper incisor has a lingual cingulum and is not as spatulate as those of papionins. The lower incisors clearly possess lingual enamel. The male P3 has a relatively short mesiobuccal flange. The molars have high cusps separated by deep lingual notches and strong lophids with a low level of lateral flare. Little can be said about the taxonomic status of this material beyond the fact that it indicates the presence of a second species of colobine. 3. Discussion

Figure 6. Comparison of lateral views of colobine mandibles. cf. Kuseracolobus sp. (KNM-KP 29255); Kuseracolobus aramisi (NME ARA-VP-1/87 male, holotype);Cercopithecoides williamsi (KNM-ER 4420 male, image reversed). Scaled so that P3 e M3 length approximately equal.

The last review of Kanapoi non-human primates (Harris et al., 2003) recognized the presence of P. ado, cf. Theropithecus sp. indet., cf. Cercopithecoides sp. indet., and two different colobines of indeterminate affinities. With the accumulation of new material, we are able to clarify and expand the non-human primate fauna, even though the fragmentary nature of most of the material still leaves several tantalizing questions about the taxonomic identity and diversity of this community. As noted by Harris et al. (2003), the dominant member of the Kanapoi cercopithecid community is Parapapio cf. ado. The majority of specimens recovered from 2007 to 2015 reinforce this finding. However, the new sample highlights some of the differences in molar size and morphology between the Kanapoi and type series from Laetoli, something also pointed out by Harrison (2011) based on the earlier material. As a result, we are more tentative in assigning the Kanapoi Parapapio specimens to Pp. ado than were Harris et al. (2003). Re-examination of the fossils assigned by Harris et al. (2003) to cf. Cercopithecoides sp. reveals a closer morphological affinity of these specimens with Kuseracolobus than with Cercopithecoides, particularly the relatively deep mandible that deepens even further posteriorly. We retain the material listed as colobine A (and some cf. Cercopithecoides) in Harris et al. (2003) as a colobine of indeterminate genus and species. The single specimen allocated to Colobinae gen. et sp. indet. B, a mandible fragment with P3 (KNMKP 29308), is a perfect match for the mandible of Theropithecus sp. (KNM-KP 58577), and so we have transferred the specimen to Theropithecus sp. The new fossils collected from the 2007e2015 field seasons include KNM-KP 58577 and several isolated teeth that can be assigned to Theropithecus, confirming the presence of this genus, initially identified in the Kanapoi sample by Harris et al. (2003) based on a single broken molar. These fossils therefore establish

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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Figure 7. Colobinae genus et species indeterminate. KNM- KP 56982 male mandibular symphysis with right I1, superior and lateral views; KNM-KP 30408 left mandible with M1, P3erupting, superior and lateral views; KNM-KP 29307 right mandible with dp3, superior and lateral views; KNM-KP 59884 left P4-M1, occlusal and lingual views; KNM-KP 37382 right I2, labial and lingual views; KNM-KP 36830 left Mx, occlusal and lingual views; KNM-KP 53100 left Mx, occlusal and lingual views; KNM-KP 32803 rightMx, occlusal and lingual views; KNM-KP 32821 left M2, occlusal and lingual views; KNM-KP 59901 left Mx, occlusal and lingual views; KNM-KP 53081 left di2, labial and lingual views.

4

that the Kanapoi sample represents the first known appearance of Theropithecus at approximately 4.2 Ma. Pending the discovery of more complete cranial material, there is insufficient diagnostic

Table 7 Dental dimensions in millimeters for Colobinae gen. et sp. indet.a Cat. No. KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP KNM-KP a

Sex 29307 30408 32803 32821 36830 37382 53081 53100 53145 56982 59884 59884 59894 59901

M

M

Tooth

WS

Width

Other

Length

dp4 M1 MX MX MX I2 di2 MX MX I1 P4 M1 I2 MX

6 5 0 6 0

4.4 6.6 7.7 7.6 6.0 6.0 3.1 7.8 7.6 4.2 (5.4) 6.1 5.7 7.2

5.1 6.8 7.5 8.0 6.1 7.2 4.5 8.1 e e e 6.2 8.9 7.5

6.9 8.8 10.0 9.7 8.5 3.5 1.9 9.6 (8.5) e 7.4 8.5 2.9 9.2

Dimensions same as for Table 4.

3

4 9 9

morphology to erect a new species or otherwise determine the specific affinities of these fossils. However, the primitive dental morphology of the Kanapoi specimens is most consistent with a basal, stem form of Theropithecus. Significantly, the 2007e2015 expeditions yielded the remains of a small guenon, N. browni. It is the size of Miopithecus, but with lower, narrower molar crowns (Plavcan et al., 2019). Guenon remains are rare in the eastern African Pliocene record (Leakey, 1988; Jablonski and Frost, 2010) and the different cercopithecin genera can often be difficult to distinguish from each other. Most of the known fossils with diagnostic morphology are of Pleistocene age and resemble Chlorocebus aethiops or Ch. patas (Kalb et al., 1982; Frost, 2001b; Frost and Alemseged, 2007) which inhabit woodland/savanna habitats (Fleagle, 2013). The humerus tentatively allocated to N. browni suggests that this taxon was more arboreal than either Ch. aethiops or Ch. patas. Nanopithecus browni (Plavcan et al., in press) is also present from the lower Koobi Fora Formation (probably the Tulu Bor Member), where it is associated with a similar assemblage of cercopithecids as at Kanapoi: Theropithecus (both T. brumpti and T. o. darti), a papionin similar in size to Pp. cf. ado and a large colobine (Jablonski

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et al., 2008). The only other guenons from Koobi Fora are 6 specimens from the KBS and Okote (and possibly Upper Burgi) Members that are significantly larger than N. browni and close in size to Cercopithecus mitis (Jablonski et al., 2008). Other Pliocene and early Pliestocene localities with guenons include the Omo Usno and Shungura Formations (Units B-10, C-6/7, G-3, 9, 10, J-6) and thus range from 3.3 to 1.6 Ma (Eck, 1987). Size variation in this material suggests at least two taxa, one close in size to the larger Koobi Fora guenon and another intermediate between N. browni and the larger Koobi Fora species (Eck, 1987; Frost, 2001b). Together, Kanapoi, Koobi Fora and the Omo Valley occurrences suggest a persistent presence of the tribe in the Turkana basin over the last four million years, and as many as three distinct taxa present during Tulu Bor/ Shungura Member B times. The small guenon from Kanapoi extends this record nearly a million years, hints at a temporally deep diversity of guenons, and underscores the unique nature of past non-human primate communities in eastern Africa (Plavcan et al., 2019). One of the striking things about the Kanapoi cercopithecid assemblage is its diversity, with five species represented. Including the specimen of Galago sp. indet. described by Harris et al. (2003) and the hominin Australopithecus anamensis, there is a community of seven primate species. This primate diversity is remarkable compared to other early Pliocene sites, despite the fact that the sample size is relatively small. For example, there are only two cercopithecid species present at Aramis, Ethiopia (4.4 Ma), despite a sample of more than a thousand specimens (White et al., 2009). Woranso-Mille, Ethiopia (3.8e3.6 Ma) also has five cercopithecid

species, but again with a sample of well over one thousand fossils (Frost et al., 2014). It is also interesting that even though P. ado, or Parapapio cf. ado, are the most common primates at Laetoli and Kanapoi respectively, with the probable exception of Theropithecus, none of the other cercopithecids appear to be shared between these sites (Harrison, 2011). Another feature of the Kanapoi series is the presence of taxa that are rare at other sites. Cercopithecins are very rare in Pliocene assemblages, with a total sample size of approximately 10 specimens ethe vast majority of their record is Pleistocene (Jablonski and Frost, 2010). Additionally, galagids are also very rare in general, with the entire eastern African record including only a few specimens (Harrison, 2010). The rarity of the latter could be related to their small body size. Kanapoi is also notable for the abundant preservation of microfauna, which is also different from most other Plio-Pleistocene sites in the Turkana Basin and perhaps partially accounts for the occurrences of the new guenon species and Galago, and thus its relatively high primate diversity. The relative abundances of the different species of cercopithecid at Kanapoi are quite distinct from those at other Pliocene hominin sites (Fig. 8). The Kanapoi cercopithecid fauna is most similar to that of Allia Bay on the eastern side of Lake Turkana, which is only slightly younger in age than Kanapoi (3.9 Ma; Jablonski et al., 2008). Somewhat similar is Laetoli, Tanzania, in turn only slightly younger than Allia Bay (3.7 Ma; Harrison, 2011, Fig. 8). Kanapoi is more distinct from the Ethiopian sites in relative abundance of species. Compared to most early Pliocene sites, colobines are comparatively rare at Kanapoi, comprising approximately 18% of the assemblage. Only at the 3.8e3.6 Ma horizons at Woranso-Mille are they rarer,

Figure 8. Relative abundances of cercopithecid dental groupings (sensu Delson, 1973) from Kanapoi and contemporary eastern African sites. Sample size of specimens identifiable to group given in parentheses. Data sources: Lonyumun (Jablonski and Leakey, 2008); Laetoli (Harrison, 2011); Aramis (White et al., 2009); Asa Issie (White et al., 2006); WoransoMille (Frost et al., 2014).

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

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where colobines make up just 6% of the assemblage (Frost et al., 2014). At both Allia Bay and Laetoli, colobines make up about 30% (Jablonski et al., 2008; Harrison, 2011), and they are the most common cercopithecids at both Aramis and Asa Issie in the Middle Awash (Frost, 2001a; White et al., 2006, 2009). This may suggest that Kanapoi was somewhat more open in comparison to these other localities. Whereas Theropithecus is present, but rare, at both Kanapoi and Allia Bay, it is vastly predominant at Woranso-Mille (Frost et al., 2014). To date, all fossils of Theropithecus have been found to be grazers based on d13C from their enamel carbonates (Cerling et al., 2013; Levin et al., 2015) and microwear texture (Shapiro et al., 2016). Although Kanapoi Theropithecus have yet to be studied in this regard, the presence of Theropithecus suggests at least some C4 resources were accessible for primates. Alternatively, basal Theropithecus may have differed from later ones in dietary preference. Kanapoi also shares relatively few taxa with more recent Pliocene sites (Pp. cf. ado with Laetoli and Alia Bay; Theropithecus with Alia Bay, Woranso-Mille, and probably Laetoli; N. browni with the lower Koobi Fora Formation). It is unclear whether the variation in cercopithecid communities is due to differences in habitat, biogeography and provincialism, chronology, or some combination thereof. Nonetheless, the Kanapoi primate series bridges a key timespan filling the gap between the pre-Theropithecus Early Pliocene assemblages and Middle Pliocene and Pleistocene ones where Theropithcus greatly predominates (Frost, 2007a). Furthermore, the Kanapoi cercopithecids serve to highlight important regional variation among broadly contemporary sites and reminds us of the continued presence of paleontologically underrepresented, often small, taxa such as guenons and galagos. Acknowledgments We thank the West Turkana Paleo Project crew for their hard work and dedication. We thank the Government of Kenya, Turkana County, people of Kanapoi, and the directors, curators and staff of the National Museums of Kenya for permission to conduct fieldwork and for assistance. Fieldwork that yielded these fossils was supported by the Leakey Foundation and the Palaeontological Scientific Trust (PAST) of South Africa (to FKM), NSF BCS-1231749 (to CVW & FKM), NSF BCS-1231675 (to JMP& PSU), the Wenner Gren Foundation, University of Missouri Research Board and the West Turkana Paleo Project. Supplementary Online Material Supplementary online material to this article can be found online at https://doi.org/10.1016/j.jhevol.2019.102642. References Cerling, T.E., Chritz, K.L., Jablonski, N.G., Leakey, M.G., Manthi, F.K., 2013. Diet of Theropithecus from 4 to 1 Ma in Kenya. Proceedings of the National Academy of Science 110, 10507e10512. Delson, E., 1973. Fossil colobine monkeys of the circum-Mediterranean region and the evolutionary history of the Cercopithecidae (Primates, Mammalia). Ph.D. Dissertation. Columbia University. Delson, E., 1978. New fossil cercopithecids from East Africa. American Journal of Physical Anthropology 48; 389. Delson, E., 1984. Cercopithecid biochronology of the African Plio-Pleistocene: correlation among eastern and southern hominid-bearing localities. Courier Forschungsinstitut Senckenberg 69, 199e218. Delson, E., 1993. Theropithecus fossils from Africa and India and the taxonomy of the genus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 157e189. Delson, E., Dean, D., 1993. Are Papio baringensis R. Leakey, 1969, and P. quadratirostris Iwamoto, 1982, species of Papio or Theropithecus? In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 125e156.

15

Delson, E., Eck, G.G., Leakey, M.G., Jablonski, N.G., 1993. A partial catalogue of fossil remains of Theropithecus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 499e525. Delson, E., Terranova, C.J., Jungers, W.J., Sargis, E.J., Jablonski, N.G., Dechow, P.C., 2000. Body mass in Cercopithecidae (Primates, Mammalia): estimation and scaling in extinct and extant taxa. American Museum of Natural History Anthropological Papers 83, 1e159. Eck, G.G., 1987. Plio-Pleistocene specimens of Cercopithecus from the Shungura Formation, Southwestern Ethiopia. In: Coppens, Y., Howell, F.C. (Eds.), Les  istoce nes de la Basse Valle e de l'Omo (Ethiopie). faunes Plio-Ple Tome 3, Cerontologie, Travaux de copithecidae de la Formation de Shungura. Cahiers de Pale ontologie Est-Africaine. CNRS, Paris, pp. 142e146. Pale Eck, G.G., Jablonski, N.G., 1984. A reassessment of the taxonomic status and phyletic relationships of Papio baringensis and Papio quadratirostris (Primates: Cercopithecidae). American Journal of Physical Anthropology 65, 109e134. Eck, G.G., Jablonski, N.G., 1987. The skull of Theropithecus brumpti compared with those of other species of the genus Theropithecus. In: Coppens, Y., Howell, F.C.  istoce nes de la Basse Valle e de l'Omo (Ethiopie). (Eds.), Les faunes Plio-Ple Tome ontologie, 3, Cercopithecidae de la Formation de Shungura. Cahiers de Pale ontologie Est-Africaine. CNRS, Paris, pp. 11e122. Travaux de Pale Eisenhart, W.L., 1974. The fossil cercopithecoids of Makapansgat and Sterkfontein. B.A. Thesis, Harvard College. Feibel, C.S., 2003. Stratigraphy and depositional setting of the Pliocene Kanapoi Formation, Lower Kerio Valley, Kenya. Contributions in Science, Natural History Museum of Los Angeles County 468, 9e20. Fleagle, J.G., 2013. Primate Adaptation and Evolution. Academic Press, San Diego. Fleagle, J.G., McGraw, W.S., 2002. Skeletal and dental morphology of African papionins: Unmasking a cryptic clade. Journal of Human Evolution 42, 267e292. Freedman, L., 1957. The fossil Cercopithecoidea of South Africa. Ann. Transvaal Mus 23, 121e257. Frost, S.R., 2001a. New Early Pliocene Cercopithecidae from Aramis, Middle Awash Valley, Ethiopia. Am. Mus. Novit. 3350, 1e36. Frost, S.R., 2001b. Fossil Cercopithecidae from the Afar Depression, Ethiopia: species systematics and comparison to the Turkana Basin. Ph.D. Dissertation. City University of New York. Frost, S.R., 2007a. African Pliocene and Pleistocene cercopithecid evolution and global climatic change. In: Bobe, R., Alemseged, Z., Behrensmeyer, A.K. (Eds.), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht, pp. 51e76. Frost, S.R., 2007b. Fossil Cercopithecidae from the Dawaitoli Formation, Middle Awash, Ethiopia. American Journal of Physical Anthropology 134, 460e471. Frost, S.R., Alemseged, Z., 2007. Middle Pleistocene fossil Cercopithecidae from Asbole, Afar Region, Ethiopia. Journal of Human Evolution 53, 227e259. Frost, S.R., Delson, E., 2002. Fossil Cercopithecidae from the Hadar Formation and surrounding areas of the Afar Depression, Ethiopia. Journal of Human Evolution 43, 687e748. Frost, S.R., Plummer, T., Bishop, L.C., Ditchfield, P., Ferraro, J., Hicks, J., 2003. Partial cranium of Cercopithecoides kimeui from Rawi, Kenya. American Journal of Physical Anthropology 122, 191e199. Frost, S.R., Haile-Selassie, Y., Hlusko, L., 2009. Cercopithecidae. In: HaileSelassie, Y., WoldeGabriel, G. (Eds.), Ardipithecus kadabba:Late Miocene Evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley, pp. 135e158. Frost, S.R., Jablsonki, N.G., Haile-Selassie, Y., 2014. Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar,Ethiopia) and the origins of the Theropithecus oswaldi lineage. Journal of Human Evolution 76, 39e53. Gilbert, C.C., 2007. Craniomandibular morphology supporting the diphyletic origin of mangabeys and a new genus of the Cercocebus/Mandrillus clade, Procercocebus. Journal of Human Evolution 53, 69e102. Gilbert, C.C., 2013. Cladistic analysis of extant and fossil African papionins using craniodental data. Journal of Human Evolution 64, 399e433. Gilbert, C.C., Goble, E.D., Kingston, J.D., Hill, A., 2011. Partial skeleton of Theropithecus brumpti (Primates, Cercopithecidae) from the Chemeron Formation of the Tugen Hills, Kenya. Journal of Human Evolution 61, 347e362. Gilbert, C.C., Bibi, F., Hill, A., Beech, M.J., 2014. Early guenon from the late Miocene Baynunah Formation, Abu Dhabi, with implications for cercopithecoid biogeography and evolution. Proceedings of the National Academy of Science 111, 10119e10124. Guthrie, E.H., 2011. Functional Morphology of the Postcrainum of Theropithecus brumpti (Primates: Cercopithecidae). PhD Thesis. University of Oregon. Harris, J.M., Brown, F.H., Leakey, M.G., 1988. Stratigraphy and paleontology of Pliocene and Pleistocene localities West of Lake Turkana, Kenya. Contributions in Science, Natural History Museum of Los Angeles County 399, 1e128. Harris, J.M., Leakey, M.G., Cerling, T.E., 2003. Early Pliocene tetrapod remains from Kanapoi, Lake Turkana Basin, Kenya. Contributions in Science, Natural History Museum of Los Angeles County 468, 39e112. Harrison, T., 2011. Cercopithecids (Cercopithecidae, Primates). In: Harrison, T. (Ed.), Paleontology and Geology of Laetoli: Human Evolution in Context, Fossil Hominins and the Associated Fauna, vol. 2. Springer, Dordrecht, pp. 83e139. Hlusko, L.J., 2006. A new large Pliocene colobine species (Mammalia: Primates) from Asa Issie, Ethiopia. Geobios 39, 57e69. Leakey, M.G., 1993a. Evolution of Theropithecus in the Turkana Basin. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 85e123.

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642

16

S.R. Frost et al. / Journal of Human Evolution xxx (xxxx) xxx

Jablonski, N.G., 1993. The phylogeny of Theropithecus. In: Jablonski, N.G. (Ed.), Theropithecus: the Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 209e224. Jablonski, N.G., 2002. Fossil Old World monkeys: the late Neogene radiation. In: Hartwig, W.C. (Ed.), The Primate Fossil Record. Cambridge University Press, Cambridge, pp. 255e299. n, M., 2008. Systematic paleontology of the cerJablonski, N.G., Leakey, M.G., Anto copithecines. In: Jablonski, N.G., Leakey, M.G. (Eds.), Koobi Fora Research Project, The Fossil Monkeys, vol. 6. California Academy of Sciences, San Francisco, pp. 103e300. Jablonski, N.G., Frost, S.R., 2010. Chapter 31. Cercopithecoidea. In: Werdelin, L., Sanders, W.J. (Eds.), The Cenozoic Mammals of Africa. University of California Press, Oakland, pp. 393e428. Kalb, J.E., Jaeger, M., Jolly, C.J., Kana, B., 1982. Preliminary geology, palaeontology and paleoecology of a Sangoan site at Andalee, Middle Awash Valley, Ethiopia. Journal of Archaeological Science 9, 349e363. Leakey, R.E.F., 1969. New Cercopithecidae from the Chemeron Beds of Lake Baringo, Kenya. Fossil Vertebrates of Africa 1, 53e69. Leakey, M.G., 1988. Fossil evidence for the evolution of the guenons. In: Gautier Hion, A., Bourliere, F., Gautier, J.-P. (Eds.), A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge University Press, Cambridge, pp. 7e12. Leakey, M.G., 1993b. Evolution of Theropithecus in the Turkana Basin. In: Jablonski, N.G. (Ed.), Theropithecus:The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 85e123. Leakey, M.G., Delson, E., 1987. Fossil Cercopithecidae from the Laetolil Beds, Tanzania. In: Leakey, M.D., Harris, J.M. (Eds.), The Pliocene Site of Laetoli, Northern Tanzania. Oxford University Press, Oxford, pp. 91e107. Leakey, M.G., Leakey, R.E.F., 1976. Further Cercopithecinae (Mammalia, Primates) from the Plio/Pleistocene of East Africa. In: Savage, R.J.G., Coryndon, S.C. (Eds.), Fossil Vertebrates of Africa, vol. 4. Academic Press, London, pp. 120e146. Leakey, M.G., Feibel, C.S., McDougall, I., Walker, A., 1995. A new four millionyear-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376, 565e571. Leakey, M.G., Feibel, C.S., McDougall, I., Ward, C., Walker, A., 1998. New specimens and confirmation of an early age for Australopithecus anamensis. Nature 393, 62e66. Leakey, M.G., Teaford, M.F., Ward, C.V., 2003. Cercopithecidae from Lothagam. In: Leakey, M.G., Harris, J.M. (Eds.), Lothagam: the Dawn of Humanity in Eastern Africa. Columbia University Press, New York, pp. 201e248. Levin, N.E., Haile-Selassie, Y., Frost, S.R., Saylor, B.Z., 2015. Dietary change among hominins and cercopithecids in Ethiopia during the early Pliocene. Proceedings of the National Academy of Science 112, 12304e12309. McKee, J.K., Kuykendall, K.L., 2016. The Dart deposits of the Buxton Limeworks, Tuang, South Africa, and the context of the taung Australopithecus fossil. Journal of Vertebrate Paleontology. https://doi.org/10.1080/02724634.2015.1054937. Patterson, B., 1968. The extinct baboon, Parapapio jonesi, in the Early Pleistocene of northwest Kenya. Breviora 282, 1e4. Perelman, P., Johnson, W.E., Roos, C., Seu anez, H.N., Horvath, J.E., Moreira, M.A.M., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M.P.C., Silva, A.,

O'Brien, S.J., Pecon-Slattery, J., 2011. A molecular phylogeny of living primates. PLOS Genetics 7 e1001342. Plavcan, J.M., Ward, C.V., Kay, R.F., Manthi, F.K., 2019. A diminutive guenon from Kanapoi, West Turkana, Kenya. Journal of Human Evolution in press. Raaum, R.L., Sterner, K.N., Noviello, C.M., Stewart, C.-B., Disotell, T.R., 2005. Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. Journal of Human Evolution 48, 237e257. Rae, T.C., 2008. Paranasal pneumatization in extant and fossil Cercopithecoidea. Journal of Human Evolution 54, 279e286. Semaw, S., Simpson, S.W., Quade, J., Renne, P.R., Butler, R.F., McIntosh, W.C., Levin, N., Dominiguez-Rodrigo, M., Rogers, M.J., 2005. Early Pliocene hominids from Gona, Ethiopia. Nature 433, 301e305. Shapiro, A.E., Venkataraman, V.V., Nguyen, N., Fashing, P.J., 2016. Dietary ecology of fossil Theropithecus: inferences from dental microwear textures of extant geladas from ecologically diverse sites. Journal of Human Evolution 99, 1e9. Springer, M.S., Meredith, R.W., Gatesy, J., Emerling, C.A., Park, J., Rabosky, D.L., Stadler, T., Steiner, C., Ryder, O.A., Janecka, J.E., Fisher, C.A., Murphy, W.J., 2012. Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLOS One 7 e49521. Szalay, F.S., Delson, E., 1979. Evolutionary History of the Primates. Academic Press, New York. Tosi, A.J., Melnick, D.J., Disotell, T.R., 2004. Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (Tribe Cercopithecini). Journal of Human Evolution 46, 223e237. Tosi, A.J., Detwiler, K.M., Disotell, T.R., 2005. X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini). Molecular Phylogenetics and Evolution 36, 58e66. Ward, C.V., Leakey, M.G., Walker, A., 2001. Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. Journal of Human Evolution 41, 255e368. Ward, C.V., Manthi, F.K., Plavcan, J.M., 2013. New fossils of Australopithecus anamensis from Kanapoi, West Turkana, Kenya (2003-2008). Journal of Human Evolution 65, 501e524. Ward, C.V., Plavcan, J.M., Manthi, F.K., 2019. New fossils of Australopithecus anamensis from Kanapoi, West Turkana, Kenya (2012e2015). Journal of Human Evolution in press. White, T.D., WoldeGabriel, G., Asfaw, B., Ambrose, S., Beyene, Y., Bernor, R.L., Boisserie, J.C., Currie, B., Gilbert, H., Haile-Selassie, Y., Hart, W.K., Hlusko, L.J., Howell, F.C., Kono, R., Lehmann, T., Louchart, A., Lovejoy, C.O., Renne, P., Saegusa, H., Vrba, E.S., Wesselman, H., Suwa, G., 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883e889. White, T.D., Ambrose, S.H., Suwa, G., Su, D.F., DeGusta, D., Bernor, R.L., Boisserie, J.-R., Brunet, M., Delson, E., Frost, S.R., Garcia, N., Giaourtsakis, I.X., Haile-Selassie, Y., Howell, F.C., Lehmann, T., Likius, A., Pehlevan, C., Saegusa, H., Semprebon, G., Teaford, M.F., Vrba, E., 2009. Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 87e93. Xing, J., Wang, H., Zhang, Z., Ray, D.A., Tosi, A.J., Disotell, T.R., Batzer, M.A., 2007. A mobile element-based evolutionary history of guenons (Tribe Cercopithecini). BMC Biology 2007(5), 5.

Please cite this article as: Frost, S.R et al., Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007e2015), Journal of Human Evolution, https://doi.org/10.1016/j.jhevol.2019.102642