2017 Volume 125 Issue 2 Pages 45-51
The African primate fossil record is very poor between the mid-Middle and mid-Late Miocene. Nakali (~10–9.8 Ma) is one of the rare African localities that have yielded primate fossils from this period, including a new genus of great ape, Nakalipithecus nakayamai, and another large-bodied hominoid species. The Nakali primate fauna also includes small-bodied ‘apes’ and Old World monkeys (mostly colobines). In this article, we describe a new specimen of a small-bodied ‘ape’ discovered from Nakali, which is assigned to nyanzapithecines. Nyanzapithecines are characterized by their derived dental morphology, and the previously known nyanzapithecines range in chronological age between the Late Oligocene and early Middle Miocene (~25–13.7 Ma). The new nyanzapithecine specimen from Nakali is therefore the latest occurrence of this group in the African fossil record, extending its chronological range by almost 4 million years younger.
The nyanzapithecines are a highly specialized group of small to medium-sized non-cercopithecoid catarrhines in the African Oligo-Miocene. At present, there are six genera (Nyanzapithecus, Mabokopithecus, Rangwapithecus, Turkanapithecus, Xenopithecus, Rukwapithecus) with nine species recognized in the nyanzapithecines (Harrison, 2010a; Pickford et al., 2010; Stevens et al., 2013) (Figure 1 and Figure 2).
Location of Nakali and other African Oligocene/Miocene localities mentioned in the text.
Chronological distribution of the nyanzapithecines and Oreopithecus.
Rukwapithecus fleaglei was recently discovered from Nsungwe 2B, a Late Oligocene locality in Tanzania (~25 Ma) (Stevens et al., 2013). Rangwapithecus gordoni and Xenopithecus koruensis are known from the Early Miocene of western Kenya (Songhor and Koru, respectively) (Hopwood, 1933; Andrews, 1974, 1978; Cote, 2004; Hill et al., 2013), while Turkanapithecus kalakolensis was reported from the Early Miocene of Kalodirr in northern Kenya (Leakey and Leakey, 1986). Pickford et al. (2010) described a new species of Turkanapithecus (T. rusingensis), though the present hypodigm is comprised of several fragmentary specimens from various localities (Rusinga/Mfwangano, Songhor, Napak, and Kipsaraman). Apart from East Africa, Harrison (2010a) suggests that the fragmentary large upper molar from Ryskop, South Africa (~18 Ma) (Senut et al., 1997) may belong to the nyanzapithecines. If this is the case, the nyanzapithecines had obtained a wide distribution from east to southern Africa by ~18 Ma. The Ryskop material is, however, represented by one half of an upper molar crown only.
More derived taxa such as Nyanzapithecus and Mabokopithecus are mainly known from western Kenya with N. vancouveringorum mainly from the Early Miocene of Rusinga/Mfwangano (~18 Ma) and N. pickford and Mabokopithecus clarki from the early Middle Miocene of Maboko (~15 Ma) (Koenigswald, 1969; Harrison, 1986, 2002, 2010a). N. cf. pickfordi was also reported from the early Middle Miocene Muruyur Formation (~14.5 Ma) in the Tugen Hills (Kelley et al., 2002; Pickford and Kunimatsu, 2005). On the other hand, N. harrisoni was described from material discovered from the early Middle Miocene of Nachola (= Baragoi) (~15 Ma), on the eastern flank of the Rift Valley in northern Kenya (Kunimatsu, 1992, 1997; Sawada et al., 2006). New specimens from Maboko might necessitate the taxonomic revision of Nyanzapithecus and Mabokopithecus (Benefit et al., 1998), but detailed description of them has yet to be done.
A few isolated teeth from the mid-Middle Miocene of Fort Ternan and Kapsibor (~13.7 Ma) are considered to belong to a large species of the nyanzapithecines (Harrison, 1986, 1992, 2010a). They very likely represent a new species, but the presently available material is so fragmentary that they are retained as nyanzapithecine indet. (Harrison, 2010a). This is the latest occurrence of the nyanzapithecines in the fossil record so far known.
Nakali was briefly investigated by previous expeditions in the 1960s and 1970s (Aguirre and Leakey, 1974; Benefit and Pickford, 1986; Hill, 1994; Gundling and Hill, 2000). The Kenya–Japan Joint Expedition to Nakali started new fieldwork in 2002 (Nakatsukasa, 2009). Since then, thousands of fossils including vertebrates and plant leaves have been recovered through surface collection and excavation (Kunimatsu et al., 2007, 2016; Nakatsukasa, 2009; Nakatsukasa et al., 2010; Handa et al., 2015; Tsubamoto et al., 2015).
During fieldwork in the early Late Miocene locality at Nakali, an isolated left P3 (KNM-NA 55061: Figure 3) of a small non-cercopithecoid catarrhine was discovered through surface collection. Although this is a single, isolated tooth, its unique crown morphology strongly suggests that it belongs to the nyanzapithecines, which are previously known from Early to early Middle Miocene sites in Kenya and from an Oligocene site in Tanzania (Harrison, 1986, 2002, 2010a; Kunimatsu, 1992, 1997; Kelley et al., 2002; Pickford and Kunimatsu, 2005; Stevens et al., 2013). The discovery of the Nakali specimen extends the younger limit of the chronological range of the nyanzapithecines by almost 4 million years from ~13.7 Ma to 9.9–9.8 Ma (Kunimatsu et al., 2007).
(a) Left P3s of nyanzapithecine gen. et sp. indet. from Nakali (a1: KNM-NA 55061) and Nyanzapithecus vancouverngorum from Rusinga, Kenya (a2: KNM-RU 2058) (occlusal, stereo). (b, c) Mesial and distal views of the same specimens of nyanzapithecine gen. et sp. indet. (left) and N. vancouveringorum (right). Scale = 5 mm.
The nyanzapithecine specimen described in this article (KNM-NA 55061) was collected on the surface at Site NA38, where an upper molar of Nakalipithecus nakayamai had been discovered previously (Kunimatsu et al., 2007). The sediments exposed at Site NA38 belong to the Upper Member of the Nakali Formation (Kunimatsu et al., 2007). Site NA38 is located several hundred meters south of Site NA39, where the majority of the N. nakayamai specimens were excavated (Kunimatsu et al., 2007; Nakatsukasa, 2009). The magnetostratigraphic reversed polarity zone in the Upper Member is correlated to Chron C5n.1n (9.88–9.74 Ma) on the basis of the 40Ar–39Ar ages. Because of the rapid sediment accumulation, the age of the fossils is estimated to be 9.9–9.8 Ma (Kunimatsu et al., 2007; Sakai et al., 2013).
Order Primates Linnaeus, 1758
Suborder Anthropoidea Mivart, 1864
Infraorder Catarrhini Geoffroy, 1812
Superfamily incertae sedis
Nyanzapithecine gen. et sp. indet.
KNM-NA 55061 is a left upper P3 with the roots missing. The crown is slightly worn, showing small lakes of dentine exposed on the apices of the two main cusps. The occlusal outline of the crown is ovoid with the buccal moiety being only slightly longer than the lingual moiety, suggesting that this tooth is a P3 rather than P4. The lingual basal flare is moderately developed, while the buccal face is nearly vertical. The cusps are high and inflated. The protocone is very well developed, being only slightly lower than the paracone. There is not a lingual cingulum, though a small pit is distinctly incised on the lingual aspect of the crown near the base of the postprotocrista and there are a few short, vertical grooves on the mesial aspect of the protocone. The preparacrista is low and rounded, running mesially from the apex to end at a tiny style. The postparacrista is better developed than the preparacrista, and runs distally to end at a tiny style. There is a short mesiolingual ridge, which comes out from the paracone apex to meet the preprotocrista. Distal to the junction between these two ridges lies a distinct longitudinal groove, which separates the bases of the protocone and paracone. The protocone has two ridges, pre- and postprotocrista. The preprotocrista runs mesiobuccally, and becomes inflated after the junction with the mesiolingual ridge from the paracone. The preprotocrista further runs mesiobuccally and meets the mesial marginal ridge at a point very close to the base of the preparacrista. Consequently, the mesial cingulum and fovea are quite strongly restricted to be a small pit. The postprotocrista is as well developed as the postparacrista, and runs distally and slightly buccally to meet the well-defined distal marginal ridge. The lingual cingulum is restricted to a prominent but very short ledge at the distal end of the lingual aspect. In buccal view, the buccal cingulum is absent except for the short ledges at the mesial and distal ends of the buccal face.
The newly discovered Nakaki specimen (KNM-NA 55061) is similar to previously known nyanzapithecines, especially the genus Nyanzapithecus, in having a relatively elongated crown, high and inflated cusps positioned closely to each other, a well-developed protocone that is only slightly smaller and lower than the paracone, a prominent distal cingulum which is elevated high from the cervix. On the other hand, the Nakali specimen differs from the upper P3 of Nyanzapithecus and other nyanzapithecines in the course of the preprotocrista (Figure 3). In the Nakali specimen, the preprotocrista is much more buccally directed to meet the mesial marginal ridge at a point very close to the base of the preparacrista. Consequently, the mesial fovea and cingulum are extremely restricted buccolingually to be a distinct pit at the buccal end of the mesial margin. The Nakali specimen further differs from the other nyanzapithecines in its smaller size and having a relatively more elongated crown (Table 1). In addition, it is different from N. vancouveringorum and R. gordoni in lacking a well-developed, continuous lingual cingulum (Harrison, 1986).
These morphological differences suggest that the Nakali specimen very likely belongs to a new species of the nyanzapithecines, more closely related to Nyanzapithecus than to Rangwapithecus or Turkanapithecus. As far as the premolar morphology is concerned, it may be a more specialized member of the lineage, considering the more elongated crown and the unique ridge pattern. However, as there is only a single upper premolar at present, we refrain from creating a new taxon and prefer to leave it as nyanzapithecine gen. et sp. indet.
Among the previously known samples, the few isolated teeth from Fort Ternan and Kapsibor are the latest occurrence of the nyanzapithecines. The age of Fort Ternan is dated to 13.7 ± 0.3 Ma (Pickford et al., 2006), and Kapsibor is at the same stratigraphic level as Fort Ternan (Pickford, 1986). The Fort Ternan and Kapsibor materials are only poorly represented by a left M1 (KNM-FT 36), a right P4 (KNM-FT 37), a right M3 (KNM-FT 38), a left M2 (KNM-KR 9755), and possibly a left upper canine (KNM-FT 41) (Harrison, 1986, 1992, 2010a). Compared to Nyanzapithecus, the Fort Ternan/Kapsibor nyanzapithecine is much larger, in contrast to the Nakali nyanzapithecine, which is smaller than other nyanzapithecines (Table 1). Although the Nakali P3 (KNM-NA 55061) is similar to the Fort Ternan P4 (KNM-FT 37) in having the protocone and paracone high and inflated, and positioned close to each other, there are considerable differences even if we take into account the fact that their tooth types are slightly different (P3 and P4). The Nakali P3 has more prominent occlusal ridges, while they are only poorly developed in the Fort Ternan P4. In the latter, the mesial cingulum is a well-developed shelf-like structure, continuous all along the mesial margin of the crown, in strong contrast to the extremely restricted condition in the former. The distal transverse crest is not developed in the Nakali P3 so that the longitudinal groove between the main cusps runs distally up to the distal cingulum. On the other hand, a very low and thick transverse crest confines the central fovea distally and clearly separates it from the distal fovea and cingulum in the Fort Ternan P4. Concerning the upper premolar size and morphology, the Nakali nyanzapithecine is more similar to Nyanzapithecus than to the Fort Ternan/Kapsibor nyanzapithecine.
In the collection at the National Museums of Kenya, there is an isolated upper premolar of a small non-cercopithecoid catarrhine recovered from the Ngorora Formation, Tugen Hills (Pickford, 1978; Andrews, 1980; Harrison, 1982), which is slightly older (~12.5 Ma) than Nakali, but is younger than the majority of the African Miocene localities that have yielded small non-cercopithecoid catarrhines. As the specimen (KNM-BN 993) is a right upper P4 crown (Harrison, 1982), the tooth type is not completely identical with the Nakali P3 described in this article. However, comparing the size and general morphology with the latter, the crown of KNM-BN 993 is smaller (MD: 3.6 mm, BL: 5.5 mm, MD × BL: 19.8 mm2) and relatively much broader (MD/BL: 65.5%) with much more extensive lingual basal flare (Table 1). In addition, the main cusps are not inflated and more heteromorphic. In sum, the Ngorora P4 (KNM-BN 993) neither matches the Nakali P3 (KNM-NA 55061) nor belongs to the nyanzapithecines. Rossie and Hill (2005) reported several new catarrhine specimens from the Ngorora Formation, representing at least two species, one of which can be recognized to be “a new species of small-bodied ape bearing some resemblance to Simiolus enjiessi and Kalepithecus songhorensis.” Although detailed description of these new fossils has yet to be done, it appears unlikely that they belong to the nyanzapithecines if they resemble S. enjiessi and K. songhorensis from the Early Miocene of East Africa (Harrison, 1986, 1988, 2002, 2010a; Leakey and Leakey, 1987).
The phylogenetic relationship between the African nyanzapithecines and European Oreopithecus has been debated (Benefit and McCrossin, 1997, 2001; Harrison and Rook, 1997; Harrison, 2002, 2010a). Based on the remarkable similarities in peculiar dental morphology between these two groups, Harrison (1986) initially suggested that the nyanzapithecines were ancestral to Oreopithecus known from the Late Miocene of Italy, assigning them in the Oreopithecidae. Later, he changed the interpretation, suggesting that Oreopithecus was a specialized dryopithecine and was not closely related to the African nyanzapithecines (Harrison and Rook, 1997). Oreopithecus shares many suspensory adaptations with the extant hominoids and European dryopithecines (Harrison and Rook, 1997), which are not observed in the African nyanzapithecines (Harrison, 1982, 2002; Leakey and Leakey, 1986; Leakey et al., 1988; McCrossin, 1992; Rose, 1993, 1994). If the postcranial similarities are true synapomorphies among Oreopithecus, extant hominoids, and European dryopithecines, the peculiar dental morphology observed in Oreopithecus and nyanzapithecines is a result of parallel evolution (Harrison and Rook, 1997). On the other hand, if the peculiar dental morphology reflects the close phylogenetic relationship between Oreopithecus and nyanzapithecines, it may suggest parallelism in postcrania during the hominoid evolution. The situation is similar to the Sivapithecus problem, in which the craniodental evidence strongly suggests a close phylogenetic relationship between Sivapithecus and extant orangutans, while the postcranial specimens provide contradictory evidence (Pilbeam, 1982; Ward and Brown, 1986; Brown and Ward, 1988; Pilbeam et al., 1990; Madar et al., 2002). With only an isolated P3 specimen on hand, evaluation of the phylogenetic relationship between Oreopithecus and nyanzapithecines is beyond the scope of the present study. However, it is interesting that this discovery of the nyanzapithecine specimen from Nakali narrows the gap between the temporal distributions of Oreopithecus in the Late Miocene of Europe and the nyanzapithecines in the Early to Middle Miocene of Africa (Figure 2).
Line drawings of left P3s of nyanzapithecine sp. indet from Nakali (KNM-NA 55061; right column) and Nyanzapithecus vancouveringorum from Rusinga, Kenya (KNM-RU 2058; left column). Upper row: occlusal view. Lower row: mesial view. Scale = 5 mm. The inset shows upper premolar traits.
The presently available nyanzapithecine material from Nakali is quite limited, but it extends the chronological distribution of the nyanzapithecines by almost 4 million years from the early Middle to the early Late Miocene (Harrison, 1986, 2010a; Kunimatsu, 1992, 1997). To date, no nyanzapithecine or other non-cercopithecoid small catarrhines have been discovered from Africa after the age of Nakali. From the Nakali Formation, a considerable number of cercopithecoid fossils have been recovered. Many of them are a small (~4 kg) colobine Microcolobus (Kunimatsu et al., 2007; Nakatsukasa et al., 2010). This is not a dedicated folivorous primate, unlike living colobines (Benefit, 2000), and could have been a potential competitor for sympatric, small, non-cercopithecoid catarrhines. Climatic change and fluctuation in the Late Miocene caused a transition from C3 to C4 environment in Africa during 10–7 Ma (Cerling et al., 1997; Uno et al., 2011). This environmental change shrunk and fragmented forested habitats for primates, leading to extinction of local populations. At the same time, it might have escalated competition between small non-cercopithecoid catarrhines and similar-sized cercopithecoids (Simons, 1970; Andrews, 1981). However, it is still premature to conclude that the cercopithecoids eventually replaced the non-cercopithecoid catarrhines via direct competition (Harrison, 2010b; Nakatsukasa and Kunimatsu, 2012). Revealing the aspects of their extinction would shed light on the decline of the diversity of African hominoids and the origins of living African apes and humans.
We thank the NACOSTI of Kenya for research permission, the staff of the National Museums of Kenya for their assistance, B. Onyango, T. Mukhuyu, W. Mangao, P. Nzube, D. Mutinda, N. Kanyenze, K. Munguti, S. Oginga, E. Afwande, S. Yatur, M, Nzube, J. Mbithi, B. Okot, J. Kamula, and V. Kennedy for their support during fieldwork, and H. Ishida for logistic support. We are grateful to A. Mariba, D. Arupe, and other Baringo County officers, and the people of Akwichatis and Nasorot. We also appreciate the assistance from the JSPS Nairobi Research Station during our research in Kenya. We thank the Primate Research Institute, Kyoto University, for the permission to access to the primate skeletal and cast collections through the Cooperative Research Program. We thank Terry Harrison and an anonymous reviewer for their useful comments. This expedition and comparative studies were funded by grants from the JSPS and MEXT (KAKENHI #18255006, #22255006, #25257408, #24570254, #16H02757).