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Home , Cercopithecini, Cercopithecoides, Dinopithecus, Gorgopithecus, Ileret, Koobi Fora

Kroeber Anthropological Society Papers, Nos. 71-72, 1990

Diet, Species Diversity and Distribution of African Brenda R. Benefit and Monte L. McCrossin

Based on measurements ofmolarfeatures shown to befunctionally correlated with the proportions of fruits and leaves in the diets ofextant monkeys, Plio-Pleistocenepapionin baboonsfrom southern are shown to have included more herbaceous resources in their diets and to have exploited more open country habitats than did the highlyfrugivorousforest dwelling eastern African species. The diets ofall species offossil are reconstructed to have included morefruits than the diets ofextant Theropithecus . , T. quadratirostris and T. darti have greater capacitiesfor shearing, thinner enamel and less emphases on the transverse component ofmastication than T. oswaldi, and are therefore interpreted to have consumed leaves rather than grass. Since these species are more ancient than the grass-eating, more open country dwelling T. oswaldi, the origin ofthe genus Thero- pithecus is attributed tofolivorous adaptations by largepapionins inforest environments rather than to savannah adapted grass-eaters. Reconstructions ofdiet and habitat are used to explain differences in the relative abundance and diversity offossil baboons in eastern andsouthern Africa.

INTRODUCTION abundance between eastern and southern Africa is observed for members of the Papionina (Papio, Interpretations of the dietary habits of fossil Cercocebus, Parapapio, Gorgopithecus, and Old World monkeys have been based largely on ). [We follow Szalay and Delson analogies to extant with lophodont teeth (1979) in recognizing two tribes of cercopithe- (Jolly 1970; Napier 1970; Delson 1975; Andrews cines, Cercopithecini and , and three 1981; Andrews and Aiello 1984; Temerin and subtribes of the Papionini: Theropithecina (gela- Cant 1983). With the exception of Jolly's (1972) das, fossil and modern), Macacina (, study of , such inter- fossil and modern) and Papionina (baboons, pretations have focused on the origins of drills, and mangabeys, fossil and mod- Cercopithecoidea with relatively litde attention ern)]. Eighty-four percent of the fossil monkeys given to more recent dietary diversification widtin in southern Africa are papioninans (Freedman the superfamily. 1976), while only 10% of those in eastern Africa In this study the dietary habits of Plio- are members of this subtribe. In southern Africa cercopithecine monkeys from fossil at least nine species ofpapioninan monkeys have sites in eastern and southern Africa are recon- been recovered, but only three species are known structed on the basis of dental features shown to to have occurred in eastern Africa (although the be functionally correlated to diet among extant actual number is presendy indeterminable due to cercopithecoids (Kay 1977, 1978, 1981, 1984; the fragmentary and incomplete nature ofthe ma- Kay and Covert 1984; Kay and Hylander 1978; terial). Reconstructions of the dietary habits of Benefit 1987). A major concern ofthe study is to these extinct , in combination with infor- better understand the differences in the patterns of mation about the habitats in which they lived and species diversity and the relative abundance of studies of food consumption and habitat use by cercopithecine monkeys which existed in the eas- living mammals, are used to describe a new sce- tern and southern regions of the African continent nario about the , diversity, distribution during the Plio-Pleistocene. and relative abundance of fossil Theropithecus In cave deposits of southern Africa Thero- and other baboons during the Plio-Pleistocene. pithecus is rare, comprising 7% of the total cercopithecoid fauna collected prior to 1976 (Freedman 1976). In contrast, 84% of the mon- MATERIALS AND METHODS keys collected at the Omo and 85% of those collected at , both in eastern Africa, Fossil cercopithecine monkeys were sampled prior to the same date belong to the genus Thero- from Plio-Pleistocene deposits in southern Africa pithecus (Eck 1976; Leakey 1976). In addition, (Sterkfontein Member 4, Kromdraai Members A Theropithecus is more diverse in deposits from and B, Taung, and Swardcrans Member 1) and eastem Africa, with five species occurring in the eastern Africa ( and Olduvai, ; fossil deposits, as opposed to only two in south- and Koobi Fora, -- Areas 1- ern Africa. The opposite pattem ofdiversity and 203; Omo, -- Usno Formation, Shun- 78 gura Formation Members B- Table 1. Numbers of fossil cercopithecine molars measured. H, and Kalam Area). Spe- L = Lower, U = Upper. cies sampled are listed by deposit in Table 1. [A complete list of specimens LM1 LM2 LM3 UMI UM2 UM3 sampled is given in Benefit Cercocebus sp., KOOBI FORA 5 T7 1T 5 (1987).] Taxonomic identi- fications for the southern Cercocebus ado, OLDUVAI 1 1 1 African are largely Parapapio ado, LAETOLI 5 8 10 4 8 5 based on Freedman (1957, 1961a, 1961b, 1965, Parapapio jonesi, KANAPOI 1 1 1 1976), Freedman and Brain Parapapio sp., KOOBI FORA 2 3 6 2 2 2 (1972), Freedman and Stenhouse (1972), Maier Papionini indet, BARINGO 1 (1971a, 1971b) and Eisen- Papio sp., OLDUVAI 2 3 1 2 hart (1974). Identification Theropithecus oswaldi, of fossil monkeys from KOOBI FORA & (combined) 13 61 40 12 44 17 eastern Africa are based on AREA 1 (1.5-1.6 my) 3 1 descriptions by R.E. Leakey AREA 8 (1.5-1.6 my) 8 1 2 8 1 AREA 103 (1.6-1.7 my) 5 1 1 (1969), Jolly (1970, 1972), AREA 10 (1.7-1.9 my) 3 1 1 1 M.G. Leakey (1976, 1982), AREA 123 (1.7-1.9 my) 3 5 Leakey and Leakey (1973a, AREA 130 (1.8-1.9 my) 3 8 5 1 4 2 Eck AREA 104 (1.7-2.0 my) 2 4 3 1 1 1973b, 1976), (1977), AREA 106 (2.0 my) 1 Eck and Howell (1982), AREA 116 (2.0 my) 1 2 1 1 1 Eck and Jablonski (1984) and Delson OMO SHUNGURA FORMATION and Leakey Member G 4 (1987). Member H 1 Biostratigraphic dating of Kalam area (Members J-L) 1 the southern African cave deposits indicates that Ma- OLDUVAI 2 11 12 4 8 8 kapansgat is the oldest site OLORGESAILIE 39 35 23 35 25 14 at approximately 3.0 million Theropithecus brumpti years (my), followed by KOOBI FORA/TULU BOR Sterkfontein (3.2-2.5 my AREA 117 &204 (3.3 my) 4 2 6 1 2 3 and 1.75-1.4 my), Krom- AREA 203 (3.3 my) 2 6 6 1 draai (2.7-1.8 my), Taung OMO, SHUNGURA FORMATION (2.3-1.0 my) and Swart- Member C krans (1.8-1.6 my and Member D 2 1.25-0.9 my) (Vrba 1982). Theropithecus quadratirostris Eastern African deposits are OMO USNO FORMATION more securely dated on ra- Member 11 1 diometric grounds. Laetoli is considered to be 3.8-3.5 my (Leakey et al. 1976; SOUTHERN AFRICA Leakey and Hay 1982), the Ml LM2 LM3 UMi UM2 UM3 Usno and Shungura Forma- Dinopithecus ingens, SWARTKRANS 3 5 7 4 7 5 tions at the Omo range in age from 2.9-1.3 my Gorgopithecus major, KROMDRAAI 1 3 4 3 4 (Shuey et al. 1974; Brown Papio angusticeps, KROMDRAAI 2 2 2 1 2 2 and Nash 1976; Brown et TAUNG 3 1 2 2 al. 1985), Koobi Fora and Papio robinsoni, SWARTKRANS 6 10 10 5 15 10 Ileret Formations range in Parapapio ionesi, SWARTKRANS 2 1 2 1 2 2 age from 3.3-1.5 my (Feibel 1 et al. 1989), Olduvai from STERKFONTEIN 3 7 3 4 5 2.2-0.6 my (Leakey and Parapapio whitei, STERKFONTEIN 2 4 4 2 2 2 Hay 1982) and Olorgesailie from 1.3-0.5 my (Potts Parapapio broomi, STERKFONTEIN 3 4 3 2 5 3 1989). Because of the long Theropithecus darti, SWART[RANS 2 4 2 3 79 time ranges represented at mostt of the deposits, grinding takes place during the second phase of samples of monkeys were examiiined according to occlusion as the jaw moves lingually and mesi- their stratigraphic unit of proveinience whenever ally, with the protoconid and hypoconid coming possible. into direct contact with the protocone and hypo- Dietary estimates for the fossil species are cone as a result (Crompton and Hiiemae 1970; based on the relationship betwreen molar mor- Kay and Hiiemae 1974; Kay 1975, 1978). The phology and diet in nine extarit species which tendency for monkeys that include large amounts have been studied extensively in the wild and for of leaves in their diets to have longer shear crests which the proportions of leaves and fruits in the than monkeys which eat greater amounts of fruits annual diet are known (Table 2). The species and seeds has been demonstrated by Kay (1975, considered were Colobus baditus (n=33), Colo- 1978, 1981; Kay and Covert 1984). bus guereza (n=22), Colobus satanas (n=2), In this study eight shear crest lengths for Presbytis melalophos (Kay anId Covert 1984), each upper and lower molar were measured using Presbytis obscura (Kay and Cc vert 1984), Cer- an ocular micrometer mounted in a stereoscopic cocebus galeritus (n=20), Cercocebus albigena microscope (Figure IA). Shearing crest develop- (n=25), Macaca nemestrina (n,=6) and Macaca ment was then appraised in four ways: 1) from fascicularis (n=34). Additional comparative data calculation of Kay's (1984) shear quotient (SQ) were taken from Kay (1978, 1981; Kay and for lower second molars; 2) from the sum of Covert 1984) and Benefit (198' 7). Dental termi- shear crests gauged against molar length (abbre- nology and measurements usted in this paper viated PERS); 3) from the sum of lingual (for follow Jolly (1972), Delson (1')73), Kay (1978, lower molars) or buccal (for upper molars) shear 1981) and Benefit (1987). crests relative to molar length (PERLS); and 4) Folivorous monkeys use their molars to from the sum of shear crests bordering the lingual puncture and shear leaves wihile frugivorous and buccal notches relative to molar length monkeys crush and grind hardler, more fibrous (PERMS). The shear quotient is calculated using fruits and seeds (Walker and Miurray 1975). Fo- the formula SQ = 100(So-Se/Se), with So (ob- livores emphasize the shearing or first phase of served shear) equal to the sum of the lengths of molar occlusion as the mandiblle moves upward the eight shear crests, and Se (expected shear) and medially, while frugivoroius crushing and equal to 2.79 (lower second molar length) to the 0.982 exponent. Because the shear quotient ex- aggerates variation in the observed sum of shear, Table 2. Average percentages offruits and leaves the simple indices (PERS, PERLS, PERMS) in the annual diets of the extanit cercopithecoid were also used. Unworn molars were measured species sampled. for calculations of SQ, PERS and PERMS. FRUIT LEAVES Since the lingual cusps of lower molars and the Colobus badius 7.6 74.7 buccal cusps of upper molars wear less rapidly Colobus guereza 13.6 68.3 than cusps on the opposite side of the tooth, PERLS has the advantage ofbeing measurable on Colobus satanas 58.0 37.0 both unworn and moderately worn molars. PERMS is especially useful for the measurement Presbytis melalophos 58.0 39.0 of lower molars with hypoconulids or accessory cuspules on the posthypocristid, such as the third Presbytis obscura 44.0 36.0 molars of all species and the first and second molars ofTheropithecus. Cercocebus galeritus 77.0o 13.0oFor each of the extant species listed above, the average shear quotient was plotted against the Cercocebus albigena 71.0 2.6 average proportion of fruits and leaves consumed Macaca nemestrina 74.2 13.0 annually (Figure 2). Shear quotient was found to *2 13 be significantly correlated to diet (Table 3). The Macaca fascicularis 62.5 20.0 same procedure was used for the shear indices of each upper and lower molar (Benefit 1987). For Data taken from Struhsaker (1975, 1!978), Marsh (1981), those indices found to be significantly correlated Clutton-Brock (1975), Gatinot (1975),,Oates (1977), Gau- to diet, regression equations best describing the tier-Hion (1978,1980), McKey (1978),,Homewood (1978), relationship (Table 4) were used to estimate the Waser (1977, 1984), Quris (1975),Freeland (1979), proportions of fruits and leaves eaten by the ex- Caldecott (1986), Aldrich-Blake (1980), MacKinnon and tinct monkeys. MacKinnon (1978), Mah(1980), Wheady (1980) and Rae- Greater shear crest length on the molars of makers and Chivers (1980). folivorous colobine monkeys is accomplished by 80

Figure 1. Measurements of molar features functionally correlated to diet among extant cercopithecoids. A. Lengths of shear crests, numbers 1-8; END = entoconid, MED = metaconid, HYD = hypoconid, PRD = protoconid. B. Lingual notch height; NH = vertical height from the notch to the base of the lin- gual notch, NR = vertical height from the base of the notch to the cervix below. C. Proximity between mesial pairs of cusps; MW = mesial width, MCP = distance between mesial cusp tips. D. Enamel thick- ness.

A

NCP NCP

ENAMEL ENAMEL T C K ..A R NlI N I 9 8 NzlIt a a

P NHY D AR D E X PO0 e D THICKNESS THICNES

CENCOPITHECINAA

c D

a decrease in the heights of the central basin, me- As for the shear indices, index NHNR sial fovea and distal fovea above the cervix, (height of the crown above the notch/height of the rather than through an increase in absolute cusp crown below the notch x 100) was plotted against height (Benefit 1987). As a result the lingual the proportions offruits and leaves eaten annually notch on lower molars (buccal notch on upper by the extant species and found to be significantly molars) is significantly taller and the height ofthe correlated to diet for the lower second and third crown from the base of the notch to the cervix is molars as well as for the upper second molar (Ta- significantly lower on colobine than on frugivo- ble 3). Regression equations based on NHNR rous cercopithecine molars (Delson 1973; Benefit (Table 4) are used in additon to the shear indices and Pickford 1986; Benefit 1987) (Figure 1B). to reconstruct the diets of the fossils papionins. 81 Figure 2. Bivariate plots of shear quotient values against percentages of food items in the annual diets of extant monkeys.

7+ 24. 7 22, 54. S14 20,

i,

14 St

12 12.

10. 90 a .58 S S

0 so 4 I'

0 32 3+ -2. 44. -2 4t

-4. -4

-S, 2. -S 24.

I. 14. -S. -S

-10 10 20 20 40 50 *0 70 s0 10 20 20 40 50 s0 T0 so LEAVES FRUITS

1 = Cercocebus albigena; 2 = Cercocebus galeritus; 3 = Macaca nemestrina; 4 = Macacafascicularis; 5 = Colobus satanas; 6 = Colobus guereza; 7 = Colobus badius; 8 = Presbytis melalophos; 9 = Presbytis obscura. Kay 1984; + Benefit 1987

The emphasis colobine and cercopithecine tremely limited on cercopithecine molars. Con- monkeys place on shearing and grinding is appar- sequently, the chance that opposing cusps will ent not only from the lengths of the shear crests rub against each other is enhanced, as is the rate and notch heights but also from the manner and at which the crown wears. The cusp tips of colo- rate at which the teeth wear. Although the enamel bine molars are set much further apart than those is thick, the molars of cercopithecine monkeys of cercopithecines (Benefit 1987). The wide dis- are adapted to wear flat rapidly, while the cusps tance between the cusps and the subsequently of thin enamelled colobine monkeys maintain large size ofthe central basin allows the occlu- their height and integrity even when large areas of ding cusps to interdigitate more freely, leading to dentine are exposed (Figure 3). The rapid rate at a decrease in the rate at which the molars wear. which cercopithecine teeth wear is probably rela- The combination oflow cusp relief and close ted to the significantly closer proximity of their cusp proximity causes cercopithecine molars to cusp tips and loph(id)s than is observed for wear flat rapidly. The shearing capacity of the colobines (Benefit 1987), and the resulting con- molar is lost as wide enamel rims, created by the striction of the central basin. The space in which merging together of worn grinding facets, form occluding cusps and basins can interdigitate is ex- around circular and concave patches of dentine on 82

Table 3. Pearson correlation coefficients for den- within each subfamily for the extant sample, cor- tal indices significantly correlated to the average relations between a simple enamel index relating proportions of fruits and leaves included in the enamel thickness to molar length and diet was not annual diets of nine extant species. found to be significant, and no regression equa- L = Lower, U = Upper. tion was computed. However, the relationship between enamel thickness and diet was demon- INDEX FRUIT LEAVES strated by Kay (1981; Kay and Covert 1984) on LM2 SQ -0.9450 0.9710 the basis of logarithm-transformed measure- ments. Enamel thickness is therefore referred to LM2 PERS -0.9642 0.9766 in this paper as a general indicator of frugivory and folivory. LM2 PERLS -0.9738 0.9855 One of the inherent problems in reconstruc- ting the diets of extinct monkeys based on dental LM2 PERMS -0.9599 0.9773 morphology is that the dental indices alone do not differentiate grass-eating from leaf-eating. The UM2 PERS -0.9882 0.9806 molars of extant grass-eating Theropithecus gel- ada are unique among cercopithecids in that they UM2 PERLS -0.9815 0.9743 combine characteristics of both folivorous col- obine and frugivorous cercopithecine molars. UM2 PERMS -0.9744 0.9751 From the lingual perspective, the lower molars of T. gelada resemble colobine monkeys with high LM2 FL -0.9302 0.9149 occlusal relief, low crown height below the lin- gual notch and long shear crests. From buccal LM3 FL -0.9087 and occlusal perspectives, Theropithecus lower molars resemble cercopithecines with close cusp LM2 NHNR -0.9648 0.9682 proximity, small central basins, short shear crests and a high position of the lowest point of the lo- LM3 NHNR -0.9828 0.9695 phids above the cervix. As might be expected from consideration of the cercopithecine charac- UM2 NHNR -0.9506 0.9593 teristics of the molars, the cusp tips wear flat rapidly with flat enamel rims quickly forming on the molars. As noted by Jolly (1972), the pattern of enamel ridges is more elaborate on Theropithe- the flat cusp tips (Figure 3). Because cercopithe- cus than other monkeys due to the presence of cine crowns are flared, with greater width at the additional ridges, clefts and infoldings of enamel cervix than between mesial and distal pairs of along the mesial and distal shelves. Grasses are cusps, the perimeter of the enamel rim and the milled between the teeth as occluding molars surface area that can be devoted to grinding in- scrape transversely against each other in a manner creases as the crown wears. On colobine molars, similar to that of grazing ungulates. The enamel which experience little change in cusp relief as rims differ from those ofother in they wear, elongated areas of dentine surrounded being positioned well above the occlusal basin. by thin enamel rims occur along the crests of The height ofthe wear surface is thought to main- lophs, providing little surface area for crushing tain the lifetime of the crown as the teeth are and grinding. subjected to rapid wear resulting from abrasion For the extant species sampled, significant by the grasses and soil particles that adhere to correlations were found between proportions of plants (Jolly 1972). fruits and leaves consumed and the degree to From consideration ofTheropithecus molars which the lower second and third molars and it is surmised that either the consumption of abra- upper second molars were flared (mesial crown sive silicaceous grasses and/or the cercopithecine width at the apex of cusps/mesial width x 100) characteristic of close cusp prximity are respon- (Figure 1C; Table 3). As for cusp relief and sible for the rapid rate of cusp deformation. We shear indices, regression equations based on conclude that if a species has long shear crests, these measurements were used to estimate the colobine-like cusp proximity and thin enamel, but diets of fossil species. a rapid rate of cusp deformation, it may have In addition to the dental indices mentioned eaten grass rather than leaves. Patterns of wear above, enamel thickness was also measured on are therefore considered together with dental in- the extant and fossil teeth (Figure ID). Because dices in reconstructing the diets of fossil species. there was little variation in enamel thickness However, differentiating grass-eating from leaf- 83 eating molars, given a combination of colobine (66.5% fruits) was found to be highly frugivo- and cercopithecine characteristics (as in Thero- rous. Otherwise, three of the southern species pithecus), presents an extremely difficult and were reconstructed as having consumed 58-60% perhaps unresolvable situation. fruits and five as 50-55% fruits. In eastern Africa, fossil Parapapiojonesi (83% fruits), Cer- cocebus (74% fruits) and Papio (67% fruits) RESULTS were found to be the most committed to frugivory (74% fruits, on average), while Parapapio ado Papionina and Parapapio spp. were found to be the least frugivorous (52-53% fruits). Dietary estimates for fossil Cercopithecinae are presented in Table 5. In general, southern African papioninans were found to be less com- Theropithecus mitted to frugivory than their eastern African counterparts, the average diet of the former con- The dietary habits of fossil Theropithecus are sisting of 56% fruits and 27% leaves (range: 50- more difficult to assess than those of other ba- 66.5% fruits, 16-33% leaves) and the latter 61% boons due to their unusual molar morphology fruits and 22.5% leaves (range: 52-83% fruits, which includes the presence of accessory cus- 0-31.5% leaves). Among the southern African pules along shear crests bordering mesial and species only the diet of Dinopithecus ingens distal shelves. The accessory cuspules make it

Table 4. Linear regression equations used to reconstruct the proportions offruits and leaves consumed by fossil species. L = Lower, U = Upper. St d, Err. R-squared Estimate Fruit=62.53 - (2.37139 * LM2SQ) 0.89304 8.887 Leaves=24.67 + (2.48568 * LM2SQ) 0.94290 6.625 Fruit=57.77 - (-0.97320 * LM2SQW) 0.94712 8.1536 Leaves=25.25 + (0.97424 * LM2SQW) 0.94914 7.8701 Fruit=236.59 - (3.0471 * LM2FL) 0.86529 11.6888 Leaves=-145.70 + (2.94397 * LM2FL) 0.86370 12.6289 Fruit=95.24 - (0.55408 * LM2NHNR) 0.93086 9.3229 Leaves=-145.70 + (0.5472 * LM2NHNR) 0.93739 8.7323 Fruit=301.29 - (0.8998 * LM2PERS) 0.92977 9.3967 Leaves=-217.57 + (0.89692 * LM2PERS) 0.95370 7.5092 Fruit=203.04 - (1.20434 * LM2PERMS) 0.92131 9.9461 Leaves=-159.24 + (1.50747 * LM2PERMS) 0.95507 7.3971 Fruit=102.79 - (0.65061 * LM3NHNR) 0.92580 6.5573 Leaves=-18.37 + (0.63173 * LM3NHNR) 0.940 8.5481 Fruit=119.11 - (1.22808 * UM2NHNR) 0.90372 11.0018 Leaves=-35.72 + (1.21971 * UM2NHNR) 0.92026 9.8542 Fruit=318.61 - (0.97324 * UM2PERS) 0.97732 5.3396 Leaves=-229.35 + (0.95017 * UM2PERS) 0.96167 6.8321 Fruit=337.32 - (2.0863 * UM2PERLS) 0.96337 6.7857 Leaves=-247.89 + (2.0353 * UM2PERLS) 0.94983 7.8163 Fruit=265.76 - (1.77564 * UM2PERMS) 0.94946 7.9708 Leaves=-179.61 + (1.7489 * UM2PERMS) 0.95089 7.7333 84 Figure 3. Comparison of worn colobine and cercopithecine molars. LOWER MOLARS

M t ~~~~DDX-

CERCOPITHECINAE COLOBINAE

a

D difficult to measure mesial and distal shear crests rous in the wild (Dunbar 1983). accurately. As a result the shear quotient, which It is impossible to know whether fossil incorporates the lengths of all crests, is highly va- Theropithecus consumed leaves or grasses. riable. The length of shear crests bordering the Examination of wear striations under a light mi- central basin provide the least variable and croscope revealed deep bucco-lingually oriented therefore most reliable measure of shear for parallel striations and the relative absence ofpits Theropithecus. on the molars of T. oswaldi from Koobi Fora Estimated proportions of fruits and leaves (Benefit 1987). These deep striations were pro- consumed by fossil Theropithecus based on SQ, bably caused by the inclusion of grit in the diet of PERMS and the average ofpredictions of all indi- T. oswaldi. They are also indicative of a heavy ces are summarized in Table 6. Predictions based reliance on the transverse component of mastica- on index PERMS for lower second molars were tion, such as is associated with grass-eating in found to more accurately reflect the diet ofextant modern T. gelada. It is plausible that the non- T. gelada than those based on shear quotients fruit component of the diet of T. oswaldi consis- (Table 6). It is therefore reasonable to assume ted of the blades, seeds and rhizomes of grasses that predictions based on PERMS for fossil spe- as suggested by Jolly (1972), rather than leaves. cies are also more accurate, and greater weight is However, the diet of T. oswaldi is reconstructed placed on these results. here as having been more eclectic than that of T. All dietary predictions indicate that the south- gelada, counter to Jolly's (1972) suggestion that ern African T. darti and the more ancient of the the species predominantly ate grass. eastern African Theropithecus, T. brwnpti (3.2- The molars of T. brunpti are generally more 2.0 my) and T. quadratirostris (3.4-3.2 my), gracile than those ofT. oswaldi with fewer acces- have had longer shear crests and a higher poten- sory cuspules and infoldings of enamel. Deep tial for folivory than the more recent eastern transverse striations are not apparent on the worn African species T. oswaldi (2.5-0.5 my). These molars of T. brwnpti, indicating that little grit ad- results are partly corroborated by the presence of hered to its food and that possibly the transverse thicker enamel on the molars of T. oswaldi from component ofmastication was not emphasized by the Omo [enamel thickness (1.5 mm)/crown the species. Theropithecus brumpti may have length (17.3 mm) = 8.7%] than on molars of T. been a true papionin folivore rather than a grass- brumpti from the same site [enamel thickness eater. A similar diet is suggested for T. quadra- (1.16 mm)/crown length (15.6 mm) = 7.4%], tirostris and T. darti. The rapid rate of cusp indicating a greater potential for frugivory for the deformation observed for the molars of T. former. According to index PERMS all fossil brumpti can be attributed to the close proximity of Theropithecus included more fruits in their diets the molar cusps and the consumption of fruits, than do extant , which are rarely frugivo- rather than to a diet of abrasive grass. 85

Table 5. Estimated proportions of fruits and leaves con- Theropithecus oswaldi sumed OBI FORA & ILERET LM2FL 61.7 23.2 by fossil cercopithecines. (For Omo Theropithecus R0 LM2PERMS 49.8 32.5 and Theropithecus gelada, s = shear crests measured in a UM2PERS 72.7 10.7 straight line without inclusion of accessory crests and UM2PERLS 81.6 1.5 cuspules and a = additive shear crest measurements with UM2PERMS 58.6 24.4 inclusion ofall features.) mean 53 42 AREA 1 (1.5-1.6 my) LM2SQW 51.4 31.9 EAST AFRICA LM2NHNR 15.4 67.3 UM2PERS 100.0 0 FRUIT LEAVES UM2PERLS 88.2 0 Cercocebus sp. [OOBI FORA LM2SQ 79.6 6.8 UM2PERMS 81.6 1.8 LM2SQW 66.6 16.4 mean 67 20 LM2NHNR 65.9 17.2 LM2PERS 84.2 0 AREA 8 (1.5-1.6 my) LM2SQW 49.8 33.2 LM2PERMS 72.5 4.2 LM2FL 48.2 36.3 LM2FL 92.4 0 LM2NHNR 54.3 28.7 LM3NHNR 67.9 18.4 mean 51 33 UM2NHNR 52.3 30.6 UM2PERS 74.9 8.5 AREA 103 (1.6-1.7 my) LM2FL 100.0 0 UM2PERLS 70.7 12.2 LM2NHNR 43.0 39.8 UM2PERMS 71.3 11.95 LM2PERMS 41.25 43.2 mean 74 11.5 mean 61 28 Cercocebus ado OLDUVAI LM3NHNR 74.6 8.9 AREA 10 (1.7-1.9 my) UM2NHNR 9.0 73.6 UM2PERMS 33.9 48.7 Parapapio ado LAETOLIL LM2SQ 60.0 27.3 mean 21.5 61 LM2SQW 56.1 26.9 LM2NHNR 50.8 32.1 AREA 123 (1.7-1.9 my) LM3NHNR 26.3 55.9 LM2PERS 58.9 24.0 LM2PERMS 41.4 43.1 AREA 130 (1.8-1.9 my) LM2SQ 63.1 24.0 LM2FL 0 83.5 LM2SQW 58.6 24.4 UM2NHNR 82.0 1.1 LM2NHNR 45.6 37.3 UM2PERMS 68.9 14.2 LM2PERS 65.0 18.0 mean 52 31.5 LM2FL 80.4 5.2 LM3NHNR 34.3 48.1 Parapapio jonesi KANAPOI LM2SQW 83.1 0 UM2NHNR 34.9 47.9 UM2PERS 63.0 15.1 Paraoapio sp. OOBI -?ORA LM2SQW 58.4 24.6 UM2PERLS 71.0 11.9 LM3NHNR 69.7 12.7 UM2PERMS 64.8 18.3 UM2NHNR 32.3 50.0 mean 58 25 mean 53 29 AREA 104 (1.7-2.0 my) LM2SQ 36.1 52.4 Papionini indet. BAR-NGO LM3NHXR 63.3 19.9 LM2SQW 46.9 36.1 LM2NHNR 17.1 65.3 Papio sp. OLDUVAI LM2FL 39.0 45.2 LM2PERS 36.1 46.7 LM2NHNR 61.9 21.2 LM2PERMS 40.1 44.7 LM3NHNR 60.0 23.1 LM2FL 30.5 53.5 UM2NHNR 21.0 61.7 mean 27.5 50 UM2PERS 99.5 0 UM2PERLS 96.3 0 AREA 106 (2.0 my) LM2NHNR 47.9 35.0 UM2PER!S 90.5 0 mean 67 13 AREA 116 (2.0 my) UM2PERS 82.9 0.8 Theropithecus brumpti UM2PERLS 97.8 0 KOOBI FORA/TULU BOR UM2PERMS 38.8 43.2 AREA 117 (3.2-3.3 my) LM2SQ 46.1 41.7 mean 73 15 LM2SQW 51.0 32.0 LM2NHNR 26.6 56.0 OLDUVAI LM2FL 100.0 0 LM2PERS 45.4 37.5 LM2PERS 72.9 10.1 LM2PERMS 26.3 62.0 LM2PERMS 54.0 27.4 LM3NHNR 28.3 54.0 mean 76 12 UM2PERS 70.3 13.0 UM2PERLS 72.2 10.7 OLORGESAILIE LM2SQW 49.2 33.8 UM2PERMS 65.0 18.1 LM2FL 92.8 0 mean 48 36 LM2NHNR 22.7 59.8 LM2PERS 55.4 27.5 LM3NHNR 26.35 55.9 LM2PERMS 47.3 35.7 AREA 203 (3.3 my) LM3NHNR 0 99.6 OMO SHUNGURA FORMATION UM2PERS 87.4 0 Member unknown LM2SQW a 61.4 21.6 UM2PERLS 100.0 0 LM2FL a 13.2 70.1 UM2PERMS 64.9 18.2 mean 37 46 mean 53 30 Members C-G SQ 28.8 60.1 Theropithecus Member C LM2SQ a 55.4 32.1 quadratirostris OMO LM2PERS a 0 83.8 a 11.4 78.1 LM2PERMS 28.4 60.4 LM2PERS s 57.0 25.9 mean 14 72 a 17.0 66.6 LM2PERMS 36.8 50.1 Theropithecus aelada EXTANT LM2SQ m 60.2 27.1 mean a 50 36 a 30.7 58.1 mean a 22 65 LM2PERS m 43.0 39.8 Member D LM2SQ a 0.6 89.5 a 0 90.9 LM2PERS a 0.8 82.0 LM2PERMS 0 86.5 LM2PERMS 28.4 60.4 mean a 34 51 mean 10 77 mean a 10 78.5 86

Table 5, continued. SOUTHERN AFRICA Dinopithecus ingens FRUIT LEAVES Parapapio Jonesi SWARTKRANS LM2SQW 15.9 67.1 SWARTKRANS LM2SQ 68.9 14.3 0 LM2SQW 62.1 20.9 LM2FL 95.1 LM2NHXR 63.8 19.3 LM2NHNR 53.4 29.5 LM2PERS 73.1 9.9 mean 55 32 LM2PERMS 62.4 16.8 STERKFONTEIN LM2SQ 48.4 39.4 LM2FL 66.0 19.2 LM2SQW 53.3 29.8 LM3NHNR 60.8 22.4 LM2NHNR 62.2 20.8 UM2PERS 75.0 8.4 LM2PERS 49.8 33.2 mean 66.5 16 LM2PERMS 51.4 30.6 LM2FL 60.3 24.6 Gorgopithecus major 55.6 27.5 KROMDRAAI LM2SQ 36.7 51.8 LM3NHXR LM2SQW 47.5 35.5 UM2PERS 48.5 34.4 LM2PERS 36.9 45.9 UM2PERLS 40.8 41.4 LM2PERMS 31.4 55.6 UM2PERMS 61.0 22.1 LM2FL 66.3 18.9 mean 53 30 LM2NHNR 50.2 32.7 LM3NHNR 28.5 27.6 Parapapio whitei SWARTKRANS UM2PERS 67.9 15.4 UM2PERS 100.0 0 UM2PERLS 61.1 21.6 UM2PERLS 100.0 0 UM2PERMS 27.5 55.0 UM2PERMS 100.0 0 52 31 mean 60 27 mean STERKFONTEIN LM2SQ 46.8 41.1 Papio angusticeps LM2SQ;; 51.3 31.7 KROMDRAAI LM2SQ 58.3 29.1 LM2NHNR 48.2 34.6 LM2SQW 58.0 25.0 LM2PERS 45.7 37.2 LM2NHSR 61.8 21.2 LM2PERMS 46.6 36.6 LM2PERS 61.9 21.1 LM2FL 36.6 47.5 LM2PERMS 56.1 24.7 LM3NHNR 45.2 37.5 LM2FL 53.3 31.4 UM2PERS 83.5 0.2 LM3NHNR 45.9 36.9 0 UM2PERS 54.0 29.0 UM2PERLS 97.2 UM2PERLS 60.8 21.9 UM2PERMS 81.6 1.7 UM2PERMS 65.5 17.6 mean 54 27 mean 58 24

Parapapio broomi Papio angusticeps STERKFONTEIN LM2SQ 60.4 22.7 TAUNG LM3NHNR 63.3 20.0 LM2FL 59.6 25.3 UM2PERS 46.8 36.0 LM2NHNR 56.3 26.6 UM2PERLS 44.7 37.6 LM2PERS 67.3 15.2 UM2PERMS 45.1 37.7 LM2PERMS 45.3 38.2 mean 50 33 LM3NHNR 43.9 38.8 mean 55.5 28 Papio robinsoni SWARTKRANS LM2SQ 58.4 29.0 Theropithecus darti LM2SQW 58.3 24.7 SWARTKRANS LM2SQ 23.6 65.4 LM2PERS 57.8 25.2 LM2SQW 45.6 37.4 LM2PERMS 56.1 24.7 LM2NHNR 12.1 70.3 LM2NHNR 54.1 28.9 LM2PERS 33.1 41.7 LM3NHNR 55.1 28.0 LM2PERMS 35.8 50.1 UM2PERS 67.1 16.1 LM2FL 95.4 0 UM2PERLS 68.0 14.8 LM3FL 5.9 77.2 UM2PERMS 61.5 21.6 LM3NHNR 0 84.9 mean 60 23 mean 31 53

DISCUSSION of Papio baboons living in unforested (desertic) areas of Namibia consisted of 80% grasses The relative proportions of fruits, leaves and (Hamilton et al. 1978). In a similar environment grasses in the diets of fossil baboons is probably in Ethiopia the diet consisted of 40% related to whether or not they occupied forest or grasses (Dunbar and Dunbar 1974). In contrast, woodland habitats versus open or treeless savan- grass composed only 10-20% of the diet of nahs. African grasslands are characterized by baboons living in heavily forested areas, and 20- low and seasonal fruit productivity. Grasses are 50% of the diet of baboons living in wooded but an important supplement to the diets of baboons not heavily forested regions (Post 1978; Popp living near or on the savannah during times of the 1978; Kummer 1968; Sharman 1980; Dunbar and year when fruits are unavailable (Dunbar 1983). Dunbar 1974). Based on the principle of uni- Extant baboons exploiting forested habitats tend formitarianism, it is assumed that the same to eat higher quantities of fruits than grasses or relationship between diet and habitat observed for herbs, while the opposite is true of baboons li- extant baboons would have existed for fossil ving in scrub savannah (Dunbar 1983). The diet papionins. 87 The idea that the diets and habitats ofextant In general, baboons from Sterkfontein and species can be used to infer that highly frugivo- Taung appear to have included larger quantities of rous fossil baboons of eastern Africa occupied grasses or herbaceous foods in their diets than the forest or woodland habitats has been suggested baboons from Kromdraai and Swartkrans. The independently by Leakey (1982). It is probably presence of the most frugivorous of the southern more than coincidence that the least frugivorous baboons at Swartkrans, Dinopithecus ingens, of the eastern African baboons, Parapapio ado, indicates that the site may have been associated comes from the site of Laetoli which has been with a higher degree of tree cover than Taung or reconstructed as a dry savannah environment Sterkfontein. This evidence contradicts inter- (Leakey 1982). Indications that the southern pretations of Swartkrans as representing a drier African papioninans were less frugivorous than environment than was represented at Sterkfontein those from eastern Africa (Table 5) is similarly (Cartmill 1967; Vrba 1982). consistent with reconstructions of the southern A situation analogous to that of the baboons cave deposits as representing drier, more open was discerned for australopithecines based on the savannah habitats than was typical of eastern study of deciduous teeth (Grine 1981). Similar African sites such as Koobi Fora and the Omo to the baboons, Grine (1981) observed that Aus- (Boaz 1977). tralopithecus robustus at Swatans had shorter

Table 6. Summary of dietary predictions for Theropithecus. SHEAR QUOTIENT FRUITS LEAVES/GRASSES Mean Range Mean Range T. gelada 45.5 31-60 42.5 27-58 T. oswaldi 50 36-63 38 24-52 T. brumpti 28.5 0.5-46 60 32-89.5 T. darti 24 65 PERMS FRUITS LEAVES/GRASSES Mean Range Mean Range T. gelada 0 86.5 T. oswaldi 47 40-54 36 27-45 T. brumpti 30.5 26-3 7 56 50-62 T. darti 36 50 T. quadratirostris 28 60 MEAN OF ALL INDICES FRUITS LEAVES/GRASSES Mean Range Mean Range T. gelada 22 10-34 65 51-78.5 T. oswaldi 65.5 21.5-76 36 12.5-61 T. brumpti 33 10-51 53 36-77 T. darti 31 53 T. quadratirostris 14 72 88 shear crests and probably ate more hard fruits plained by the absence of forested environments than africanus at Taung and in that region. This hypothesis is consistent with Sterkfontein. However, Grine (1981) attributed the absence of leaf-eating colobine monkeys in the shorter shear crests ofA. robustus to the con- the southern African cave deposits. The only sumption of small and hard, dry-adapted fruits fossil colobine found in southern Africa, Cerco- and reconstructed Swartkrans as more xeric than pithecoides, exhibits open country cursonral Taung and Sterkfontein. It is equally possible postcranial adaptations (Birchette 1981) and an that, as is the case for the baboons at Taung and unusual pattern of tooth wear that can only have Sterkfontein, A. africanus had longer shear crests resulted from the consumption of grasses than A. robustus because it supplemented its diet (Benefit 1987). Alternatively, Theropithecus in with grasses and herbs. According to Dunbar southern Africa may have suffered from com- (1983), hard and small legumes are extremely petition with grass-eating savannah adapted scarce on the African savannah and would have papioninan baboons. Papioninans were present proved an unlikely diet for any , including in southern Africa during the late at the australopithecines. Based on this evidence, site of Langebaanweg (Grine and Hendey 1981), Grine's (1981) data corroborate the reconstruc- but Theropithecus did not occur in the area until tion of Swartkrans as having been more mesic the Middle at the site of Makapansgat. than Taung or Sterkfontein. If Theropithecus were endemic to eastern Africa, The inclusion of more fruits in the diet of as seems likely, they may have arrived in south- fossil Theropithecus indicates that its habitat may ern Africa after the papioninan baboons had have been characterized by a higher degree oftree successfully fllled the grass-eating niches avail- cover than that occupied by the extant species T. able to monkeys, inhibiting Theropithecus from gelada. Theropithecus oswaldi, which probably "swamping" the southern grasslands with its high consumed grasses rather than leaves, is likely to population numbers, as T. oswaldi did in eastern have occupied open country habitats adjacent to Africa. more wooded areas, such as grasslands growing The greater diversity ofTheropithecus in the along the margins of shallow lakes where sea- eastern region is in part attributable to reduced sonal flooding inhibited the growth of trees, as competition between species of the genus as a re- suggested by Jolly (1972). If the geologically sult ofdiffering preferences for fruits, leaves and more ancient of the eastern African species, T. grasses. The overwhelming abundance of T. os- brumpti and T. quadratirostris, consumed leaves waldi fossils in collections from eastern Africa rather than grasses as has been suggested here, it between 2.5 my and 0.5 my may be due to its is possible that they inhabited forested environ- having lived closer to fluvial and lacustrine depo- ments. This reconstruction is consistent with sitional environments than the more forest postcranial studies by Ciochon (1986) indicating adapted monkeys, resulting in a higher frequency that T. brumpti may have been less cursorial than of fossilization. It is also likely that population T. oswaldi and that it may have occupied a forest numbers of T. oswaldi were absolutely greater habitat similar to that of the extant . The than those of the forest cercopithecines. Popula- occurrence of T. darti, which is also reconstruc- tion densities of extant T. gelada are considerably ted as having eaten more leaves than grass, at higher than those of any known population of Swartkrans provides further evidence that the site Papio, presumably because dense and evenly dis- may have been more mesic than other studies tributed grasses can support larger numbers of have indicated. Since leaf-eating, forest adapted animals than forest resources which are more Theropithecus are more ancient than savannah sparsely and patchily distributed (Dunbar 1983). dwelling species, we suggest that the origin of The lower species diversity and rarity of the genus is linked to the beginnings of leaf- papioninan fossils in eastern Africa may have re- eating in forest dwelling baboons, as opposed to sulted from their preference for forest habitats. grass-eating in open country environments as The eastern mangabeys and baboons would have suggested by Jolly (1972). competed for forest resources with T. brumpti The dietary and habitat preferences of the and large-bodied colobine monkeys. Plio-Pleis- fossil cercopithecines almost certainly influenced tocene colobine monkeys seem to have been less the patterns of species diversity and relative specialized for folivory than their extant relatives. abundance observed for Plio-Pleistocene Thero- Paracolobus andRhinocolobus have been recon- pithecus and papioninans in eastern and southern structed as including almost equal portions of Africa. If the origin of the genus Theropithecus fruits and leaves in their diets (Benefit 1987, is linked to the beginnings ofleaf-eating in forest 1990). Competition between the forest baboons dwelling baboons, as suggested here, the paucity and colobines would have been more intense of Theropithecus in southern Africa may be ex- during the Plio-Pleistocene than it is today. As a 89 consequence, the diversity of forest dwelling brumpt was observed to have a greater potential members of both Colobinae and Cercopithecinae for shearing and thinner enamel than T. oswaldi. seems to have been effected. Since Papio ba- It also placed less emphasis on the transverse boons did not become the dominant savannah component of mastication than T. oswaldi. This monkey in eastern Africa until after the demise of evidence indicated that T. brumpti may have con- T. oswaldi, when it presumably began to exploit sumed leaves rather than grasses. It is postulated the grassland habitats for the first time, it is pos- that T. brwnpti inhabited forested habitats, unlike sible that competition with T. oswaldi prevented the more recent species T. oswaldi which the papioninans from taking advantage of grass- consumed grasses and occupied open country land resources at an earlier time. Competition habitats such as grasslands along seasonally with other forest monkeys and lack of grass-eat- flooded lakes and rivers. Since the folivorous ing savannah adaptations, combined with lower Theropithecus species (T. brumpti, T. quadratir- population densities in forest habitats, are pro- ostris and T. darti) are geologically older than the bably responsible for the low numbers and grass-eating species (T. oswaldi and T. gelada), diversity ofpapioninan fossils at deposits in east- the origin of the genus is attributed here to the ern Africa. Thus, the greater abundance and beginnings of folivory in a large-bodied forest diversity of the southern papioninan baboons is dwelling papionin. The paucity of Theropithecus attributed to the absence of, and lack of com- in southern African deposits can be explained by petition with, T. oswaldi and forest dwelling the absence of forested habitats in the region, colobines, to the general tendency for grasslands and/or by the inability of T. darti to successfully to support large numbers of animals, and to a di- compete with the savannah adapted papioninan versity of dietary preferences among the baboons baboons. The abundance of Theropithecus, es- themselves. pecially T. oswaldi, in eastern African deposits may be due to their occupation of habitats that were more prone to fossilization, such as the SUMMARY shores of lakes and rivers, as well as to their greater population numbers. Measurements of dental features shown to be functionally correlated to diet among extant mon- keys were used to establish criteria from which to ACKNOWLEDGMENTS assess the relative proportions of fruits and leaves/grasses consumed annually by extinct ba- We are grateful to the Office of the Pres- boons from Plio-Pleistocene deposits in eastern ident, Republic of Kenya for permission to and southern Africa. The reconstructed diets of conduct research in Kenya. We are also grateful fossil papioninans from southern Africa include a to the Director () of the National generally higher percentage of herbaceous mate- Museums of Kenya, as well as to the curators rials than do the diets of their eastern African ( and Lou Jacobs) and staff (Alice counterparts. It is suggested that the southern Maundu, Aifreda Ibui and Mary Muungu) of the baboons were savannah adapted, supplementing Department of Palaeontology, for permission to their diets with grasses dunng periods when study materials in their care and for the generous fruits were seasonally unavailable, in a manner use of their resources. Access to southern Afri- similar to extant Papio baboons (Dunbar 1983). can fossils and resources was granted by Philip The more frugivorous mangabeys and baboons Tobias of the University of the Witswatersrand of the eastern region probably occupied habitats Medical School, Department of Anatomy, and with higher tree cover such as forests and wood- C.K. Brain, Elizabeth Vrba, Alan Turner and Da- lands. Competition from large-bodied colobine vid Panagos of the Transvaal Museum. Prof F. monkeys and both grass- and leaf-eating Thero- Clark Howell generously granted access to speci- pithecus, in addition to lower population mens collected by the Omo expedition which are densities, may be responsible for the rarity and temporarily housed in the Laboratory for low diversity of eastern African papioninan ba- Evolutionary Studies at U.C. Berkeley. Grati- boons. The greater abundance and diversity of tude is also expressed to Guy Musser and the southern savannah adapted baboons is Wolfgang Fuchs of the American Museum of attributed to the late ardval and scarcity ofThero- Natural History where the comparative extant pithecus, as well as to the capacity for grasslands monkeys were measured. We thank Richard F. to support large numbers ofanimals. 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