Terrestrial foraging and dental microwear in Papio ursinus

PRIMATES, 40(4): 559-572, October 1999 559

Terrestrial Foraging and Dental Microwear in Papio ursinus

DAVID J. DAEGL1NG Yale University

and FREDERICK E. GRINE State University of New York

ABSTRACT. Dental microwear of ten wild-shot chacma baboons (Papio ursinus) from Northwest and Northern Provinces, South Africa was examined by scanning electron microscopy. All specimens were collected during the dry season, during which these primates exploit hypogeous (underground) food items, including tubers and corms. The microwear fabric of this P. ursinus sample is characterized by high pitting frequencies and large microwear features. It differs significantly from those displayed by other terrestrially foraging papionins of the genus Theropithecus. Exogenous grit is hypothesized to be largely responsible for the observed P. ursinus wear pattern, which resembles the microwear profiles of durophagous primates. It is suggested that large microwear features and a high incidence of enamel pitting, which are generally held to represent a microwear "signature" of durophagy, may not always be indicative of hard-object feeding in anthropoid primates.

Key Words: Diet; Feeding behavior; Scanning electron microscopy; Papionins.

INTRODUCTION

The study of dental microwear has emerged as an effective technique by which the dietary habits of extinct primates may be inferred. It has been applied to a number of fossil taxa, including Paranthropus and Australopithecus (WALKER, 1981; GRINE, 1981, 1984, 1986, 1987; GmNE & KAY, 1988; KAY & GRINE, 1988; UNGAR & GRINE, 1991), Sivapithecus (COVERT & KAY, 1981; TEAFORD & WALKER, 1984), Theropithecus (TEAFORD, 1993), and Gigantopithecus (DAEGLING & GRINE, 1994). An ever-growing inventory of data on the microwear of extant primates with known diets provides a comparative baseline by which the patterns observed in extinct taxa may be evaluated (RYAN, 1981; GORDON, 1982; TEAFORD & WALKER, 1984; TEAFORO, 1985, 1986, 1993; TEAFORD & ROmNSON, 1989; UNBAR, 1990, 1994; KELLEY, 1990; TEAFORD & GLANDER, 1991; TEAFORD & RUNESTAD, 1992; TEAFORD et al., 1994; DAEGLING & GRINE, 1994).

The prevailing wisdom among those who study dental microwear is that the relative proportion of distinctive features (i.e. pits versus scratches) provides a reliable, if somewhat imprecise guide to diet (TEAFORD, 1994). A preponderance of elongate, relatively narrow striations (scratches) is generally indicative of a high degree of folivory, whereas a disproportionate number of deeply excavated, roughly ovoid gouges (pits) usually corresponds to durophagous activity. Dietary habits may also be inferred by analyzing microwear feature dimensions, which obviates the use of arbitrarily defined categories such as pits and scratches. The degree to which feature width in particular corresponds to diet in modern primates is impressive: mean feature widths of hard- object feeders such as Cercocebus albigena and Cebus apella are large, while those of more folivorous taxa (e.g. Colobus and Gorilla) are notably smaller (TEAFORD & WALKER, 1984).

Despite such encouraging results, several confounding factors can potentially produce false dietary signals which are obviously relevant for the interpretation of the microwear patterns of

560 D.J. DAEGLING 81. E E. GRINE

fossil species (GORDON, 1984; TEAFORD • OYEN, 1989; TEAFORD, 1994). For example, paleoeco- logical factors might account for observed microwear differences in two species that have similar diets but occupy ecological zones that differ in relative aridity (TEAFORD, 1993). Not only may seasonal and ecological factors be reflected in occlusal microwear patterns (TEAFORD & GLANDER, 1991; TEAFORD et al., 1994), but collection bias may either accentuate or mask such variation (TEAFORD & ROBINSON, 1989). Finally, nondietary items, such as exogenous grit, may contribute to microwear feature formation (cf. COVERT & KAY, 1981; GORDON & WALKER, 1983; KAY & COVERT, 1983), perhaps even in the higher levels of forest canopies (UNGAR et al., 1995).

A seminal study of microwear indicated that browsers and grazers could be distinguished from one another based on dental wear profiles (WALKER et al., 1978). That study implicated not only food items, but also the mode of foraging (i.e. terrestrial vs arboreal) as an important variable in the etiology of microwear features. Terrestrial foraging also has been implicated as a significant variable in the production of non-occlusal microwear in primates (UNGAR & TEAEORD, 1996).

With reference to occlusal microwear patterns among anthropoid primates, the effects of terrestrial foraging have yet to be explored thoroughly; an exception is TEAFORD'S (1993) study of modern and fossil species of Theropithecus. Among extant papionins, Theropithecus gelada is the most terrestrial (FLEAGLE, 1988). TEAFORD (1993) demonstrated that microwear of T. gelada most closely resembles that exhibited by folivorous primates, despite the fact that geladas feed primarily on grasses and grass seeds (JOLLY, 1970; DUNBAR 8,: DUNBAR, 1974; DUNBAR, 1977; IWAMOTO, 1979; IWAMOTO & DUNBAR, 1983). Chacma baboons, by contrast, are more catholic in their food choices. Insects, arthropods, fruits, seeds, grasses, leaves, and tubers are taken in various quantities, with seasonal opportunistic exploitation of preferred items (HALL, 1963; HAMILTON et al., 1978). Of relevance to the present study is the observation that Papio ursinus forages extensively for hypogeous (i.e. underground) food items during the dry season months (WHITEN et al., 1987, 1991; BYRNE et al., 1993). These items include roots, corms, bulbs, and plant stem bases. By contrast, the exploitation of subterranean or "ground-level" items by Theropithecus is largely limited to grass roots and stems, and these items account for a mere fraction of the gelada's diet (DUNBAR & DUNBAR, 1974).

Because the diet of P ursinus is considerably more variable and generalized than that of T. gelada, the microwear fabrics of these two taxa might be expected to differ as well. Of particular interest is whether substantial quantities of hypogeous items in the diet of P ursinus produce differences in microwear with respect to T. gelada, a terrestrial forager that does not exploit such items to a significant extent. This presents an opportunity to compare the wear fabrics of two papionin species in which terrestrial foraging is normative behavior, but for which the con- stituents of the diet differ quite dramatically.

For this study, molar microwear was examined in specimens of P ursinus that were collected during the mid to late dry season of northern South Africa. These data are compared to those recorded by TEAFORD (1993) for Theropithecus gelada. By comparing two terrestrial foragers, it can be ascertained whether feeding on the ground itself produces distinctive microwear features not seen in arboreal forms (WALKER et al., 1978; UNGAR & TEAFORD, 1996).

MATERIALS AND METHODS

BABOON SAMPLES: PROVENANCE AND DIET

Maxillary second permanent molars (M2s) of ten wild-shot specimens (five males and five females) of Papio ursinus from the Northwest and Northern Provinces of South Africa were examined by scanning electron microscopy (SEM) for occlusal microwear. The sample is

Dental Microwear in Papio ursinus 56 l

nbur~

Fig. 1. Geographic provenance of the study sample. Three specimens were collected from Messina, five from the D'nyala Reserve near Ellisras, and two from the Rustenburg Provincial Nature Reserve.

housed at the Transvaal Museum, Pretoria, South Africa. Seven of the specimens were collected in July, while the other three were collected later during the winter dry season. Five individuals (two males and three females) are from the D'nyala Game Reserve, Ellisras; two (one male and one female) are from the Rustenburg Provincial Nature Reserve, and three (two males and one female) were taken from the farm Samaria, near Messina (Fig. 1).

The regions from which the specimens derive are broadly characterized as bushveld. The habitat surrounding Messina has been further described as "Mopaniveld" (ACOCKS, 1988, veld type No. 15), in which short, Shrubby mopane trees (Colophospermum mopane) and sometimes sparse, tufted grasses compose the dominant vegetation. Within this region, baboons frequent mountainous, riverine, and broken vegetational areas (STOLTZ & KE1TH, 1973). The D'nyala Game Reserve (Ellisras) is a semi-arid scrub woodland (MEADOWS, 1985), which has been referred to as "Mixed Terminalia-Dichapetalum Veld" by ACOCKS (1988, veld type No. 18b). The area of the Rustenberg Provincial Nature Reserve is described as "Sour Bushveld" by ACOCKS (1988, veld type No. 20), characterized by rocky valleys in which Acacia caffra and Protea caffra dominate along with a floristically rich grassveld (COETZEE, 1975). A feature of all the regions from which the baboons were collected is that the winters are dry with little or no rainfall (STOLTZ & SAAYMAN, 1970; MEADOWS, 1985; WHITEN et al., 1987). For example, the Rustenberg Provincial Nature Reserve receives an average of some 700-800 mm of annual rainfall, of which 85% to 90% accumulates between October and March (COETZEE, 1975).

During the dry season in these areas, Papio ursinus has been observed to frequently ingest hypogeous tubers, bulbs, and roots (WH1TEN et al., 1987, 1991; BYRNE et al., 1993). Indeed, in certain groups of chacma baboons, the collection of underground food items may account for upwards of 90% of feeding observations during the dry season (WHITEN et al., 1987). In the Rustenberg Provincial Nature Reserve, Eriospermum bulbs comprise the vast bulk of Papio's winter diet (H. GLEN & D. HARDY, pers. comm.). Mastication of these items is undoubtedly accompanied by a substantial amount of grit from the sandy soils that dominate in these areas (ACOCKS, 1988).

DENTAL MICROWEAR PROTOCOL

For each Papio ursinus specimen, a single molar (M 2) was examined. One Phase I and one

562 D.J. DAEGL1NG & F. E. GRINE

Fig. 2. Schematic right upper molar of Papio ursinus. Shaded regions indicate the wear facets sampled in this study. Facets are numbered according to the system of KAY and HIIEMAE (1974). Phase I occlusal surfaces are represented by facets 1, 3, 5 and 6; Phase II occlusal surfaces are represented by facet 9. See text for explanation.

Phase II facet (KAY & HIIEMAE, 1974) were analyzed for each tooth (Fig. 2). Extensive dentine exposure on most specimens made it impossible to examine the same Phase I facet on all; thus, facet 1 was examined on four specimens, facet 5 on three specimens, facet 3 on two specimens, and facet 6 on one specimen. On all molars, Phase II facet number 9 retained enamel and was suitable for analysis. For each facet, the frequencies of pits and scratches were determined from micrographs recorded at 100x magnification. Scratch width, pit length, and pit width were measured on 200x micrographs. Preparation of specimens and SEM procedures follow GRINE'S (1986) protocol.

RESULTS AND DISCUSSION

FORMATION OF MICROWEAR FEATURES

Microwear features were measured on occlusal surfaces (= wear facets) that correspond to distinct events during mastication. Wear on the lingual slopes of maxillary molar cusps are produced during superior and medial movement of mandibular cusps into centric occlusion (Phase I), while wear produced on the buccal aspects of upper molars reflects the inferior and medial action of mandibular cusps out of centric occlusion (Phase II) (GmNE, 198 I). These two masti- catory phases have been related to shearing and grinding activity, respectively. The degree to which Phases I and II wear fabrics reflect these distinctive modes of tood breakdown, however, is dependent on the nature of species-specific occlusal relief at various stages of attrition.

MICROWEAR FEATURE FREQUENCIES

The number of microwear features per mm 2 on Papio ursinus molars is nearly the same on Phase I and II facets, with the average Phase II incidence exceeding that for Phase I by only about 1% (Table 1). This contrasts markedly with the relative Phase I - P h a s e II frequencies

Dental Microwear in Papio ursinus

Table 1. Papio ursinus M 2 microwear features per mm 2.

563

Facet X SD Observation range I 349.8 81.9 207--468

II 353.4 144.0 201-708

recorded for Pan troglodytes (GORDON, 1982), Australopithecus africanus, and Paranthropus robustus (GRINE, 1986), in which the Phase II incidences were greater by between about 21% (Australopithecus) and 46% (Pan). The P ursinus Phase I mean is somewhat greater than the corresponding value for Australopithecus (290.4 per mm2), but lower than those of Paranthropus (437.6) and Pan (397.0); the Papio Phase II average exceeds those for both Australopithecus (230.2) and Paranthropus (323.9), but is substantially lower than the Pan mean (736.0) recorded by GORDON (1982).

Pits comprise some 43% of the wear features on both Phase I and Phase II facets of P. ursinus molars (Table 2). The close correspondence of Phases I and II pitting frequencies in P. ursinus contrasts with the condition observed in many other primate species in which these facets have been examined (i.e. Australopithecus africanus, Paranthropus robustus, Pan troglodytes, Piliocolobus badius, Cebus apella, C. nigrivittatus, C. capucinus, and Hapalemur griseus) (GORDON, 1982; TEAFORD, 1985, 1986; GRINE, 1986; DAEGLING c~; GRINE, 1994). In these taxa, Phase II pitting frequencies exceed the corresponding Phase I incidences by between 12% (Cebus apella) and 58% (Pan troglodytes). The closest correspondence of Phases I and II frequencies among extant species has been recorded for Colobus guereza, in which the incidences differ by only 1.1% (TEAFORD, 1986). An apparently anomalous result for Alouatta palliata (a higher Phase I pitting frequency) was suggested by TEAFORD and WALKER (1984) as being attributable to the absolutely low occlusal feature densities in this species. Higher Phase I pitting frequencies have been recorded also for a small sample (n=4) of Gigantopithecus blacki teeth (DAEGLING & GRINE, 1994); this discrepancy may be attributable to the small number of teeth examined, and/or to the inclusion of one P4 and two M3s in that sample. Thus, P ursinus is unusual (but not unique) among extant primates in exhibiting a very close correspondence in the pitting incidences on Phase I and Phase II facets.

The significance of the similar pitting incidences on Phase I versus Phase II facets in P. ursinus is not immediately apparent. The ingestion of large amounts of grit is perhaps responsible; however, Colobus guereza exhibits comparable pitting incidences, yet it seems improbable that grit comprises a significant portion of ingested material in this taxon's diet. A second possibility is that the relative inclination of Phase I and Phase II facets in the sample is a contributing factor, although the limited comparative data would seem to indicate that relatively high Phase I pitting incidences (relative to those on Phase II facets) is neither characteristic of nor peculiar to taxa with bilophodont teeth. Existing microwear data on fossil hominids also suggest that the relationship between facet inclination and microwear feature incidences is, at best, equivocal (GRINE, 1986).

Table 2. Percentage incidence of occlusal pitting on Papio ursinus M2s. Facet X SD Observation range 1 43.1 11.1 25.0-61.0

11 43.3 11.6 20.9-58.5

564 D.J . DAEGLING & E E. GRINE

Table 3. Phase II facet pitting frequencies (%) recorded for extant and extinct primates.

Taxon Frequency Source

Cercocebus albigena 55.2 Paranthropus robustus 48.5 Cebus apella 45. l Papio ursinus 43.3 Pongo pygmaeus 42.5 Sivapithecus sivalensis 35.3 Australopithecus africanus 30.8 Theropithecus brumpti 29.5 Gigantopithecus blacki 29.0 Hapalernur griseus 28.8 Pan troglodytes 24.2 Cebus nigrivittatus 16.2 Theropithecus oswaldi 14.0 Piliocolobus badius 12.6 Cebus capucinus I 1.7 Colobus guereza 9.8 Theropithecus gelada 8.8 Alouatta palliata 8.8 Gorilla gorilla 3.4

TEAFORD 8~ WALKER (1984, Fig. 5)* GRINE (1986, Table 5) TEAEORD (1985, Table l)* Present study TEAFORD 8,:. WALKER (1984, Fig. 5)* TEAFORD & WALKER (1984, Fig. 5)* GRINE (1986, Table 5) TEAEORD (1993, Table 12.2) DAEGL1NG & GR1NE (1994, Table 2) DAEGLING & GRINE (1994, Table 2) TEAEORD 8s WALKER (1984, Fig. 5)* TEAFORD (1985, Table 1)* TEAFORD (1993, Table 12.2) TEAEORD (1986, Table 2)* TEAEORD (1985, Table l)* TEAEORD (1986, Table 2)* TEAFORD (1993, Table 12.2) TEAFORD 8~ WALKER (1984, Fig. 5)* TEAFORD 8,~ WALKER (1984, Fig. 5)*

*Data recorded here have been recalculated by M. TEAFORD (pers. comm.) from published values that employed a length:width ratio of 10:1 to a ratio of 4:1 in the definition of a "pit."

The mean Phase II occlusal pit t ing f requency of 43.3% recorded for Papio ursinus M2s is

among the highest recorded for l iv ing and extinct pr imate taxa (Table 3). In the present study,

pits and scratches were scored independent ly by subjec t ive determinat ion fo l lowing the method

uti l ized by GORDON (1982), GRINE (1986), and DAEGLING and GR~NE (1994). GRINE (1986)

determined that features thus recognized as "pi ts" possessed a length:width ratio be tween 1:1

and about 4:1. The data reported by TEAFORD and WALKER (1984) and TEAFORO (1985, 1986)

for a variety o f pr imates employed a length:width ratio o f 10:1 to def ine whether a feature was

classif ied as a scratch or pit, such that the pitting f requencies reported in those studies cannot be

compared to results for Papio and Theropithecus. The f requencies recorded in Table 3 for the

pr imate species examined by TEAFORD and WALKER (1984) and TEAFORD (1985, 1986) have

been adjusted (M. TEAFORD, pers. comm.) so that pits are def ined as features with a length:

width ratio o f f rom 4:1 to 1 : 1.

The pit t ing f requency of the P. ursinus sample is reminiscent o f hard-object feeders such as

Cebus apella (TERBORGH, 1983), and the general ly f rugivorous Pongo pygmaeus, which is a

strongly opportunist ic forager that includes substantial amounts of bark and even earth in its diet

Table 4. Microwear feature dimensions in Papio ursinus (/~m).

N X SD SE 95% C.L.

Scratch width Phase I 10 3.15 0.42 0.13 2.84--3.45 Phase Ii 10 3.15 0.59 0.19 2.72-- 3.57

Pit width Phase I 10 8.64 1.86 0.59 7.31 --9.97 Phase 11 10 10.72 4.13 1.31 7.76-- 13.67

Pit length Phase I l0 16.10 3.80 1.20 13.38-18.83 Phase II 10 17.28 5.12 1.62 13.62--20.94

Analysis of variance reveals no significant difference for scratch breadth and pit length between Phase ! and Phase I1 surfaces. Pit width, however, differs significantly (p<.01) between Phase I and Phase II wear facets.

Dental Microwear in Papio ursinus 565

(MAcKINNON, 1974; GALDIKAS, 1988). Pitting incidences recorded for Theropithecus gelada (TEAFORD, 1993) are most similar to those of Colobus guereza and Alouatta palliata, both of which are highly folivorous. The pitting frequency of extinct T. oswaldi is somewhat higher than that of T. gelada, being most similar to the incidences recorded for Piliocolobus badius and Cebus nigrivittatus. These species have diets which include fruits as well as invertebrates and leaves (MARSH, 1981; ROBINSON, 1986). The pitting frequency of the other extinct papionin, T. brumpti, falls closer to the Papio value (29.5% versus 43.3%), but its nearest neighbors (Gigantopithecus and Australopithecus) are both extinct. As noted by TEAFORD (1993), a living primate analogue for T. brumpti may not exist (or, at least, it has not been sampled). The closest living primate to T. brumpti in terms of its occlusal pitting frequency is Hapalemur griseus, which subsists on the leaves and young shoots of bamboo (PETTER & PEYRIERAS, 1970).

MICROWEAR FEATURE DIMENSIONS

The average widths of microwear scratches on Phase I and Phase II facets of Papio ursinus MZs are identical, whereas the averages for pit width and pit length are larger on Phase II facets than on Phase I facets, with the difference in pit width achieving statistical significance (Table 4). Microwear scratches are distinctly broader, and pits are larger (in both breadth and length) on Phase II facets of Papio ursinus in comparison to the feature dimensions recorded by TEAFORD (1993) for three species of Theropithecus (Fig. 3). The magnitude of these differences is even more apparent when they are considered in relation to the dimensions recorded for other primate species, where Papio and Theropithecus occupy different extremes of the microwear spectrum (Fig. 4). Indeed, the Papio ursinus specimens examined in this study possess among the largest microwear features recorded for any living or fossil primate species.

Papionin Microwear Feature Dimensions (Phase II)

Scratch Width 7. oswaldi | T. brumpti 4k T. ge;ada r m. ursinus

Pit Width T. oswaldi - - I - T. brumpti i I T. gelada P. ursinus

Pit Length T. oswaldi T. brumpti T. gelada I P. ursinus I

' ' ' ' ' ' ' ' ' ' ' ' ' '

0 2 4 6 8 10 4 16 1 2 24 #m

Fig. 3. Papio and Theropithecus microwear feature dimensions. Means (vertical lines), one standard error (bars) and one standard deviation (horizontal lines) are shown. Papio feature dimensions are significantly larger than in all three species of Theropithecus by the Games and Howell multiple comparisons test (SOKAL & ROOF, 1995; p<.05 for Papio ursinus-T, gelada contrasts of pit length and width and for Papio ursinus-T, brumpti contrast of pit width; p<.01 for all other Papio-Theropithecus comparisons). Therop- ithecus data from TEAFORD (1993).

566 D.J . DAEGLING & E E. G R I N E

It should be noted, however, that TEAFORD (1993, pers. comm.) measured feature dimensions from 500x micrographs, while the data recorded in this study and by GRINE (1986; DAEGL1NG & GR1NE, 1994) are from micrographs taken at 200x. Although in both cases the measurements were calibrated correctly, the possibility of bias exists. Because the smallest features on 500x micrographs are likely to be undersampled in 200x micrographs, it is possible that smaller field micrographs will systematically yield smaller mean feature dimensions. While we cannot rule out this potential source of error, its effects may be negligible for at least two reasons. First, the

Microwear Scratch Width (Phase II)

Cercocebus albigena - - - ~ l l - -

Papio urainua i ~ Cebus apella

Pongo pygmaeus - - ~ Pan troglodytes

Paranthropua robustus Sivapithecus sivalensis

Cebus capucinus Gorilla gorilla

Piliocolobus badius Colobus guereza - - ~

Australopithecus africanus -~-

Cebus nigrivittatus Theroplthecus gelada

Theropithecue brumpti ~[ Theroplthecua oswaldi ~4}

I I I I I I I 0 1 2 3 4 5 6

I I 7 8 ~tm

Microwear Pit Width (Phase II)

Papio ursinus J

Cercocebus a/bigeoa J Cebus nigrivittatus

Cebus apella Paranthropus robustus

Pongo pygmaeus

Pan troglodytes - - I ~ l ~ ' - - Piliocolobus badius I

Gorilla gorilla I Colobus guereza - - ~ J ~ - -

Sivapithecus sivalensia Cebua capucinus

Australopithecus africanus

Theroplthecue gelada Q Theropithecus brumptl ,

Theropithecus oewaldi ~1

i I I I I 0 i 0 2 4 6 8 1 12

I I 14 16i~m

Fig. 4. Comparison of Papio and Theropithecus microwear feature widths with those recorded for other primate taxa. Means (vertical lines), one standard error (bars), and one standard deviation (horizontal lines) are shown. Theropithecus data from TEAFORD (1993); data for other extant anthropoids and for Sivapithecus provided by TEAFORD (pers. comm.); data for Australopithecus and Paranthropus from GRINE (1986).


taxa that were examined at 200x do not consistently yield higher feature dimensions than those studied at 500x (Fig. 4). Second, GOROON's (1982) and TEAFORD and WALKER'S (1984) feature width data from chimpanzee molars are comparable (i.e. their means are within one standard deviation of each other), despite the fact that GORDON used magnifications of only 120 to 140x. Furthermore, while the potential for "resolution effect" to influence morphometric estimates is well-recognized in the field of stereology, its effect is most problematic in the measurement of surface areas and volumes, and is not particularly acute for linear measures such as those used here (WEIBEL, 1979). Restricting comparison to microwear feature widths also serves to reduce such bias (TEAFORD 8Z WALKER, 1984).

MICROWEAR PITTING FREQUENCY AND SIZE

Examination of the relationship between microwear pit size and frequency (Fig. 5) reveals that all three Theropithecus species display fairly small pits (i.e. their average width is less than 5 to 6/xm, about the average prism diameter of anthropoid primates) that occur with relatively low frequency (i.e. below 33%). Papio ursinus, by contrast, occupies the opposite end of the spectrum, displaying a high frequency of large pits (Fig. 5). This wear profile of P ursinus, although very close to that of Cercocebus albigena, serves to differentiate it somewhat from the profiles of two other extant durophagous primates, Cebus apella and Pongo pygmaeus. Among fossil primate taxa, it distinguishes Papio ursinus from Paranthropus robustus, whose profile of pitting frequency and size closely approximates those of Pongo pygmaeus and Cebus apella.

Several implications for comparative microwear analyses emerge from this study. First, it appears that terrestrial foraging alone does not produce a microwear "signature" among primates, since the two extant terrestrial foragers that have been sampled are dramatically different in the context of other species. Instead, differences in food choice as well as foraging behavior have produced microwear differences that overwhelm any general effect that terrestrial feeding

1 2 -

1 0 -

~ 8 - -

6 -

:~ 4-

�9 R ursinus

�9 C. albigena

�9 A. palliata �9 C. nigrivittatus �9 apella

�9 R robustus

�9 R troglodytes �9 R pygmaeus G. gorilla

�9 �9 R badius �9 C. guereza �9 S. sivalensis

�9 C. capucinus �9 africanue

�9 T. gelada

�9 Z oswaldi �9 7~ brumpti

.... ~ I ~ I ~ I ~ I ~ I ~ I 1 0 2 0 3 0 4 0 5 0 6 0

Mean Percentage of Pits

Fig. 5. Relationship between average pit width and the proportion of pits in various anthropoid primates. Sources of data are as Figure 4. Note that Papio ursinus and Theropithecus gelada occupy different ends of this spectrum.

568 D.J. DAEGL1NG & E E. GR1NE

might entail. The fact that Papio and Theropithecus occupy opposite extremes of the microwear spectrum (Figs. 4 - 6 ) suggests that microwear fabrics cannot be expected to differentiate arboreal or terrestrial feeding habits unless a number of confounding variables can be controlled.

Within the present Papio ursinus sample, severe dental attrition is obvious at a macroscopic level. This is reflected microscopically in the sizes of the wear features and the relative abundance of enamel pitting, both of which contrast quite dramatically with the microwear fabric of T. gelada (Fig. 6). While the presence of numerous, large pits is generally reflective of durophagy among arboreal primates (e.g. Cercocebus albigena, Cebus apella, Pongo pygmaeus), it is not clear that hard food items are the causal agents of the microwear fabrics seen in the Papio specimens examined in this study. Compared to the microwear patterns exhibited by arboreal, durophagous primates, the wear fabric of P ursinus comprises features that are large (both absolutely and relatively) in comparison to the proportion of pits.

The ingestion of hypogeous tubers, bulbs, and roots is a frequent feeding behavior of Papio ursinus during the dry season in the Northwest and Northern Provinces (WHITEN et al., 1987, 1991; BYRNE et al., 1993). Many of the above-ground food items utilized by Papio during the dry season in the Northwest and Northern Provinces of South Africa may be relatively tough (PETERS & MAGUmE, 1981), although field observations of baboons give little indication that they exploit a great proportion of particularly "hard" items at any time of the year. For example, PETZRS and MAGUIRE (1981) report that baboons do not eat marula nuts or Tylosema beans (pre- sumably because they may be "beyond their dental capabilities"), and that most seeds, including those of Grewia, pass through their digestive tract intact. It seems unlikely, therefore, that the structural properties of the food items themselves are solely responsible for the wear fabrics

Fig. 6. Representative scanning electron micrographs from Phase II surfaces of Papio ursinus (a) and Theropithecus gelada (b) M 2 s. The scale is the same for both micrographs.


seen on baboon molars during the dry season. However, mastication of hypogeous items is undoubtedly accompanied by a substantial amount of exogenous grit. The molar microwear fabric of the Papio ursinus sample may be a direct effect of this non-food agent, although we cannot rule out the possibility that the food items themselves are making a significant contribution to the wear profile.

Exogenous grit has been hypothesized to be an important agent in the formation of microwear features in animals that forage terrestrially (WALKER, 1976; UNGAR, 1990), and TEAFORD (1993) has implicated soil or sand particles in the formation of the few pits that are found on gelada molars. While exogenous grit may form the occasional pit on gelada molars, the majority of wear features on these molars are likely caused by the abundant opaline phytoliths found in grasses (WALKER et al., 1978).

IMPLICATIONS FOR DIETARY INFERENCE IN FOSSIL PRIMATES

These results may help to clarify dietary inferences drawn from microwear data in extinct taxa. For example, DAEGLIN6 and GRINE (1994) have suggested that Gigantopithecus blacki was specialized for neither hard-object feeding nor folivory as practiced by living primates. The heavy pitting encountered on Papio molars is quite unlike the pattern observed in Gigantopithecus. If exogenous grit is indeed the principal agent of pitting on baboon teeth, as seems likely, an additional inference may be drawn that Gigantopithecus did not exploit hypogeous items to a significant degree.

In terms of microwear feature size and the relative proportion of pits versus scratches, the wear pattern of Papio ursinus is not altogether different from that documented for Paranthropus robustus (GRINE, 1986). On these data alone, however, it is probably unwise to conclude that such similarities might be due to ingestion of grit by these fossil hominids. Not only does Paranthropus resemble several arboreal hard-object feeders more than it does Papio (Figs. 4 & 5), but in the relationship of feature incidences and dimensions between Phase I and Phase II facets, Papio and Paranthropus are also dissimilar.

SUMMARY AND CONCLUSIONS

Molar microwear was quantified for a sample of Papio ursinus collected during the dry season in the Northwest and Northern Provinces, South Africa. These data were compared to those from TEAFORD'S (1993) study of modern and fossil Theropithecus. Higher incidences of enamel pitting and larger feature dimensions distinguish Papio from Theropithecus. While the presence of numerous, large pits is usually held to be indicative of hard-object feeding, it is suggested that ingestion of large amounts of exogenous grit is the causal agent in the formation of the microwear fabric of Papio ursinus as these baboons are known to exploit hypogeous foods during the dry season.

It has been suggested that terrestrial foraging produces distinctive microwear fabrics compared to feeding in an arboreal milieu. While the premise of the hypothesis is sound, terrestrial foraging obviously entails distinctive food selection and feeding behavior among different species. Both grit (soil and sand) and silicas (opal phytoliths) may be encountered in relative abundance by a ground-dwelling primate, and while both of these agents can be expected to participate in the formation of microwear, their respective impacts on microwear fabrics may be dramatically different.

570 D.J. DAEGLING & E E. GRINE

Ackowledgments. We thank FRANC1S THACKERAY, Transvaal Museum, Pretoria, for permission to examine the dental specimens used in this study. We are grateful to MARK TEAFORD, who generously provided his data on a variety of primate species, as well as the Theropithecus gelada micrograph. We thank L. BETTI-NASH for her expert preparation of the illustrations.

REFERENCES

ACOCKS, J. E H. 1988. Veld types of south Africa. Memoirs Botanical Survey South Africa, 57 (I-X): 1 - 146. BYRNE, R. W.; WHITEN, A.; HENZl, S. E; McCULLOCH, E M. 1993. Nutritional constraints on mountain

baboons (Papio ursinus): implications for baboon socioecology. Behav. Ecol. Sociobiol., 33: 233-246. COETZEE, B. J. 1975. A phytosociological classification of the Rustenburg Nature Reserve. Bothalia, 11:

561-580. COVERT, H. H.; KAY, R. E 1981. Dental microwear and diet: implications for determining the feeding

behaviors of extinct primates, with a comment on the dietary patterns of Sivapithecus. Amer. J. Phys. Anthropol., 55:331-336.

DAEGLING, D. J.; GRINE, E E. 1994. Bamboo feeding, dental microwear and diet of the Pleistocene ape Gigantopithecus blacki. S. Afr. J. Sci., 90: 527-532.

DUNBAR, R. I. M. 1977. Feeding ecology of gelada baboons: a preliminary report. In: Primate Ecology, CLUTTON-BROCK, Z. H. (ed.), Academic, New York, pp. 251-273.

DUNBAR, R. 1. M.; DUNBAR, E. P. 1974. Ecological relations and niche separation between sympatric terrestrial primates in Ethiopia. Folia Primatol., 21 : 36-60.

FLEAGLE, J. G. 1988. Primate Adaptation and Evolution. Academic, New York. GALDIKAS, B. M. E 1988. Orangutan diet, range, and activity at Tanjung Puting, central Borneo. Int. J.

Primatol., 9 :1 -35 . GORDON, K. D. 1982. A study of microwear on chimpanzee molars: implications for dental microwear analy-

sis. Amer. J. Phys. Anthropol., 59: 195-215. GORDON, K. D. 1984. Hominoid dental microwear: complications in the use of microwear analysis to

detect diet. J. Dent. Res., 63: 1043-1046. GORDON, K. D., WALKER, A. C. 1983. Playing 'possum: a microwear experiment. Amer. J. Phys. Anthropol.,

60: 109-112. GRINE, E E. 1981. Trophic differences between 'gracile' and 'robust' australopithecines: a scanning electron

microscope analysis of occlusal events. S. Afr. J. Sci., 77: 203-230. GRINE, E E. 1984. Deciduous molar microwear of South African australopithecines. In: Food Acquisition

and Processing in Primates, CHIVERS, D. J.; WOOD, B. A.; BILSBOROUGH, A. (eds.), Plenum, New York, pp. 525-534.

GRINE, E E. 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J. Human Evol., 15: 783-822.

GRINE, E E. 1987. Quantitative analysis of occlusal microwear in Australopithecus and Paranthropus. Scanning Microsc., 1 : 647-656.

GRINE, E E., KAY, R. E 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature, 333: 765-768.

HALL, K. R. L. 1963. Variations in the ecology of the chacma baboon, Papio ursinus. Syrup. Zool. Soc. Lond., 10: 1-28.

HAMILTON, W. J.; BUSKIRK, R. E.; BUSKIRK, W. H. 1978. Omnivory and utilization of food resources by chacma baboons, Papio ursinus. Amer. Naturalist, 112:911-924.

IWAMOTO, T. 1979. Feeding ecology. In: Ecological and Sociological Studies of Gelada Baboons, KAWAI, M. (ed.), Kondasha, Tokyo, pp. 279-330.

IWAMOTO, T.; DUNBAR, R. 1. M. 1983. Thermoregulation, habitat quality and the behavioral ecology of gelada baboons. J. Anita. Ecol., 52: 357-366.

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

KAY, R. F.; COVERT, H. H. 1983. True grit: a microwear experiment. Amer. J. Phys. Anthropol., 61: 33-38. KAY, R. E; GRINE, E E. 1988. Tooth morphology, wear and diet in Australopithecus and Paranthropus

from southern Africa. ln: Evolutionary History of the "Robust" Australopithecines, GRINE, E E. (ed.), Aldine de Gruyter, New York, pp. 427-447.


KAY, R. E; HnEMAE, K. M. 1974. Jaw movement and tooth use in recent and fossil primates. Amer. J. Phys. Anthropol., 40: 227-256.

KELLEY, J. 1990. Incisor microwear and diet in three species of Colobus. Folia Primatol., 55: 73-84. MAcKmNON, J. 1974. The behaviour and ecology of wild orangutans (Pongo pygmaeus). Anim. Behav.,

22: 2-74. MARSH, C. W. 1981. Diet choice among red colobus (Colobus badius rufomitratus) on the Tana River,

Kenya. Folia PrimatoL, 35:147-178. MEADOWS, M. E. 1985. Biogeography and Ecosystems of South Africa. Juta, Cape Town. PETERS, C. R.; MAGUIRE, B. 1981. Wild plant foods of the Makapansgat area: a modern ecosystems ana-

logue for Australopithecus africanus adaptations. J. Human Evol., 10:565-583. PETTER, J. J.; PEYRIERAS, A. 1970. Observations ecoethologiques sur les lemuriens malagaches de genre

Hapalemur. Terre Vie, 3: 356-382. ROBINSON, J. G. 1986. Seasonal variation in the use of time and space by the wedge-capped capuchin

monkey, Cebus olivaceus: implications for foraging theory. Smithsonian Contrib. Zool., 431:1-60. RYAN, A. S. 1981. Anterior dental microwear and its relationship to diet and feeding behavior in three

African primates (Pan troglodytes troglodytes, Gorilla gorilla gorilla, and Papio hamadryas). Primates, 22: 533-550.

SOr,:AL, R. R.; ROHLF, E J. 1995. Biometry (3rd ed.). W. H. Freeman, New York. STOLTZ, L. P.; KEITH, M. E. 1973. A population survey of chacma baboon in the northern Transvaal. J.

Human Evol., 2: 195-212. STOLTZ, L. P.; SAAVMAN, G. S. 1970. Ecology and behaviour of baboons in the northern Transvaal. Ann.

Transvaal Mus., 26:99 - 143. TEAFORD, M. E 1985. Molar microwear and diet in the genus Cebus. Amer. J. Phys. Anthropol., 66: 363-370. TEAFORD, M. E 1986. Dental microwear and diet in two species of Colobus. In: Primate Ecology and

Conservation, ELSE, J.; LEE, P. (eds.), Cambridge Univ. Press, Cambridge, pp. 63-66. TEAFORD, M. F. 1993. Dental microwear in extant and extinct Theropithecus: preliminary analyses. In:

Theropithecus: The Rise and Fall of a Primate Genus, JABLONSKI, N. (ed.), Cambridge Univ. Press, Cambridge, pp. 331-349.

TEAFORD, M. E 1994. Dental microwear and dental function. Evol. Anthropol., 3: 17-30. TEAFORD, M. E; GLANDER, K. E. 1991. Dental microwear in live, wild-trapped Alouatta from Costa Rica.

Amer. J. Phys. Anthropol., 85: 313-319. TE~ORD, M. E; O'r O. J. 1989. In vivo and in vitro turnover in dental microwear. Amer. J. Phys. Anthropol.,

80: 447-460. TEAFORD, M. E; PASTOR, R. E; GLANDER, K. E.; UNGAR, E S. 1994, Dental microwear and diet: Costa

Rican AIouatta revisited. Amer. J. Phys. Anthropol. (suppl.), 18: 194. TEAFORD, M. F.; ROBINSON, J. G. 1989. Seasonal or ecological differences in diet and molar microwear in

Cebus nigrivittatus. Amen J. Phys. Anthropol., 80:391-401. TEAFORD, M. E; RUNESTAD, J. A. 1992. Dental microwear and diet in Venezuelan primates. Amer. J. Phys.

Anthropol., 88: 347-364. TEAFORD, M. E; WALKER, A. C. 1984. Quantitative differences in dental microwear between primate species

with different diets and a comment on the presumed diet of Sivapithecus. Amer. J. Phys. Anthropol., 64: 191-200.

TERBORGH, J.W. 1983. Five New Worm Primates: A Study in Comparative Ecology. Princeton Univ. Press, Princeton, New Jersey.

UNGAR, P. S. 1990. Incisor use and microwear in Cebus olivaceous and Alouatta seniculus. Amen J. Primatol., 20: 43-50.

UNGAR, E S. 1994. Incisor microwear of Sumatran anthropoid primates. Amer. J. Phys. Anthropol., 94: 339-363.

UNGAR, P. S.; GRINE, E E. 1991. Incisor size and wear in Australopithecus africanus and Paranthropus robustus. J. Human Evol., 20: 313-340.

UNCAR, P. S.; TEAFORD, M. E 1996. Preliminary examination of non-occlusal dental microwear in anthropoids: implications for the study of fossil primates. Amer. J. Phys. Anthropol., 100:101 -113.

UNGAR, E S.; TEAFORD, M. E; GLANDER, K. E.; PASTOR, R. F. 1995. Dust accumulation in the canopy: a potential cause of dental microwear in primates. Amer. J. Phys. Anthropol., 97: 93-99.

WALKER, A. C. 1981. Diet and teeth: dietary hypotheses and human evolution. Phil. Trans. R. Soc. Lond., 292(B): 57-64.

572 D.J . DAEGLING & E E. GRINE

WALKER, A. C.; HOECK, H. N.; PEREZ, L. 1978. Microwear of mammalian teeth as an indicator of diet. Science, 201: 808-810.

WALKER, P. S. 1976. Wear striations on the incisors of cercopithecus monkeys as an index of diet and habitat preference. Amer. J. Phys. Anthropol., 45: 299-308.

WEIBEL, E. R. 1979. Stereological Methods, Vol. 1: Practical Methods for Biological Morphometry. Academic, London.

WHITEN, A.; BYRNE, R. W.; BARTON, R. A.; WATERMAN, P. G.; HENZl, S. P. 1991. Dietary and foraging strate- gies of baboons. Phil. Trans. Royal Soc. Lond., B334:187-198.

WHITEN, A.; BYRNE, R. W.; HENZI, S. P. 1987. The behavioral ecology of mountain baboons. Int. J. Primatol., 8: 367-388.

- - Received: August 6, 1998; Accepted: May 22, 1999

Authors' Names and Present Addresses: DAVID J. DAEGL1NG, Department of Basic Medical Sciences, California College ~)f Podiatric Medicine, 1210 Scott Street, San Francisco, California 94115, U. S. A. e-mail: [email protected]; FREDERICK E. GRINE, Departments of Anthropology and Anatomical Sciences, State University of New York, Stony Brook, New York 11794, U. S. A.

Documents

Terrestrial foraging and dental microwear in Papio ursinus