The late Early Pleistocene suid remains from the paleoanthropological site of Buia (Eritrea):...

Palaeogeography, Palaeoclimatology, Palaeoecology 431 (2015) 26–42

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Palaeogeography, Palaeoclimatology, Palaeoecology

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The late Early Pleistocene suid remains from the paleoanthropologicalsite of Buia (Eritrea): Systematics, biochronology andeco-geographical context

Tsegai Medin a,b, Bienvenido Martínez-Navarro a,c,d,⁎, Florent Rivals a,c,d, Yosief Libsekal b, Lorenzo Rook e

a IPHES, Institut Català de Paleoecologia Humana i Evolució Social, Campus Sescelades URV (Edifici W3), 43007 Tarragona, Spainb National Museum of Eritrea, P.O. Box 5284, Asmara, Eritreac ICREA, Barcelona, Spaind Area de Prehistoria, Universitat Rovira i Virgili (URV), Avda. Catalunya 35, 43002 Tarragona, Spaine Dipartamento di Science della Terra, Università degli Studi di Firenze, Via G. La Pira, 4, 50121 Firenze, Italy

⁎ Corresponding author at: IPHES, Institut Català de PaSocial, Campus Sescelades URV (Edifici W3), 43007696507513.

E-mail address: [email protected] (B. Ma

http://dx.doi.org/10.1016/j.palaeo.2015.04.0200031-0182/© 2015 Elsevier B.V. All rights reserved.

a b s t r a c t
a r t i c l e i n f o
Article history:Received 22 October 2014Received in revised form 16 April 2015Accepted 21 April 2015Available online 30 April 2015

Keywords:BuiaEritreaSuid remainsMicrowearEarly Pleistocene

The fossiliferous late Early Pleistocene deposits of the Buia Basin (dated to c. 1Ma) at the Danakil depression, con-tain three different suid species (Kolpochoerus olduvaiensis, Kolpochoerus majus, and Metridiochoerus modestus).These suid taxa are morphologically evolved and are found in association with a diverse large vertebrate faunalassemblage, including the genusHomo and a rich accumulation of Acheulean tools. The anatomic, biometric,mor-phometric anddentalmicrowear analyses, show significant data of dietary traits, habitat and evolutionary chang-es. In suids, despite their omnivorous diets, microwear study can play a significant role in understanding dietaryhabits. The results of our study show morphological distinction between the three suid species. Conversely, themicrowear patterns recorded on the dental surfaces show overlapping of ecological niches among the species.We believe that their opportunistic feeding and rapid reproduction process might have sustained their survivalwithin themosaic environments of the Buia Basin in competition with other faunas (other ungulates, carnivoresand monkeys) and hominins.

© 2015 Elsevier B.V. All rights reserved.

1. Introduction

The African Plio-Pleistocene suids belong to a limited number of lin-eages that were diversifying fairly rapidly and are thus of high value forbiochronology and correlations (Leakey, 1942, 1943; White and Harris,1977; Cooke and Wilkinson, 1978; Harris and White, 1979; Pickford,1994, 2012, 2013; Geraads, 1993, 2004; van der Made, 1996, 1999;Cooke, 1997; Sahnouni et al., 2004; Bishop et al., 2006; Bishop, 2010a,2010b; among others). The contribution of research on suids offeredcrucial support in dating and depicting paleoecological reconstructionsat various Plio-Pleistocene sites from Africa, Europe and Asia. Accordingto current knowledge, the main radiation and the development of themost extreme specializations of pigs occurred in Africa. The fossiliferouslate Early Pleistocene stratigraphic successions of Buia (Eritrean DanakilDepression) enhanced our knowledgewith the record of threemorpho-logically evolved suid species coexisting in the same paleoecologicalhabitat.

leoecologia Humana i EvolucióTarragona, Spain. Tel.: +34

rtínez-Navarro).

The site of Buia is located (Fig. 1) about 110 km south of the port cityof Massawa, in the Danakil depression of Eritrea, at the northernmostpart of the Eastern African Rift Valley, close to the Red Sea. The Homo-bearing deposits of the Buia sedimentary succession (Abbate et al.,1998, 2012;Ghinassi et al., 2009; Papini et al., 2014) yielded fossils of var-ious macro- and micro-fauna (Delfino et al., 2004; Martínez-Navarroet al., 2004, 2010; Rook et al., 2013) and Acheulean technology(Martini et al., 2004). According to combined magnetostratigraphy(Albianelli and Napoleone, 2004), geochronology (Bigazzi et al., 2004)and biochronology (Martínez-Navarro et al., 2004) the Buia Homo-bearing site has been dated to about 1.0 Ma.

The research carried out since the mid-nineties resulted in thediscovery of over 200 late Early Pleistocene localities within an ~1000-meter-thick fluvio-lacustrine sedimentary succession outcropping inthe Dandiero Rift Basin, near Buia. Within this geological succession,three different species of suids, Kolpochoerus olduvaiensis, Kolpochoerusmajus and Metridiochoerus modestus were identified (Martinez-Martínez-Navarro et al., 2004). Thesemorphologically derived suid spe-cies were sharing the same geo-paleoecological habitat with othermammals (including Homo). The main aim of this research is to com-paratively assess the evolutionary changes, biogeographic habitats,and dietary habits of the above-mentioned suid species, followingmethodologies of morphometric systematics, tooth microwear

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Fig. 1. Location map, stratigraphy and geochronology of the Buia Basin. The fossil specimens are from the Alat Formation (Alat Fm). Modified from Abbate et al. (2004) and Ghinassi et al.(2009).

27T. Medin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 431 (2015) 26–42

(Solounias and Semprebon, 2002) and statistical analysis mainly on thedentognathic specimens.

The study of tooth wear on extinct and extant mammal species issignificant in the interpretation of diets and ecological reconstructionsfollowing pioneering works of a number of researchers (Walker, 1976;Walker et al., 1978; Ryan, 1981; Rose, 1983; Grine, 1986, 1987; Grineand Kay, 1988; Teaford and Oyen, 1989; Teaford and Robinson, 1989;Ungar, 1994, 1996; Ungar and Teaford, 1996; Solounias andSemprebon, 2002; Rivals et al., 2008; Teaford, 2007; Rivals et al., 2009;Solounias et al., 2010). Rapid speciation in suids and adaptations havebeen studied from the point of view of their dental morphology, stableisotope composition (Harris and Cerling, 2002), and postcranial anato-my (Bishop, 1994, 1999). However, although suid teethmorphology re-flects the diet available as a result of environmental shifts (and thus dueto climate changes), it is not clear yet if climatic change itself is the pri-mary driving force of speciation (Cooke, 2007). Based on isotope data,trophic adaptations of suids have also been investigated (Harris andCerling, 2002). However, some researchers argue that suids are unlikelyto be grazers because of their bunodont dentition (Harris and Cerling,2002; Janis et al., 2002) because they consume a variety of resourcesand their microwear in modern species remained complicated(Kingdon, 1979; Ward and Mainland, 1999; Reed, 2008). Suidmicrowear patterns imprinted on enamel surfaces are of considerableimportance and can reveal significant information. Traditional statisticalanalyses have focused on comparing and computing the counted aver-age of pits and scratches. However, we believe that suids, unlike otherherbivores or carnivores, show complicated variability in their dietaryhabits. Therefore, in addition to the number of scratches and pits, addi-tional variables (large pits, number of puncture pits, presence of hyper-coarse scratches, etc.) should show important differences among the ex-tinct and extant species.

Attempts have been made by various researchers to better under-stand the dietary habit of suids, including the development of alterna-tive methods (Semprebon et al., 2004). For example, microscopicmicrowear studies were commonly conducted using high resolutionelectron scanning microscope (SEM with magnification typically of500×) with the objective of fast attainment and study of large databases (Ungar, 1994, 1996). Equally, low magnification (35×) stereomi-croscopes contribute significant information by exposing large enamelsurfaces (Semprebon et al., 2004) for better morphospace observationof microwear distribution. The microscopic scars imprinted on the oc-clusal enamel (microwear) document a relatively short occurrence ofdietary behavior.Microwear features observed under lowmagnificationcan yield a wider distribution of microwear scars that preserves infor-mation related to habitat preferences, adaptations and evolutionarytrends of extant and extinct animals.

2. Geo-environment, isotope data, and faunal record

The Danakil Depression is characterized by sedimentary environ-ments dominated by alluvial fans and high energy streams, with someswampy to lacustrine ponds (Abbate et al., 2004). The development ofthis lacustrine-dominated scenario in theDandiero Basin suggests a tec-tonic influence on changes in depositional environments and this hy-pothesis is supported by the occurrence of faults and angularunconformities in the studied sedimentary deposits (Ghinassi et al.,2009; Papini et al., 2014). According to Abbate et al. (2004), the occur-rence of fine-grained lithofacies and the fossil contents indicate a fresh-water lacustrine to palustrine environment. Moreover, Ghinassi et al.(2009), reported that, at about 1 Ma, the Buia environment was charac-terized by water availability and by grassland and savanna-dominatedenvironments developed on adjacent coastal plains and floodplains.

Table 1Measurements of M3 (upper third molar); m3 (lower third molar); L (Length); W(Width); H (Height); LTg (Length Trigonid); Ltd (Length Talonid) of the three suid species(Kolpochoerus olduvaiensis, Kolpochoerus majus, andMetridiochoerus modestus) from Buia.All measurements are in mm.

M3/m3

Taxon Specimen no. Teeth L W H L/Tg L/TdK. olduvaiensis MHB-1-L m3 56.10 20.70 16.51 27.90 28.20

MHB-1-R m3 61.10 20. 90 17.73 28.50 32.60UA-242 m3 66.85 19.90 15.15 24.92 41.52DAN-199 m3 50.86 19.90 12.39DAN-138 m3 64.65 20.58 17.72 28.70 34.98DAN-82 m3 61.17 18.44 9.96 28.49 31.45DAN-139 m3 19.20 31.11DAN-249 m3 16.21 13.80 26.35UA-116 m3 19.90 42.10DAN-232 m3 51.10 18.00 23.80 27.30

K. majus DAN-141 L m3 40.10 21.00 16.18 8.65 21.88DAN-141 R m3 42.7 20.90 17.01 8.64 19.89DAN-174 m3 38.67 21.70 18.02 13.38 22.91DAN-142 L M3 43.97 23.67DAN-142 R M3 40.99 23.60

M. modestus DAN-218 m3 13.46UA-449 m3 45.1 13.50 5.74 25.19 19.05UA-367 M3 10.14DAN-197 m3 13.82 14.89DAN-220 M3 42.2 14.4 23.07 13.58

28 T. Medin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 431 (2015) 26–42

Additional evidence from stable isotope analysis improves this informa-tion. That is, the fluctuations in the isotopic range values wereinterpreted as a temporarily restricted lake in the area during Pleisto-cene times.

The isotope information comes from the lacustrine/palustrine cal-careous beds of the Buia Basin mainly from four geological sections:Aladaf, Dandiero, Homo-site and Dioli/Cabura (Abbate et al., 2004).The results of the analyses of authigenic carbonates and gastropod shells(Melanoides tuberculata) show hydrologic conditions of a lake (Aladafand Dandiero river sections) and climatic change (Alat Formation) rep-resented by large amplitude fluctuations of the δ-18O. The Homo-bearing Alat Formation, which has also yielded large fossil mammalsand lithic assemblages, recorded δ-18O of 4.8‰ to−9.2‰ for the calcar-eous beds and 1.6‰ to−10.6‰ for M. tuberculata shells (Abbate et al.,2004). Moreover, the δ13C record ranges from −2.1‰ to −4.8‰ forthe calcareous beds and−3.2‰ to−5.4‰ for the gastropod shells. Ac-cording to Abbate et al. (2004) the absence of covariance of δ18O andδ13C is compatible with an open water lake or ephemeral ponds withlow residence time.

The Buia fossil fauna, including the Homo remains (Macchiarelliet al., 2004; Zanolli et al., 2014) comes from the basal portion of theAlat Formation of the Dandiero Group. It has been interpreted aslacustrine-deposited environments on which a complex deltaic systemupgraded (Abbate et al., 2004). Most of the fossils represent largemam-mals and were mainly found at the base of the channel-fill deposits of amoderate- to high-sinuosity fluvial system unit (indicated as FL2b) andsecondarily, in the fluvio-deltaic deposits of units (FL1-DL3) (Ghinassiet al., 2009). The large mammals' fossil record from Buia includes:Theropithecus cf. T. oswaldi, cf.Crocuta crocuta, Elephas recki,Ceratotheriumsimum, Equus grevyi, cf. Hippopotamus sp. (small-to-middle sized),Hippopotamus gorgops, K. olduvaiensis, K. majus, Metridiochoerusmodestus, Giraffa cf. G. jumae, Bos buiaensis, Hippotragus gigas, Kobusellipsiprymnus, Gazella sp., Tragelaphus cf. T. spekei, and Caprini indet.(Martínez-Navarro et al., 2004, 2010; Rook et al., 2010). The fauna isdominated by water-dependent species that inhabited grassland andsavanna-dominated environments (Ghinassi et al., 2009). The faunal re-cord comprises also relatively well represented herpetofauna (Pelusioscf. P. sinuatus, Varanus niloticus, Python gr. P. sebae and Crocodylusniloticus), and “minor” taxa, including a large rodent cf. Thryonomys sp.,some birds (Rallidae indet., Anhinga sp., Burhinus sp.), and fish (Clarias(Clarias) sp.) (Delfino et al., 2004; Rook et al., 2013).

3. Materials and methods

3.1. Systematics

The fossil specimens of extinct suids were collected during the lasttwo decades of field survey at the late Early Pleistocene sites of theBuia Basin, directed by the Eritreo-Italian research team. Specimenswere collected from the surface and are currently housed at the paleon-tological laboratory of the National Museum of Eritrea (NME), in Asma-ra. Specimens from the Wadi Aalad hominid site (UMTS coordinates:37P E600710 N1632638) are labeled as UA#, while those from thearea of Dioli (site A037 recorded in the Buia Project site coding; 37PE601107 N1628110), positioned south of Dandero River, are labeled asDAN#. Specimens labeled as MHB#, are from site N277 (37P E601527N1623811), south of Maebele Stream. Finally, a single specimen labeledMA# entered in the NME collections in 2001, collected at the locality ofMulhuli-Amo, about 200 m west of the provenance of Dioli site. Thesesites are correlated on the basis of lithostratigraphy (Aalat Fm), whileDioli and Wadi Aalad (Homo site) are also correlated on the basis oftheir paleomagnetic signature.

Fifty fossil specimens were systematically selected, restored andprepared for morphometric analyses. But, due to taphonomic reasons,some of them were discarded and only the well preserved specimenswere included in this research. Finally, more than half of the specimens

are incomplete and they were not useful for morphometric study. Thetwenty dentognathic fossils included in the study are listed in Table 1.

All the specimens were documented using a high resolution camera(Canon EOS 600D x 18 MP) and the photographic data were processedusing Adobe CS2. The anatomy of each specimenwas described system-atically. Measurements were made with a digital caliper to the nearest0.05 mm. The mesio-distal length (on the buccal side of the occlusalface), the bucco-lingual width, and height (from the occlusal surfaceto the root-apex) of all the dental specimensweremeasured. Moreover,to understand the morphogeometric change of the occlusal surface, thelengths of the trigonid and the talonid were also measured.

A simple bivariate plot was used to analyze the morphometricsamong the East African fossil suid species. PAST data analysis package(cfr. Hammer et al., 2001) helped to examine the 187 quantitativedata. This analysis contributes to understanding the relationship be-tween size and shape of the three suid species lower third molar (m3)specimens. The standard deviation (SD) is calculated to compare itwith other East African suid species.

3.2. Tooth microwear

Themicrowearmethod employed in this studywas adopted follow-ing the methodology developed by Solounias and Semprebon (2002)and Semprebon et al. (2004). Initially twenty-eight fossil dental speci-mens of three suid species were analyzed, but only fifteen specimenswere useful for microwear analysis, including upper and lower thirdmolars belonging to the three species: K. olduvaiensis (n = 6), K.majus (n = 5) and M. modestus (n = 4). To avoid inter-observer error,the quantification of microwear features under the stereomicroscopewas made by only one author (TM).

The microwear data of the extant suid species (Hylochoerusmeinertzhageni, Potamochoerus porcus and Tayassu pecari) were re-trieved from Solounias and Semprebon (2002), Semprebon unpublisheddata and the unpublisheddata of Sus scrofa fromoneof us (FR). Compar-ative data are from collections of NMK (NationalMuseumof Kenya, Nai-robi), AMNH (American Museum of Natural History, New York) andNMW (Naturhistorisches Museum, Vienna).

All of the fossil specimens were cleaned prior to the casting processwith cotton swabs soakedwith acetone, occasionally, laterwith ethanol.This procedure was aimed to remove any dust or chemicals left on thesurface during reconstruction process (e.g. paraloid, a thermoplastic


resin). The impressions were made using polyvinylsiloxane silicone(Heraeus Provil novo). The positive casts were made using epoxyresin (Epoxy-150 and K-151). In order to avoid inter-preparator biasthe casting process has been conducted by only one of us (TM). Thespecimens were checked under a Zeiss Stemi 2000C stereomicroscopewith a magnification of 35×.

The specimens with clear evidence of microwear features were se-lected for detailed study. The median part of the molar tooth was usedfor microwear reference in suid species (Solounias and Semprebon,2002). Therefore, counting scratches and pits was conducted on twoareas of the lower third molars' occlusal surface (both, on the trigonidand the talonid). A standard 0.16 mm2 ocular reticle was employed toquantify the number of small pits (very regular with sharp, circularand distinct borders, and very refractive or shiny) and large pits(deeper, less refractive and at least about twice the diameter of smallpits), scratches (elongated scars with parallel sides), and gouges (largescares with irregular borders). Puncture pits are very deep, symmetricalandwith regularmargins. Cross scratches are those scratches which areoriented somewhat perpendicularly to the majority of scratches ob-served on dental enamel. The ScratchWidth Score (SWS) is representedfor presence and absence of fine scratches (=0), mix of fine and coarse(=1) and coarse scratches (=2). Gray scale high-resolution micropho-tographs were prepared with a 0.1 mm scale and the editing processwas made using Adobe CS2. Empirical data of the three suid fossil spe-cies from Buia were statistically analyzed using Principal ComponentAnalysis (PCA) and compared, to the extant suoid species from Africa,Europe, and America. Densities of pits and scratches were log-transformed to analyze microwear variables.

4. Results

4.1. Systematic Paleontology

Family Suidae Gray, 1821Genus Kolpochoerus Van Hoepen and Van Hoepen, 1932Species Kolpochoerus olduvaiensis (Leakey, 1942)

4.1.1. Referred materialsUA-154 (upper C, side indet.), DAN-221 (M1, side indet.), UA-36

(right M3), UA-167 (right M3, talon part), MHB-1 (left and righthemimandibles: Left, with C, alveoli of p3–m1, worn m2 and m3;Right, with broken parts of C, alveoli of p2–m2, and m3), UA-242(right hemimandible with C, p3, p4, alveoli of m1, worn m2 and m3),DAN-199 (right mandibular corpus fragment with broken m2 andm3), DAN-132 (mandibular corpus with alveolus of p4, and worn m1;side indet.), DAN-233 (p4 fragment, side indet.), DAN-51 (right m1),DAN-138 (right m3), DAN-82 (left m3), DAN-135 (talonid of a lowerthird molar, side indet.), DAN-139 (right m3), DAN-189 (m3 fragment,side indet.), DAN-249 (left m3), UA-116 (right m3), DAN-232 (leftm3), UA-329 (m3, side indet.).

Fig. 2. Mandible of Kolpochoerus olduvaiensis UA-242. A) Occlusal view; B) right buccalview; C) and right lingual view.

4.1.2. Upper dentitionNo incisors are recorded. A single preserved upper canine (UA-154)

with a broken root and of small dimensions shows an entire surface cov-ered by enamel and a wear facet on the anterior face.

The morphology of the upper first molar (DAN-221) has a promi-nent protocone, a paracone, and a higher anterior cingulum comparedto the posterior one. The upper third molars (UA-36 and UA-167) arenot well preserved because of natural alterations (e.g. weathering);however, they show trigon symmetry (UA-167). They have a longtalon that commences interiorly with a triangular median pillar imme-diately behind the posterior median pillar of the trigon (Harris andWhite, 1979). The median pillars have triangular shapes and end in asingle pillar towards the distal side.

4.1.3. Mandibles and lower dentitionThe hemimandibles (UA-242, and mandibular rami MBH-1 left and

right) (Fig. 2) preserve the cheek teeth. Both mandibles are gracileand inflated beneath the cheek teeth. A post canine constriction is no-ticed at UA-242 and the bucco-lingual width is measured to50.34 mm. The mandibular rami of MHB-1 are well preserved, with ahigher ascending ramus, and curved at the ventral profile (Fig. 3).

Canines of this species are not well represented but, based on thecomparison of the single lower canine (UA-242) and alveoli of (MHB-1), they are sexually dimorphic. The canine alveoli for MHB-1 (in bothmandibular rami) show larger size of canines than UA-242.

The lower premolars (p3 and p4) both have sub-triangular shapesand are unicuspidate; p3 is smaller and narrower than p4, and bothare bucco-lingually compressed; p4 has an additional small anterior in-termediate cusp. However, both are smaller than K. majus specimens.

The m3 is the best preserved element within the fossil series of thisspecies. It has moderately preserved occlusal surfaces andmost of themhave well preserved cusps in the trigonid, which is bucco-linguallywider than the talonid. In all the specimens, the talonid is longermesio-distally than the trigonid (cf. Table 1). Four to five triangular cen-tral pillars separate the bicuspid paired pillars of the talonid. The enamelfolds to the lingual side at the trigonid occlusal surface (DAN-82). Thebuccal cusps are higher than the lingual ones in most of the specimens(DAN-138, DAN-82). The trigonid–talonid junction is marked by the tri-angularfirst central pillar just behind the twopillars of the trigonid (UA-242, DAN-82, DAN-249 and DAN-23). However, in some cases, doublemedian pillars in the mesio-distal direction separates the 2nd, 3rd and4th cusps followed by single two triangular median pillars towardsthe distal side of the talonid (DAN-138). The lateral, or terminal, pillarsare marked by bicuspid pillars, in which a single pillar is poorly visible(DAN-82) or ends with a developed single pillar (DAN-249, DAN-199,DAN-139 and UA-242) (Fig. 4).

Fig. 3. Mandible of Kolpochoerus olduvaiensisMHB-1 showing an interesting pathology: The right third molar is longer than the left one. A) Right hemimandible (A1: buccal view; A2:lingual view); B) left hemimandible (B1: buccal view; B2: lingual view); C) occlusal view.


The specimen MHB-1 shows different length of left and right m3 ofthe mandibular rami, that is, 56.10 mm and 61.10 mm, respectively.This asymmetry is probably related to the high inbreeding in the popu-lation of this species in the area (Martínez-Navarro et al., 2004).

The result of morphometric comparison of K. olduvaiensis specimensfrom Buia to other assemblages from East Africa, shows the increase ofthe third molar length from the ancestor K. deheinzelini (=Dasychoerusarvenensis) to the progressive K. olduvaiensis. Moreover, K. olduvaiensisfrom Buia shows close morphometric similarities to the EthiopianDaka sample.

Species Kolpochoerus majus (Hopwood, 1934)

4.1.4. Referred materialsDAN-142 (complete craniumwith left and right dental arcade, worn

P2–M2 and M3), UA-303 (maxillary fragment), UA-378 (mandibularsymphysis), DAN-187 (mandibular symphysis), UA-20 (palate withleft alveoli of P4–P2 and M3–M1, and right aleveoli of P3 and P2 andP4–M3), DAN-174 (left hemimandibular fragment with m3), DAN-194

Fig. 4. Illustration of occlusal view morphology of a K. olduvaiensis right low

(right hemimandibular fragment with m1–m2), DAN-141 (mandiblewith left and right rami; Left: anteriorly broken p4–m3, Right: wornm1–m3), UA-457 (upper C, side indet.), DAN-133 (left M2), UA-223(M2 side indet.), UA-437 (left M2), DAN-143 (left m3), UA-44 (rightm3), UA-464 (right m3).

4.1.5. CraniumThe massive cranium (DAN-142) comprises almost a complete pal-

ate and dental arcade (Fig. 5). It is short in the antero-posterior direc-tion. The muzzle is shorter and the premaxillary bone is shorter andbroader than in advanced forms of the lineage K. limnetes/K.olduvaiensis. The supraorbital channels are very deep (30.35 mmdeep), wide and extend forward towards the nasal end. The zygoma ismassive and the anterior zygomatic margin projects at right anglesfrom the sagittal axis and arches inflated downwards (DAN-142). Theentire lateral border is heavily magnified and strongly rugose. Theinfraorbital foramen is well marked and the occipital condyles are welldeveloped (width 66.53 mm). The left orbit and jugular process are

er third molar (m3) taken from the mandible UA-242. (Not to scale).

Fig. 5. Cranium of K. majus DAN-142 from Buia. A) Dorsal view; B) posterior view; C) basal view; D) left lateral view; and E) right lateral view.


broken, and the upper parts of the foramen magnum are also not pre-served. The interior transverse diameter of the orbit is 85.46 mm. The

Table 2Measurements of the Kolpochoerus majus skull from Buia (DAN-142). Metric data ofAsbole (ASB-192) and Bodo (L6-10) are from Geraads et al. (2004). Measurements arein mm.

Position of measurement Buia(DAN-142)

Asbole(ASB-192-2)

Bodo(L6-10)

Condylo-basal length 365.00 390 365Length from back of condyle to M3 142.15 152 146Length from orbit to front of canine 185.94 195 198Length of the inner orbit 83.05 – –

Transverse Diameter of the Foramenmagnum

35.43 – –

Width at nasal boss 154.92 – –

Maximum width at orbits 102.29 – –

Width at dorsal edge nuchal crest 118.20 – –

Maximum width of the occiput 127.64 155 132Height of the occipital region 144.05 135 122Width of occipital condyles 66.53 – –

Depth of foramen magnum to nuchal crest 110.15 – –

Length of M1–M3 (basal) 94 78 76Width of the palate at M1 82.04 – –

Width of the palate at M3 81.84 – –

nuchal crest is preserved with slight damage at the surface of the rightside. The least breadth of the skull at the nuchal crest was measuredat 87.38mm. The Buia cranium (DAN-142) has closermetric similaritiesto theK.majus skull fromBodo (L6-10) than to the female cranium fromAsbole (ASB-192-2) (cf. Table 2). DAN-142 has the same length at thecondylo-basal region to L6-10. However, it is shorter compared toASB-192-2. Importantly, the height of the occipital region for DAN-142is higher than both of the other specimens. The length of the palate(M1 to M3) of the Buia skull (DAN-142) is also significantly longer.

4.1.6. MandiblesTwo mandibular bodies of this species (DAN-194, DAN-174) have

well-rooted and low crownedwornm1–m2. The height of themandible(DAN-194) at m1 is 49.07 mm. The right mandibular body (DAN-174)preserves the dental arcade with p3–m3. The buccal side of the trigonidand part of the talonid of them3 is broken. The height of themandibularbody (DAN-174) atm1 is 54.05mm, while atm3 it is 57.18mm. Gener-ally, themandible gets wider towards the posterior side. This is the areadevoted to crushing hard food. The mandibles are sexually dimorphicand larger (DAN-187) than the specimens of K. olduvaiensis (UA-242).

The massive fragmentary mandibular symphysis (DAN-187) com-prises broken canines (right and left) and incisors. It shows markedpost canine constriction and the inferior surface ascends gently towards


the anterior end. Another remarkable specimen of this species is a man-dibular arcade with heavy incrustation (DAN-141) with right and leftcheek teeth. This mandible is significantly larger and probably belongsto a male individual.

4.1.7. Upper dentitionThe isolated canines are oriented bucco-lingually, abraded on the

upper part and with enamel at the anterior face (UA-457, UA-303).The premaxillary bones (DAN-142 and UA-20) preserve the alveoliand are comparatively larger but sexually dimorphic as K. olduvaiensis.

The upper premolars are not well preserved.The first molars (UA-20) have prominent anterior cingulum; and

they are mesio-distally longer and slightly narrower (bucco-lingually)than the second molars. DAN-133 has the largest and tallest cusp, ex-tending backwards to the anterior junction of the protocone andparacone. The second molars (M2) are larger compared to K.olduvaiensis specimens and mesio-distally longer. These molars (DAN-133, UA-437, DAN-142 and UA-20) have higher crowns and preservedtrigon with prominent cusps. In one specimen (UA-437), a central con-striction is visible and a poorly preserved pillar separates the anteriorand posterior pairs pillars.

The Buia K. majus upper third molars have hypsodont crowns andstrongly crenulated enamel with the same morphology reported forthe Asbole cranium (ASB-192-2) and Bodo skull (L6-10) by Geraadset al. (2004). Also they show close similarity to those from Daka andOlduvai Beds II, III and IV (cf. Table 3).

4.1.8. Lower dentitionIncisors are known from onemandibular symphysis (DAN-187) and

the second incisor (i2) is the larger on both sides of the series.The lower premolars are represented by a single and anteriorly bro-

ken fourth premolar (p4). It is proportionately large and the metaconidis significantly reduced to a small cusp.

The m1 and m2 are morphologically similar to those of K.olduvaiensis, although they are larger. The m2 is longer and widerthan the m1. The cusps are also larger in m2 than m1. In both m1 andm2, the mesial pairs of pillars are separated from the two distal pairsby a single median pillar. The m3 usually consists of three well-defined pairs of pillars plus a median distal pillar, but smaller pillarsmay be present around it, and between the second and third pairs(Kullmer et al., 2008). A double median pillar marks the m3 trigonid–talonid junction. The protoconid, paraconid, metaconid and hypoconidare well marked. The short m3 and unique hypsodonty, pillar shape, ce-mentum cover, and enamel corrugation serve to separate K.majus from

Table 3Tabular presentation of suid m3, from different Plio-Pleistocene African sites. Metric data are fKada Hadar Cooke (2007); and Galili- GLL-96 Kullmer et al. (2008).

Length

Taxon Site No. Min. L Max. L

K. deheinzelini Galili 1K. afarensis Kada Hadar 1K. heseloni Shungura Low. G 52 45.3 61.2K. olduvaiensis Buia 7 51.10 66.85K. olduvaiensis Daka 8 52.7 78.6K. majus Buia 3 38.67 42.7K. majus Daka 9 37.5 55.3K. majus Olduvai Bed III/IV 1K. majus Olduvai Bed II up. 3 45.0 50.0K. majus Olduvai Bed II low. 1M. modestus Buia 2 45.1 51.79M. modestus Daka 5 38.6 50.1M. modestus ShunguraLower G 2 39.8 45.0 42.40M. andrewsi Koobi Fora 3 45.7 48.6M. andrewsi Olduvai Bed II 1M. compactus Olduvai Bed II up. 21 60.0 110.0M. jacksoni Shungura G 21 46.0 64.4

the contemporaneous progressive K. limnetes/K. olduvaiensis specimens(Harris andWhite, 1979). Generally, K.majus upper and lower m3s aremorphologically variable.

Genus Metridiochoerus Hopwood, 1926Species Metridiochoerus aff. M. modestus (Van Hoepen and Van

Hoepen, 1932)

4.1.9. Referred materialsDAN-218 (mandibular fragmentwithm3 and alveoli of p4-m2), UA-

449 (mandibular fragment with m3 and roots of m2), DAN-220 (leftM3), UA-367 (right M3), DAN-197 (left m3), MA-01-1 (right m3).

M. modestus specimens are scarce in the Buia Basin, unlikeKolpochoerus. Only the upper and lower third molars of this speciesare preserved.

4.1.10. Upper dentitionThe M3s (UA-367 and DAN-220) have well-preserved occlusal sur-

faces and prominent cusps with trigon and talon. The enamel is presenton all faces of the trigon and talon surfaces. In DAN-220 (Fig. 6) the tri-gon and talon are separated by mesio-distally positioned central andprismatic pillars. The distal end of their talon ends in a single pillar.Their crown is higher and well-rooted with a height of 32.32 mm(UA-367) and 20.55 mm (DAN-220) respectively, at the trigon. DAN-220 shows a three pit-like depressed area (fovea) at the mesial side.

4.1.11. Lower dentitionTwo mandibular bodies preserve the alveoli of p4 to m2 and m3

(UA-449 and MA-01-1). The UA-449 mandibular corpus is larger thanthat of MA-01-1, however both have high crowns. In the m3 theprotoconid and metaconid are separated from the hypoconid andentoconid by two pairs of central tubercules. The trigonid is also sepa-rated from the talonid by two central median tubercules. The distalpart of the talonid ends in two asymmetric pairs of tubercules. The ce-ment is present in the lingual, buccal, distal and mesial surfaces of m3,and its corrugation is marked. In MA-01-1, the trigonid and talonidjunction is strongly constricted and the talonid is totally inflated to-wards the distal end. The trigonid is well developed with two first andsecond pairs of cusps separated by single central pillar. The secondpairs of pillars with the fused second central pillar have a “T-shaped”outline. The symmetry of the talonid is poorly represented. The surfaceof the trigonid is higher than the talonid. Two isolated m3 specimens(DAN-218 and DAN-197) show a high molar crown. DAN-218 probablybelongs to an old individual because its occlusal surface is deeply worn.In both specimens, the protoconid and metaconid are separated by a

rom: Daka Gilbert (2008); Shungura Lower G, Olduvai Bed II, III/IV, Koobi Fora, Galili, and

Width

Mean SD Min. W Max. W Mean SD

39.9 14.8237.7 19.054.75 3.73 17.5 24.2 21.6 1.8958.83 6.3 16.21 20.90 19.37 1.4563.55 7.6 18.3 27.8 21.7 3.140.9 2.0 20.9 21.7 21.2 0.4346.5 6.2 20.8 25.5 23.0 1.8343.0 19.748.3 2.89 21.7 22.0 21.83 0.1543.5 20.348.45 4.7 13.46 13.82 13.57 0.1645.16 4.6 11.8 14.5 13.26 1.02

3.68 14.5 16.4 15.45 1.3447.27 1.46 13.0 14.8 13.93 0.9054.0 16.279.38 13.47 14.0 22.7 18.65 2.3056.99 5.00 18.0 24.9 20.99 2.17

Fig. 6.Upper left thirdmolar ofMetridiochoerusmodestus UA-220 from Buia. A) Occlusal view; B) buccal view; and C) lingual view. Interpretation of themorphology of the occlusal surfaceto the right (Not to scale).


single central tubercule from the hypoconid and entoconid, and the dis-tal part of their talonid is represented by asymmetric pairs of pillars.

Taking the abovemorphometric data into account,M.modestus fromBuia resembles those from Daka and M. andrewsi from Koobi Fora (cf.Table 3).

Fig. 7. A simple bivariate analysis (x, y) graph showing morphometrics (mean of lengthand width) distribution of lower third molar (m3) among selected East AfricanKolpochoerus and Metridiochoerus species. The star symbol represents the Buia suid spe-cies. Numbers are attributed to: (1) K. deheinzelini (=Dasychoerus arvenensis) from Galili,(2) K. afarensis fromKadaHadar, (3) K. heseloni from Shungura lower G, (4)K. olduvaiensisfrom Buia, (5) K. olduvaiensis from Daka, (6) K. majus from Daka, (7) K. majus from Buia,(8) K. majus from Olduvai Bed III/IV, (9) K. majus from Olduvai Bed II upper, (10) K.majus Olduvai Bed II Lower, (11) M. modestus from Buia, (12) M. modestus from Daka,(13) M. modestus from Shungura lower G, (14) M. andrewsi from Koobi Fora, (15) M.andrewsi fromOlduvai Bed II, (16)M. compactusOlduvai Bed II upper, and (17)M. jacksonifrom Shungura Lower G. Metric data are from: Daka (Gilbert, 2008); Shungura Lower G,Olduvai Bed II, III/IV, Koobi Fora, Galili, and Kada Hadar (Cooke, 2007); and Galili- GLL-96 (Kullmer et al., 2008).

4.2. Statistical results

The m3 metric data of the three suid species from Buia were com-pared to species from the following African Plio-Pleistocene sites: Galili,Kada Hadar, Shungura Lower G, Daka, Olduvai Beds II (lower andupper), Beds III/IV and Koobi Fora. The data show very limited changesin molar width in Kolpochoerus species. A bivariate graph (Fig. 7) showssignificant variance of length among the species. This means suid spe-cies show a progressive increase in molar length (mesio-distal) com-pared to the molar width (bucco-lingual). K. majus, K. heseloni and K.olduvaiensis recorded the widest third molar of any other Kolpochoerusor Metridiochoerus species. The standard deviation (SD) result for theBuia suids show very low variation from the mean, at species level(that is, SD = 1.45 for K. olduvaiensis, SD = 0.45 for K. majus andSD = 0.16 for M. modustus) compared to other sites. M. compactusfrom the upper part of Olduvai Bed II has amean of 79.38mm in length,which is the larger dimension compared to any other species ofKolpochoerus or Metridiochoerus followed by K. olduvaiensis speciesfrom Buia and Daka, and K. heseloni and M. jacksoni from ShunguraLower G. However, all K. majus specimens show bucco-lingually widerthird molars, with shorter mesio-distal lengths. The data of K. majusandM.modestus show clearly hypsodontmolars,which is a typical char-acteristic of both species.


4.3. Tooth microwear results

The microwear features (pits and scratches, etc.) observed on themolar enamel surface of the three suids species revealed significant dif-ferences (Table 4). The dental specimens of K. olduvaiensis show a sig-nificantly lower density of pits and scratches compared to the fivespecimens of K.majus and the four specimens ofM.modestus. The anal-ysis does not show any important difference in the average density ofpits and scratcheswithin K. olduvaiensis specimens; however the recordshows slight variation in K. majus and high variation in M. modestus.

Fine scratches and small pits show identical densities in K.olduvaiensis. This is a comparable record of the average density of pits(70.3 pits/mm2) to the density of scratches (70.3 scratches/mm2). Thescratches observed in K. olduvaiensis specimens are comparatively lon-ger and deeper than scratches in K.majus andM.modustus. Themajorityof the specimens show fewer large pits than in K. majus and M.modustus. There is no evidence of gouges. Puncture pits are visibleonly on one specimen (DAN-249). Cross scratches and hypercoarsescratches are abundant (i.e. high scratch width scores) (Fig. 8).

In K. majus, we observe a similar quantity of pits (141.9 pits/mm2)and scratches (120.6 scratches/mm2) (Fig. 9). There is no significant dif-ference between the densities of pits and scratches (Mann–Whitney Utest; U= 0; p=0.0122). Specimens havemore pits than K. olduvaiensisand fewer thanM.modestus. However, K.majus has a greater density ofscratches than the other species. Large pits are also abundant. K. majusspecimens have more large scratches than the other species, neverthe-less the fine scratches are still the most abundant and they are denserand fainter than those observed in K. olduvaiensis and M. modestus.Small pits are dominant for K.majushowever; large pits are also record-ed in low numbers on two specimens (UA-464 and UA-44). Specimensshow evidence of large pits, cross scratches and low scratch widthscores, but like K. olduvaiensis, puncture pits and gouges are almost ab-sent. However, unlike K. olduvaiensis they have very few hypercoarsescratches.

The hypsodont specimens of M. modestus show the highest densityof pits of all species (154.7 pits/mm2) and an average density ofscratches of 70.6 scratches/mm2 (Fig. 10). However, M. modestus haverelatively the same density of scratches as K. olduvaiensis, but lowerthan in K. majus. The average density of pits in M. modestus specimensis higher than the overall average density of scratches observed. Thescratches in M. modestus specimens are quantitatively fewer, deeper,and discontinuous. The microwear features also include large pits andcross scratches. It has no record of hyper coarse scratches and gouges.

Table 4Microwear data of fossil suid species from the paleontological sites of Buia. Abbrv. Lpts= large piscore; H.crs = Hypercoarse scratches.

Taxon No. Spm. code Average # of pits Average #K. olduvaiensis MHB-1-L 19 8K. olduvaiensis MHB-1_R 19.5 11K. olduvaiensis UA-242 5 11K. olduvaiensis DAN-138 5.5 9.5K. olduvaiensis DAN-249 9.5 15.5K. olduvaiensis UA-116 8.5 12.5Average 6 11.2 11.2K. majus UA-437 21 18.5K. majus DAN-141_L 13.5 17K. majus DAN-141_R 28.5 22K. majus UA-44 31.5 25.5K. majus UA-464 19 13.5Average 5 22.7 19.3M. modestus DAN-218 25.5 8M. modestus UA-449 22.5 5.5M. modestus UA-367 28 27M. modestus MA-01-1 23 8.5Average 4 24.75 12.25

4.4. Comparative analysis to extant species

At present six living genera of suids (Sus, Potamochoerus,Hylochoerus, Phacochoerus, Porcula and Babyrousa) are known in theOldWorld (Funk et al., 2007; Gilbert, 2008). Three extant Suidae species(S. scrofa, P. porcus and H. meinertzhageni) and one AmericanTayassuidae (T. pecari) were selected for our comparative study(Table 5). These extant taxa live in different geographical areas, that is,S. scrofa is found in extensive areas of Europe andAsia,H.meinertzhageni(giant forest hog) is found in central Africa, P. porcus (bush pig) rangesthroughout sub-Saharan Africa, and T. pecari (white-lipped peccary) isa species endemic to South and Central America (Table 6).

The comparative study resulted in a significant correlation of dietaryhabits within extant and extinct suids and peccaries. The relative densi-ties of pits and scratches do not discriminate the dietary habits of thespecies. However, other microwear features such as large pits (Lp),number of puncture pits (Npp), cross scratches (XS), hypercoarsescratches, gouges and scratch width scores (SWS) were found to be sig-nificant. The PCA graph (Fig. 11) shows no significant loading value forthe number of pits and scratches. The first two components of the PCAexplained 42.8% and 20.9% of variance respectively, among the selectedmicrowear features. On thefirst component thepeccarywas found to bedistinctive. The peccary showed a greater number of large pits, puncturepits, large and hypercoarse scratches. However, the number of scratchesand pits, cross scratches and gouges was found to be lower. The num-bers of pitswere also greater than in extant and extinct suid species. Im-portantly, K. olduvaiensis, K.majus andM.modestus show slightly fewermicrowear features compared to the peccary than the other extant suidspecies. They scored higher value of large pits, puncture pits, large andhypercoarse scratches. The PCA shows lower values in the other extantsuid species. Of these, S. scrofa scored the lowest value for thesemicrowear features. The PC-2 (with 20.9% of variance) revealed highervalues of gouges, large and puncture pits, coarse and hypercoarsescratches for P. porcus followed by H. meinertzhageni and higher valuesof large and puncture pits as well as hyper coarse scratches for K.olduvianesis, K.majus andM.modestus. Along this component, P. porcusand H. meinertzhageni scored the highest number of scratches, pits andcross scratches.

The microwear features of M. modestus overlap the morphospacewith K. olduvaiensis and K. majus. Even though the density of scratchesand pits of K. olduvianesis, K. majus and M. modestus were found to bedifferent, based on the values of the additional microwear features,these species are more similar to each other in dietary habits than to

ts;Npp=Number of puncture pits; XS= cross scratches;Ggs= gouges; SWS= Scratchwidth

of scratches Lpts Npp XS Ggs SWS H. crs1 0 1 0 1 10 0 1 0 1 10 0 1 0 1 11 0 1 0 1 01 1 1 0 1 11 0 1 0 1 0

1 0 1 0 1 11 0 1 0 1 01 0 1 0 1 01 1 1 0 1 11 0 1 0 1 1

1 1 0 0 1 01 1 1 0 1 01 1 1 0 1 01 1 1 0 1 0

Fig. 8.Microwear features on lower third molar specimens of Kolpochoerus olduvaiensis from Buia: (A) UA-116, (B) DAN-249, (C) MHB-1_L, (D) MHB-1_R, (E) UA-138, and (F) UA-242.Scale= 0.1 mm.


any other extant Suidae or Tayassuidae species. The same is true for theextant suids species (H. meinertzhageni, P. porcus and S. scrofa) in that,regardless of their density of scratches and pits other microwear fea-tures are similar. These species show greater similarities in dietaryhabits than the extinct suid species and the peccary.

This shows that the counted value of the number of scratches andpits observed on the enamel surface of suids and peccaries has less im-pact in differentiating the dietary habits of omnivorous species com-pared to herbivorous animals. As shown in component two of the PCA,P. porcus has very high numbers of pits and scratches relative to H.meinertzhageni. However, H. meinertzhageni has finely texturedscratches, which are not seen in P. porcus. The latter has a high percent-age of coarse and mixed scratches (Solounias and Semprebon, 2002).

Based on the number of pits and scratches per counting area (in0.16 mm2) the peccary (with average number of pits 45.3 pits/mm2

and average number of scratches 23.5 scratches/mm2) falls within thegrazingmorphospace. P. porcusdue to its rooting habits, scored high aver-age number of pits (34 pits/mm2) and intermediate number of scratches(20.1 scratches/mm2) in comparison to extant suids. The giant H.meinertzhageni scored 28.8 pits/mm2 and 17.3 scratches/mm2, andS. scrofa 24.5 pits/mm2 and 22.7 scratches/mm2. From the extinct species,M. modestus records high average number of pits (24.75 pits/mm2) andlow average number of scratches (12.25 scratches/mm2). K. majus

shows 22.7 pits/mm2 and 19.3 scratches/mm2. However, K. olduvaiensisfalls into the browsing morphospace because of its low values of pits(11.2 pits/mm2) and scratches (11.2 scratches/mm2).

5. Discussion

5.1. Paleontology and biochronology

Fossil suid species are known from a number of Early to Middle Pleis-tocene sites in East Africa (Harris and White, 1979; Asfaw et al., 1992;Gilbert et al., 2000), North Africa (Geraads, 1993, 2002; Sahnouni et al.,2002), and importantly in the Levantine Corridor (Geraads et al., 1986;Tchernov et al., 1994). Their evolution and dispersals were related toglobal climatic changes and modes of food resource exploitation. Studieson fossil African Bovidae suggested a final phase of increased arid-adapted turn-over near 1.2 and 0.6 Ma (Vrba, 1995). Potts andBehrensmeyer (1992) reported major change in the dental morphologyas a response to the expansion of grasslands in Africa, which was greatlypronounced in the Pleistocene. Placed across this time span, the Buiamammals are represented by an increased percentage of grazing andwater dependent animals. Among these, the suid species (K. olduvaiensis,K. majus and M. modestus) have been found to be a powerful tool for

Fig. 9.Microwear features on lower third molar specimens of Kolpochoerus majus from Buia: (A) DAN-141_L, (B) DAN-141_R, (C) UA-437, (D) UA-464, (E and F) UA-44. Scale= 0.1 mm.


biochronological correlation because of their progressive craniodentalmorphology that indicates a rapid process of speciation and evolution.

Early suids show primitive morphology of the third molar. InTetraconodontinae, Nyanzachoerus, Leakey 1958, species show the en-largement of P3s and P4s and brachydont molars (Kullmer, 1999;Pickford, 2013). In Suinae the enlargement of the third molar followedby reduction of the premolars was noticed in Gerontochoerus euilus,Hopewood 1926a (=Notochoerus euilus) (Kullmer, 1999; Pickford,2013). Due to their progressive dental anatomy the tetraconodontGerontochoerus persisted until the Middle Pliocene and probablydescended fromNyanzachoerus, (Pickford, 2013). The suineNotochoerus,Broom, 1925, arrived in Africa at the base of the Pliocene (Brunet andWhite, 2001; Harris et al., 2003) and it is known for its well-developedrooting behavior (Cooke and Wilkinson, 1978). Recently, Pickford(2012) realized that, Notochoerus, Kolpochoerus, Metridiochoerus,Hylochoerus and Phacochoerus developed from Dasychoerus. Generally,these African suids are basically characterized by the developmentof a complicated talonid in the third molars, with several pairsof cuspids and thick enamel. During the Late Pliocene, suidspecies like Potamochoerus, Kolpochoerus, Metridiochoerus appearedwith such progressive dental anatomy. These lineages are todayrepresented by bush pig (Potamochoerus porcus), forest hogs(H. meinertzhageni) and warthog (Phacochoerus aethiopicus) respec-tively (Harris and Cerling, 2002).

K. olduvaiensis is a sexually dimorphic species. It haswell-rooted andlow-crowned molars, mandibular body bulges on the lateral margins,developed protocone on the upper molars, and elongation of the thirdmolar talonwith four to five pillars (Harris andWhite, 1979).Moreover,it is known for its two triangularmedian pillarswith a butting base fromthe junction of the talonid and trigonid. The latter characteristics are re-ported from Daka suid species (Gilbert, 2008) and evidenced on theBuia specimens. Metrically, all the teeth from suid species are elongatedmesio-distally. K. olduvaiensismetric data from Buia show close similar-ity to the suids from Daka and Shungura Member G. The progressiveelongation of the third molar (m3) from K. deheinzelini (=Dasychoerusarvenensis) to K. olduvaiensis shows the high value of this lineage as abiochronological tool (Gilbert, 2008) and chronologically younger andevolved Kolpochoerus species differs from the extant P. porcus by theircrown height and developed median pair pillars in the talonid. Howev-er, P. porcus has more similar cranial features to Kolpochoerus species,because of their inferiorly oriented zygomatic morphology and inflatedmandibular rami (Bishop, 2011). K. olduvaiensis has close similarities tothe giant H. meinertzhageni, while K. afarensis teeth are similar to P.porcus (Harris and White, 1979). The anterior border of the symphysisof K. olduvaiensis is gently curved and resembles that of Hylochoerus(Hendey and Cooke, 1985). K. olduvaiensis was not known in the fossilrecord after 0.8 Ma (Gilbert, 2008) and its last evidence was fromOlduvai Bed IV, Tanzania (0.78Ma) (White, 1995; Geraads et al., 2004).

Fig. 10. Microwear features on lower third molar specimens of Metridiochoerus modestus from Buia: (A and B) DAN-218, (C) MA-01-1, (D) UA-449, (E) UA-367. Scale = 0.1 mm.


K.majus is a moderate-sized suid species having derived and similardental morphology to K. olduvaiensis. Both species have well-rootedcrowns. However, K. majus lower third molars are shorter and low-crowned. It has, larger uppermolars and the teeth have thick cementumand show strongly crenulated enamel. It has more hypsodont cheekteeth than K. olduvaiensis and a strong lateral bulge of crown elementsabove the enamel line (Harris and White, 1979). K. majus, with itssmall and simple teeth, occurs as a rare element alongside the largerand higher-crowned K. olduvaiensis. This occurrence suggests patchesof bush with water persisting in the savanna-like environment (Bobeet al., 2007). The earliest evidence of K. majus is known from Africa atabout 1.9 Ma (Konso) and it was a successful species until the MiddlePleistocene in East Africa; in Asbole, Lower Awash (0.6–0.8 Ma) andMiddle Awash (0.6 Ma) (White, 1995; Suwa et al., 2003; Geraadset al., 2004). Buia K. majus specimens show close metric similarities toDaka and Olduvai suids (cf. Table 3). Nowadays, P. porcus, the modernbush pig, has several cranial and dental features in common with K.majus and Sus. Its preferred habitats are wooded areas with watersources nearby (Kullmer, 1999) and dense vegetation, riverine andmountain areas (Nowak, 1999).

Metridiochoerine species show: a reduced length of premolar row,delayed root fusion, moderate to extremely hypsodont M3s with pris-matic lateral pillars and numerous toll-shaped enamel islands(Kullmer, 1999; Bishop, 2010a,2010b). The species M. modestus is thesmallest of the genus, occurring alongside the very hypsodont andwarthog-like teeth of M. compactus (Bobe et al., 2007; Bishop, 2010a,

2010b). This species appears at about 2.2 Ma, in most East and SouthAfrican sites, and continues to 1.0 Ma and probably later (Harris andWhite, 1979; Suwa et al., 2003; Geraads et al., 2004; Bobe et al., 2007).M. modestus appeared in the Buia Basin around 1.0 Ma (Martínez-Navarro et al., 2004), and persisted until the middle Pleistocene. Themetric data of M. modestus from Buia overlaps with the data fromDaka and shows higher similarities than Kolpochoerus species do.

A bivariate plot for Buia suid dental specimens shows an increasedlower third molar length for K. olduvaiensis than the hypsodont K.majus and M. modestus. The metric data show quite close similaritiesto species from Daka and Olduvai Bed II/III/IV. The two small speciesK. majus and M. modestus, due to their evolved chewing advantage,might have inhabited an extended savanna area but not far from thelakes and swamps. For example, stable isotope data of two uppermolarsof K. majus and one lower third molar of M. modestus from the middleAwash site of Ashbole (Ethiopia), show exclusively C4 grazing dietaryhabits for both species (Bedaso et al., 2010).

5.2. Tooth microwear and paleoecology

Themoderate-sized andhypsodontK.majuswas contemporaraneouswith the advanced K. olduvaiensis. Thus it may have been adapted to theopen grasslands of the Buia Basin together with the small M. modestus.These species might have consumed dry leaves, grasses, wood bark,and importantly, might have relied on a rooting diet. The results is thatbrowser characteristics for K. olduvaiensis, mixed feeding for K. majus

Table 5Microwear counting data of extant suid species from Africa and Europe, and peccaries from America. Abbrv., #Pits= number of pits; #scr = number of scratches; LP= large pits; Npp =Number of puncture pits; XS= cross scratches; Ggs = gouges; SWS = Scratch width score; Hyp.crs = Hypercoarse scratches. The counting was made on two sample areas on the occlusalsurface. The data come from (1) Solounias and Semprebon (2002); (2) Florent Rivals (unpublished data) and (3) Gina Semprebon (unpublished data).

Pits Scratches

Species No. Code # Pit#1 Pit#2 Av. # Pits Scr.1 Scr.2 Av. # Scr. LP Npp XS Ggs SWS Hyp. crs

P. porcus (1) 220139 48 52 50 6 4 5 0 0 1 1 2 0P. porcus (1) 220145 37 37 27 11 6 8 0 0 1 0 2 0P. porcus (1) 220413 48 40 44 16 12 14 0 0 1 0 1 0P. porcus (1) 482000 10 4 7 20 15 17.5 0 0 1 0 1 0P. porcus (1) 2201142 42 35 38.5 18 18 18 0 0 1 0 1 0P. porcus (1) 220141 20 29 24.5 25 12 18.5 0 0 1 0 1 0P. porcus (1) – 38 42 40 17 21 19 0 0 1 1 1 0P. porcus (1) 48200 48 40 44 24 19 21.5 0 0 1 0 2 0P. porcus (1) 182152 52 34 43 18 26 22 0 0 1 1 2 0P. porcus (1) 164542 53 44 48.5 22 30 26 0 0 1 1 0 0P. porcus (1) 220411 40 40 40 21 32 26.5 0 0 1 0 1 0P. porcus (1) 220412 45 40 42.5 26 27 26.5 0 0 1 1 2 0P. porcus (2) 220143 16 14 15 27 29 28 0 0 1 0 2 0P. porcus (2) 162850 12 14 13 30 32 31 0 0 1 0 1 0Average 14 34 20.1Sus scrofa (2) 3792 24 30 27 19 23 21 0 0 1 1 1 0Sus scrofa (2) 3799 18 25 21.5 20 27 23.5 0 0 1 0 1 0Sus scrofa (2) 8807 32 25 28.5 23 24 23.5 0 0 1 1 1 0Sus scrofa (2) 22756 25 21 23 24 19 21.5 0 0 1 1 1 0Sus scrofa (2) 22757 20 26 23 23 27 25 0 0 1 0 1 0Sus scrofa (2) 3172 22 25 23.5 25 20 22.5 0 0 1 1 0 0Sus scrofa (2) 3202 26 19 22.5 20 24 22 0 0 1 0 1 0Sus scrofa (2) 3794 28 30 29 25 25 25 0 0 1 1 1 0Sus scrofa (2) 4229 21 24 23 18 25 21.5 0 0 1 0 1 0Sus scrofa (2) 3798 26 25 25.5 21 24 22 0 0 1 0 1 0Sus scrofa (2) 18798 17 22 19.5 17 21 19 0 0 1 0 1 0Sus scrofa (2) 18799 25 21 23 23 24 23.5 0 0 1 1 1 0Sus scrofa (2) 3791 28 28 28 23 26 24.5 0 0 1 1 1 0Sus scrofa (2) 3807 19 23 26 27 25 26 0 0 1 0 0 0Sus scrofa (2) 3808 25 24 24.5 22 24 23 0 0 1 1 1 0Sus scrofa (2) 3920 29 27 28 22 18 20 0 0 1 0 1 0Sus scrofa (2) 53 22 20 21 25 19 22 0 0 1 0 1 0Average 17 24.5 22.7H. meinertzhageni (1) 164227 34 26 30 11 18 14.5 0 0 1 0 0 0H. meinertzhageni (1) 308851 5 11 8 14 16 15 0 0 1 0 0 0H. meinertzhageni (1) 163250 29 35 32 25 18 21.5 0 0 1 0 0 0H. meinertzhageni (3) 81803 18 23 20.5 14 11 13 0 0 0 0 0 0H. meinertzhageni (3) 81803 17 20 18.5 14 16 15 0 0 0 0 0 0H. meinertzhageni (3) 53682 26 29 27.5 18 17 17.5 0 0 1 0 2 0H. meinertzhageni (3) 53678 33 36 34.5 19 23 21 0 0 1 1 1 1H. meinertzhageni (3) 53680 34 36 35 16 17 16.5 0 0 1 0 1 0H. meinertzhageni (3) 53684 34 33 33.5 17 19 18 0 0 1 0 2 0H. meinertzhageni (3) 53679 42 46 44 19 21 20 0 0 1 1 1 1H. meinertzhageni (3) 53681 38 35 36.5 19 22 20.5 0 0 1 0 1 1H. meinertzhageni (3) 53685 23 28 25.5 16 15 15.5 0 0 0 0 0 0Average 12 28.8 17.3Tayassu pecari (3) 74435 50 47 48.5 22 25 23.5 0 0 1 1 1 0Tayassu pecari (3) 74434 52 56 54 22 24 23 0 0 1 1 1 0Tayassu pecari (3) 71738 45 48 46.5 19 23 22 0 0 1 1 1 0Tayassu pecari (3) 147525 45 48 46.5 22 18 20 0 0 1 1 1 1Tayassu pecari (3) 98850 52 55 53.5 28 25 26.5 0 0 1 1 1 1Tayassu pecari (3) 147574 43 40 42.5 27 26 26.5 0 0 1 0 1 1Tayassu pecari (3) 74434 32 36 34 26 28 27 0 0 1 0 1 0Tayassu pecari (3) 71724 34 38 36 19 22 20.5 0 0 1 0 1 1Tayassu pecari (3) 74433 45 49 46.5 19 24 22.5 0 0 1 1 1 1Average 9 45.3 23.5


and for the high-crownedM.modestus, have important consequences foradaptation, habitat preference and diet.

The microwear patterns in this study show browse-dominatedmixed feeding habits for M. modestus on the basis of low numbers ofscratches and the presence of puncture pits on all specimens. Thiscould possibly be due to the replacement of the conical shaped pillarsof the notochoerines by the prismatic pillars of the metridiochoerine(M. modestus), showing greater efficiency of this species during masti-cation dominating other suids in open grass areas (Kullmer, 1999).Based on postcranial locomotor ecomorphology various researcherssuggested that the paleoecological habitat of metridiochoerineswas a closed habitat (Bishop, 1999) and open forests and swamp

environments (White et al., 2006). However, as the result of themicrowear data shows, Metridiochoerus was most likely a mixedfeeder.

The microwear analysis points to varied dietary habits among thethree suid species, revealing different ecological preferences in theBuia Basin around 1.0 Ma. Despite having a brachydont dentition,Kolpochoerus has been reported as a genus which has a less negativeδ18O signal indicating it was more water-dependent, that is, perhaps awet-grass grazer in moister environments (Harris and Cerling, 2002;Bobe et al., 2007) enjoying diets such as roots, tubers and fruits(Cooke, 2007). Its specialized teeth, especially the third molar, mightbe related to reliance on soft grass diet, as this is the case in the

Table 6Ecology and dietary habitat of extant Suidae species. Data from Nowak (1999).

Name Present distribution Habitat Body weight Diet

Suidae

S. scrofa (wild boar) Europe, North Africa and Asia Widespread; vegetation cover areas,open habitats and swamp areas

40–350 kg Omnivorous; fungi, tubers, bulbs, green vegetationand carrion.

P. porcus (Red river hog) West and East Africa Dense vegetation, riverine and mountain 46–130 kg Omnivorous; roots, berries, and fruits. Occasionally,reptiles, eggs and birds. Rooting habits

H. meinertzhageni(Giant forest hog)

Forest zone of Guinea Bissau,SW Ethiopia and North Tanzania

Open wooded savanna, swampforest montane, subalpine areas

130–275 kg Herbi–omnivore; short grass, sedges, shrubs,herbaceous growth. No rooting habits

Tayassu pecari(White-lipped Peccary)

Southern Mexico to NE Argentina Humid tropical forest, savanna andChaco

25–50 kg Omnivorous; fruits, seeds and roots; carrion andsmall vertebrates. Have rooting habit


hyper-browser close extant relativeHylochoerus (Kingdon, 1979; Harrisand Cerling, 2002). For example, the microwear pattern of K.olduvaiensis suggests reliance on soft vegetation diets. According toSolounias and Semprebon (2002), the high-scratch morphospace is oc-cupied by grazers and the low-scratch morphospace by browsers.Therefore, low density of pits and scratches for K. olduvaiensis mightbe related to the browsing dietary habits of the species consistingmost-ly of soft leaves and maybe some grass growing adjacent to a river or alake. Their less hypsodont teeth could be related to more browsing die-tary habits. The analysis shows that K. majus was grass-dominatedmixed feeder due to the high density of pits and scratches. BothKolpochoerus species might have relied on rooting tubers and barkwoods during the season when the soil is moist. The enamel surfacesin M. modestus are dominated by pits, which were probably producedby grit and dust during rooting (Solounias and Semprebon, 2002).

The present ecological habitat and dietary habits of the extant suidspecies have crucial resemblance to the paleoecological habitat oftheir fossil ancestors. The giant H. meinertzhageni, a close relative ofKolpochoerus, is a specialized herbivore. Its giant body (130–275 kg)has interesting ramifications for behavioral adaptations (Harris, 1991)related to swamp areas and/or closed habitats. The Plio-Pleistocene K.olduvaiensis also had a giant body that indicates less reliance on densevegetation for shelter and protection from predators (Harris, 1991).

Fig. 11. PCA showing comparative distribution of microwear features of extinct (KolpochoeruHylochoerus meinertzhageni, and Potamochoerus porcus) suids and the tayassuid Tayassu pecari

Based on our data, the large K. olduvaiensis may have adapted to waterenvironments and adjacent savanna and swamp areas rather thanclosed habitats. The relative reduction in the length of snouts for K.olduvaiensis, conversely to peccaries, might have restricted the speciesto more browsing feeding habits. For example, peccaries eat moreroots than any suid species as represented in the PCA graph (cf.Fig. 11). P. porcus also eat roots, but still the record of density of pits isless than in T. pecari. The fossil speciesM. modestus and K. majus mightalso have been rooting. But K. olduvaiensis like its descendant H.meinertzhageni shows less sign of this kind of habit.

The microwear features support the fact that P. porcus roots morethan H. meinertzhageni does (Solounias and Semprebon, 2002). Thissmall extant Red River Hog is omnivorous (Rothschild and Ruvinsky,1998; Nowak, 1999; Feldhamer et al., 2007) and eats roots, tubers,fruits, carrion and other foods. The body mass of this species rangesfrom 46 to 130 kg (Nowak, 1999). The microwear data show close sim-ilarity of dietary habits of S. scrofa toM.modestus,H.meinertzhageni andP. porcus.

The high density of scratches in T. pecari might be due to theirrooting habits or consumption of fruits using their narrow snouts. Ana-tomically, peccaries have somewhat narrower snouts (and thereforenarrower dental arcades), generally less robust dentition in which thesubsidiary cusps of the molars are reduced, and sharp canine tusks,

s olduvaiensis, Kolpochoerus majus, and Metridiochoerus modestus) and extant (Sus scrofa,.


which curve in a cranial–caudal plane rather than flaring laterally(Hillson, 2005). Males and females are the same size (25 to 50 kg) andthey have clearly defined crown coated with enamel (Hillson, 2005).According to Feldhamer et al. (2007), peccaries are diurnal herbivoresand root with their snouts like pigs; they mainly feed on small verte-brates, eggs, fruits and carrion.

The variation in dental morphology among suid species cannot besolely related to a grazing C4 diet. Our data show no relationship be-tween dental hypsodonty and microwear dietary variations in suidand peccary species. This is most likely related to a decoupling betweenmorphological changes over several generations (evolutionary process)and dietary changes recorded over the last days of life of an individual(microwear). Such discrepancies were observed in other ungulate spe-cies (Semprebon and Rivals, 2007, 2010; Mihlbachler et al., 2011).

6. Conclusions

Dental morphology, tooth microwear, and statistical analysis sup-ported by stable isotope data and faunal richness from the Buia Basin,show intra-specific dietary variation among the suid species. The paleo-ecological factors, diet preferences and masticatory habits might haveresulted in the development of suid progressive dental morphology.The developments of an elongated talonid (K. olduvaiensis) andhypsodont crowns (M. modestus and K. majus) might have permittedthese species to achieve their dietary preferences. For example, the pro-gressive increase in the length, height and number of pillars of the lowerthird molar in K. olduvaiensis and the increase of hypsodonty in bothM.modestus and K.majus species during the Plio-Pleistocene is typically re-lated to their omnivorous dietary habits and, in particular, their specificdifferences in diet. i.e. wet-grass browser and more water dependantbrachydont K. olduvaiensis, hypsodont and mixed-feeder K. majus andless water dependant, grazer and hypsodontM. modestus.

Themicrowear and statistical analyses for the three suid species sup-port extended overlap of dietary habits of the species within themosaicpaleoecological habitat of the Danakil Depression. This might be a re-sponse to harsh paleoecological factors during this time span withinthe Quaternary. However, for some species this could probably be relat-ed to their rooting habits. The large K. olduvaiensis had a different dietfrom the two smaller suid species K. majus and M. modestus, althoughthe two latter suid species show the same dietary habits. This is evi-dence of habitat sharing between the two species K. majus and M.modestus, different from that of K. olduvaiensis. Sharing of the same die-tary habitat by K. majus and M. modestus could probably be related toniche partitioning albeit, taking into account the temporal resolutionin the fossil record, they might not be competing for resources becausethey might not be present exactly at the same time.

Taxonomically and geographically, the suid species from Buia areclosely related to the record of Early to Middle Pleistocene suid speciesfrom East African sites: Bodo, Gona, Daka, Konso. Our study shows closesimilarity of the Buia suids to the chronologically similar Middle Awashsites (Ethiopia). The species inhabited the same geo-paleoecologicalareas. Recent sedimentology studies show that these sites were mainlyformed by the deposition in fluvial and lacustrine environments. Fur-thermore, the chronostratigraphic setting of the Alat Formation andthe contrast between the 1 Ma Eastern Africa arid climate and develop-ment of a lacustrine-dominated scenario in the Dandiero Basin suggeststectonic influence on changes in depositional environments. This condi-tion of environmental change was recorded in all Pleistocene EastAfrican sites. Then, the availability of water and grassland-dominatedlandscapes throughout the extent of the rift valley induced the mam-mals to share the same paleoecological habitat. The anatomical similar-ities of suid species recorded in Buia and Daka is a good example of this.Combined data from isotope, paleontology and sedimentology, supportthe existence of fluvio-deltaic and savanna dominated environments atthe Buia Basin. Therefore, this paleoenvironmental setting could have

been attractive for the suid species and other largemammal fauna to oc-cupy extended territories, hence varied dietary habits.

The persistent climatic variability during Early and Middle Pleisto-cene times affected omnivorous species including hominins over timeto face major possible trends-adaptation and/or dispersals- for betterdietary preferences. Within the late Early to Middle Pleistocene Buiamammalian fauna, suid species show diverse taxonomic developmentsfairly rapidly. Their dental anatomy showed a special evolutionary trendthat allowed them to respond to harsh and cyclic paleoenvironment indifferent geo-ecological habitats during the Quaternary. The last repre-sentatives of these species are found in the Middle Pleistocene, albeitdescendants of a number of these species have survived until the pres-ent day.

Acknowledgments

This work has been funded by grants of the Atapuerca Foundation(to T. M.), the Spanish Ministry of Economy and CompetitivenessCGL2010-15326/BTE and HAR2013-48784-C3-1-P, Generalitat de Catalu-nya GENCAT 2014 SGR 901, the European Commission's Research Infra-structure Action via the SYNTHESYS Project AT-TAF-4385 (to FR), theL.S.B. Leakey Foundation (to LR), the National Geographic Society(7946/05 to LR), and the Wenner Gren Foundation (7575/06 to LR).We further acknowledge the Eritreo-Italian (Buia Project) collaborativeproject (sponsored by Eritrean National Museum) and supported byItalianMIUR (ItalianMinistry for University and Education, to E. AbbateandM.Ghinassi), Grandi Scavi Archeologici Univ. “La Sapienza” of Rome(to A. Coppa), and MAE (Italian Ministry for Foreign Affairs, to LR).Sergio Ros-Montoya helped in the preparation of the figures. Finally,we genuinely thank Gina Semprebon for providing uswith unpublishedpeccary microwear data.

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