80 2011 roksandic et al homo mala balanica

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A human mandible (BH-1) from the Pleistocene deposits of Mala Balanica cave(Sicevo Gorge, Nis, Serbia)

Mirjana Roksandic a,*, Dusan Mihailovic b, Norbert Mercier c, Vesna Dimitrijevic b, Mike W. Morley d,Zoran Rakocevic e, Bojana Mihailovic f, Pierre Guibert c, Jeff Babb g

aDepartment of Anthropology, University of Winnipeg, 515 Portage Avenue, Winnipeg, MB, R3B 2E9 CanadabDepartment of Archaeology, Faculty of Philosophy, Belgrade University, Cika Ljubina 18-20, 11000 Belgrade, SerbiacCentre de Recherche en Physique Applique lArchologie, Universit de Bordeaux Maison de lArchologie 3607 Pessac cedex, FrancedHuman Origins and Palaeo-Environments (HOPE) Group, Department of Anthropology and Geography, Oxford Brookes University, Gipsy Lane, Oxford OX3 0BP, UKeCenter for Digital Radiography, Faculty of Dentistry, Belgrade University, Rankeova 6, 11000 Belgrade, SerbiafNational Museum, Trg Republike 1a, 1100 Belgrade, SerbiagDepartment of Mathematics and Statistics, University of Winnipeg, 515 Portage Avenue, Winnipeg, MB, R3B 2E9 Canada

a r t i c l e i n f o

Article history:Received 23 October 2009Accepted 21 February 2011

Keywords:NeandertalArchaic Homo sapiensEuropean hominin dispersalsCentral Balkans

a b s t r a c t

Neandertals and their immediate predecessors are commonly considered to be the only humans inhabitingEurope in the Middle and early Late Pleistocene. Most Middle Pleistocene western European specimensshow evidence of a developing Neandertal morphology, supporting the notion that these traits evolved atthe extreme West of the continent due, at least partially, to the isolation produced by glacial events. Therecent discovery of a mandible, BH-1, from Mala Balanica (Serbia), with primitive character statescomparable with Early Pleistocene mandibular specimens, is associated with a minimum radiometric dateof 113 72 43 ka. Given the fragmented nature of the hemi-mandible and the fact that primitivecharacter states preclude assignment to a species, the taxonomic status of the specimen is best described asan archaic Homo sp. The combination of primitive traits and a possible Late Pleistocene date suggests thata more primitive morphology, one that does not show Neandertal traits, could have persisted in the region.Different hominin morphologies could have survived and coexisted in the Balkans, the hotspot ofbiodiversity. This rst hominin specimen to come from a secure stratigraphic context in the CentralBalkans indicates a potentially important role for the region in understanding human evolution in Europethat will only be resolved with more concentrated research efforts in the area.

2011 Elsevier Ltd. All rights reserved.

Introduction

The settlement of Europe has a long history, with homininspresent at the gates of the continent in Dmanisi (Georgia) as early as1.7millionyears ago (Gabunia et al., 2000). The recent recognition ofseveral new species of Homo in Europe, including H. georgicus(Gabunia et al., 2002) in Dmanisi, Georgia, H. antecessor (Bermdezde Castro et al., 1997) in Atapuerca, Spain, and H. cepranensis fromCeprano in Italy (Mallegni et al., 2003), as well as H. heidelbergensis(Schoetensack, 1908), suggests considerable diversity in the Euro-pean hominin record. While western European specimens from the

Middle and Late Pleistocene show derived Neandertal traits, this isnot necessarily true for the East and the South of the continent. Theexistence of areas of refuge in the Mediterranean peninsulas couldhave played an important role in maintaining the variability ofhominins in Europe, bya combination ofmigratory pulses and in situevolution.With a revised date, the Ceprano skull from the ApenninePeninsula could be regarded as one example where primitivemorphology persisted into the Middle Pleistocene (Muttoni et al.,2009). As a result, the peopling of Europe in the Pleistocene mayhave been very complex and the current fossil recordmay representany number of different genetic processes including drift, foundereffect, directional adaptation and hybridization. Reconstructinghuman evolution in the regional European context is thereforeinseparable from understanding the migrations of early homininsinto the area and their later movements into and out of Europe. TheBalkan Peninsula, with its river valleys used as migratory routes foranimals and humans in prehistoric as well as historic times, repre-sents themost likely corridor fromAsiaMinor into Europe and is no

* Corresponding author.E-mail addresses: [email protected] (M. Roksandic), [email protected]

(D. Mihailovic), [email protected] (N. Mercier), [email protected](V. Dimitrijevic), [email protected] (M.W. Morley), [email protected](Z. Rakocevic), [email protected] (B. Mihailovic), [email protected](P. Guibert), [email protected] (J. Babb).

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Journal of Human Evolution

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0047-2484/$ e see front matter 2011 Elsevier Ltd. All rights reserved.doi:10.1016/j.jhevol.2011.03.003

Journal of Human Evolution 61 (2011) 186e196


doubt of extreme importance in understanding Paleolithic migra-tions (Mihailovic, 2009; Dennell et al., 2010). However, the regionhas a very limited Paleolithic research history and very few fossilnds (for a recent overview of Paleolithic research in Greece seeHarvati et al., 2009). New systematic prospection of several regionsin Serbia and excavations of newly identied Paleolithic sites(Mihailovic, 2008) (Fig. 1a), show that the dearth of fossil evidencefrom southeast Europe should be attributed to the lack of systematicresearch in the area.

A recently discovered hominin fossil fromMala Balanica1 cave isthe rst hominin specimen in the Central Balkans recovered fromcontrolled excavations with rm stratigraphic context. Here, wepresent a detailed description of the partial human hemi-mandiblefrom Mala Balanica (BH-1) in its stratigraphic context and discussits potential signicance. The preservation of the specimen (seebelow) precludes a more complete analysis of its species status,while its primitive morphology raises questions about the role thatthe Balkan Peninsula, the least researched glacial refugium inEurope, played in hominin evolution on the continent.

Geoarchaeological and cultural context

Mala Balanica (N4320.2110, E2205.1150) is an elongate karsticchamber, 8 m wide, 25 m deep and 2.8 m high, measured from thepresent-day surface in the interior of the cave. The site is situated atan elevation of 332 m above sea level, approximately 100 m abovethe Nisava River, with the cave mouth facing SSW across the valley(Fig.1b). It is separated by a distance of 7m from the entrance to thelarger Velika Balanica cave with which it forms the Balanica CaveComplex. The cave complex is situated on the southern slopes ofthe Svrljig Mountain chain, formed of Cretaceous and Jurassiclimestone in the area where the Rodop Mountains meet theyounger chains. The Sicevo Gorge is cut through by the Nisava River,which provides an important communication between two

adjoining river valleys. Situated at the exit from the gorge, the cavesare both easily accessible and secluded, as is often the case withMiddle Paleolithic localities (Mellars, 1996). Today the catchmentarea is characterized by a moderate continental climate withdeciduous, oak-dominated forests. The site is situated in an activekarst setting (Woodward and Goldberg, 2001) and is subject togroundwater inltration through cracks and ssures in the hostbedrock. The present development of the cave system appears to bedriven primarily by solution through inltration and colluvial slo-pewash processes.

In 2005, a test excavation of a small 2 m2 area near the westernwall of the cave identied a number of quartz artifacts and Quinascrapers immediately below the present-day surface, and revealeda clandestine pit in the southwest corner of the cave. During thefollowing four seasons, the excavation of artefact-bearing layers(averaging 30 cm in depth) was extended to a 12m2 surface (Fig. 2),and the backll from the clandestine excavations was cleared. Thelatter allowed us to expose a prole over 2 m below site datum,which was subsequently used to gather geoarchaeological andpalaeontological information (Table 1; Fig. 3).

In very broad terms, the stratigraphy exposed in the studiedprole comprised well-bedded, horizontal to sub-horizontal layersof limestone gravel contained within a silt- and sand-dominatedmatrix, with major variations in the ratio of coarse (gravel) to ne(silt-dominated) components. The prole has been bulk sampledfor detailed geoarchaeological analysis, which will provide impor-tant paleoenvironmental context to the archaeological materialrecovered from this area of the site, including the BH-1 mandible.This work is currently ongoing and the results will be presentedelsewhere. For the purposes of the current paper, the stratigraphicsuccession will be described in terms of eld observations madeduring detailed sediment logging as part of both the archaeologicaland geoarchaeological eldwork.

The exposed sequence has been divided into three facies withthe aim of describing groups of sedimentary units with similardepositional (and post-depositional) histories. These facies aredifferentiated chiey by colour, composition and the inclusion of

Figure 1. The context of the nd: (a) Map of Southeast Europe indicating sites with fossil human remains: 1 Krapina, 2 Vindija, 3 Crvena stijena, 4 Balanica, 5 Bacho Kiro, 6Petralona, 7 Theopetra, 8 Lakonis, 9 Apidima. Small letters indicate newly discovered Paleolithic sites in Serbia (aeh) and Monte Negro (iek) without hominin fossils. (b) Thelocation of Balanica cave complex in the Sicevo Gorge.

1 pronounced Balanitza.

M. Roksandic et al. / Journal of Human Evolution 61 (2011) 186e196 187


anthropogenic material (e.g. lithics). Facies 1 is a thin (c. 15 cm),sub-horizontal layer of silt and limestone clasts, which representsHolocene and sub-recent deposition at the top of the sequence.Facies 2 (a e h) is characterized by clast-supported, coarse angularto sub-angular gravels held within a matrix of reddened silts andsands. Facies 3 (a e c) is typied by matrix-supported, sub-angularto sub-rounded gravel in a matrix of brown silts and sands. At thebase of the sequence, unit 3c consisted of ne-grained silts andclays, some of which were well-cemented, with a paucity of lime-stone clasts. Facies 2 and 3 represent Pleistocene accumulation.

At the macroscopic level, the sequence is essentially minero-genic in nature, with no major organic component within thesedimentary matrix except for occasional faunal material.

Unequivocal evidence of human activity was noted only in Facies 2(aec), which could be the result of the very limited excavation areain which the prole was observed, as well as the limited depth ofthe excavation in the remainder of the squares. Animal bones arepresent throughout the sequence, although they are less commonin Facies 2de2h. Though the physical characteristics of the litho-logic units are relatively uniform, a number of preliminary obser-vations concerning the sedimentary sequence can be made. Fromthe base of the sequence upwards there is a general trend towardscoarser sedimentary components, with the frequency of medium tolarge limestone clasts increasing towards the base of Facies 2. Unit3c, at the base of the sequence, comprised well-cemented, ne-grained silts and clays, suggestive of a wetter climate, possibly with

Figure 2. Surface contours of the cave with the excavation grid. Inset shows the details of the excavation area where the specimen was found.

Table 1Features of the sedimentary layers at Mala Balanica.

Layer Summary characteristics of lithologic facies and units Archaeological material Faunaa

1 Friable clay silt with mod-freq, sub-angto sub-r, ne-medium limestone gravel.

Recent and sub-recentmaterial, charcoal

Ovis aries

2a Mod compact silt with mod-freq,ang to sub-ang, ne-med limestone gravel.

Present only near theWestern wall of the cave,Middle Paleolithic artefacts

Canis lupus, Felis silvestris Schreber,Cervus elaphus, Capra ibex.

2b Friable silt with freq med-large, ang to sub-ang, limestone clasts.Clast frequency increases towards base.

Throughout the cave, MiddlePaleolithic artefacts, charcoal

Castor bre, Lepus sp., Canis lupus,Ursus sp., Panthera pardus,Felis silvestris.

2c Clast-supported, poorly sorted, ang to sub-ang,ne-med limestone gravel in a silt matrix

Present sporadically, MiddlePaleolithic artefacts, charcoal

Apodemus sp., Castor bre,Ochotona pussila, Canis lupus,Vulpes vulpes, Martes martes,Mustelidae indet., Ursus arctos,Ursus sp., Crocuta spelaea,Felis silvestris, Cervus elaphus,Dama dama, Capreolus capreolus,Rupicapra rupicapra, Capra ibex.

2d Mod compact, slightly sandy silt with mod-freq, sub-ang to sub-r,ne limestone gravel e coarser towards base.

Very few artefacts in thetopmost segmentof the layer, no charcoal

2e/2f Mod compact sandy silt with occ-mod,ne-med, sub-ang to sub-r limestone gravel.

No artefacts, no charcoal

2g Matrix-supported, mod-sorted, ang to sub-ang, ne limestone gravel in asandy silt matrix. Appears clay enriched and more compact towards base.Freq degraded limestone fragments and ecks


2h Matrix-supported, mod-sorted, ang to sub-ang, ne-med limestonegravel in a silt matrix. Clast size increases towards base


3a Matrix-supported, poorly sorted, sub-ang to sub-r, med-coarselimestone gravel in a calcareous sandy silt matrix. Freq CaCO3 inclusions.Mod-freq large bone frags

No artefacts, no charcoal Ursus arctos, Ursus sp., Equus sp.,Capreolus capreolus.

3b Matrix-supported (occ clast-supported towards upper contact),mod to poorly sorted, ang to sub-r, ne to medium (but occ coarse)limestone gravel. Darker and less calcareous than layer 3a

No artefacts, no charcoalLayer in which the BH-1mandible was found

Canis sp., Ursus sp., Crocuta spelaea,Cervus elaphus, Dama dama, Capra ibex.

3b0 Very well carbonate-cemented silt with occ ne gravel. Also containsnodular calcium carbonate inclusions whichrest on upper contact of underlying layer

No artefacts, no charcoal Canis sp., Ursus sp., Crocuta spelaea,Cervus elaphus, Dama dama, Capra ibex.

3c Dark, compact silty clay with occ poorly sorted, ne-med limestone No artefacts, no charcoal Carnivora indet., Cervus elaphus

Abbreviations are as follows: occ (occasional); mod (moderate); freq (frequent); ang (angular); r (rounded).a Additionally, the following taxa were identied from mixed contexts: Meles meles (Linnaeus), Bos/Bison.

M. Roksandic et al. / Journal of Human Evolution 61 (2011) 186e196188


water pooling at the site. Unit 3b appeared clay- and ne silt-enriched towards its base, again indicating a wetter climateallowing ne-grained allogenic sediments to be washed into thesite. The limestone clasts observed in Facies 3 were rounder thanthe angular to sub-angular clasts of Facies 2, implying partialdissolution as a consequence of the throughput of percolatinggroundwaters. With the coarse angular gravel of Facies 2 typifyinga cooler climate where cryoclastic processes promoted the gener-ation of eboulis-like autogenic sediments (though issues of equi-nality should be borne in mind, see Bailey and Woodward, 1997),preliminary observations advocate a warm e cooling phase repre-sented in the Facies 3e2 up-prole sequence. This proposal wouldbroadly concur with the faunal observations of warm-adaptedspecies recovered from unit 3b. A marked variation was alsoobserved in the unit-to-unit variability in carbonate content. Thisparameter can be used as a paleoenvironmental proxy in identi-fying warmer, wetter climatic episodes (Woodward, 1997;Woodward and Goldberg, 2001; Schuldenrein, 2001; Straus et al.,2001) and this may help rene the paleoenvironmental recon-struction at a later stage. At present it is unknown whether thesecarbonates are primary (e.g., aeolian carbonate silt) or secondary(i.e., reprecipitated).

Stratigraphic context of the nd

The mandibular specimen, BH-1, originated from layer 3b,characterized by the presence of larger animal bones, fewer andless angular limestone clasts, and no other evidence of anthropo-genic activity. BH-1 was situated 1.5 m below the lowest recordedartifacts. The layer inwhich the specimenwas found was excavatedon a very restricted surface below the clandestine pit. The bottomof

the clandestine pit was reached at the top of layer 3b, in squares E,F, G 19/20; consequently, the pit did not disturb the underlyingsediments. Controlled excavation in squares D18a, b and E18d failedto reach bedrock and the stratigraphic sequence continues belowthe current level. The specimen was found in square D18, layer 3b,three arbitrary 5 cm spits below the base of the clandestine pit. Themandible was removed together with some adjoining sediment.Other animal bones and nodular calcium carbonatewere found andrecorded in situ in the same layer. No other fragments of bone werefound in the faunal material from this and the surrounding exca-vation loci. The faunal remains showed the same adhered sedimentand colouration as observed on the mandible. While the areaexcavated is small and a detailed site formation reconstruction iscurrently beyond our reach, there is no indication that the strati-graphic sequence at this particular part of the cave was disturbedby geological, anthropogenic or biogenic processes. Fragmentationof faunal material, evidence of gnawing by carnivores and rodents,and the general uniform slope of the sediments towards thewestern wall throughout the excavated area, indicate that accu-mulation could have originated towards the middle of the cave,gradually fanning out towards the sides of the cave. Evidence ofwater logging on the mandible cannot be readily interpreted; itcould be due to a relatively long exposure prior to burial, or to thewater pooling in layer 3c suggested by geoarchaeological obser-vations, or a number of other factors.

Fauna from the Mala Balanica cave

Animal bones are present throughout the cave sequence. Thebones and teeth of large mammals are well preserved, but highlyfragmented. Many are damaged by carnivore and rodent gnawing.

Figure 3. The prole excavated along the northern wall of the clandestine pit. Sedimentary units are described in Table 2. Layers 2ae2c produced Mousterian artifacts, layer 3Bproduced the hominin mandible, BH-1.



Some fragments have polished surfaces and randomly distributedstriations that are probably due to trampling of the bones and bonefragments, and their friction with the sediment particles. Anthro-pogenic modications are visible from layers 2a to 2d as traces ofre damage and cut- and chop-marks on animal bones. Given thesmall area from which the faunal material has been excavatedbelow these strata, it is hard to ascertain whether the lack ofanthropogenic modications in the lower strata is genuine.

The identied taxa are listed in Table 1. Because of the limitedvolume of excavations in the lower levels and the low yield offaunal remains, it is not yet possible to conclude whether there aresignicant differences in faunal composition throughout thesequence. In layers 2ae2c, the most numerous remains are of ibex,represented by cranial and postcranial elements of several adultand juvenile animals. Preliminary morphometric analysis points toa large-sized ibex, which is commonly found in Upper Pleistocenecave deposits in Serbia (Dimitrijevic, 1997). In terms of the pre-vailing environmental conditions, the most important taxa are twocervid species, roe deer (Capreolus capreolus) and fallow deer(Dama dama). Both are present in layers 3 and 2c - 2h and disappearin layers 2a and 2b. Both species were more common in warm thanin cold stages of the Pleistocene, and preferred a wooded habitat.Fallow deer were completely absent in Last Glacial deposits inSerbia (OIS 2e4), while roe deer were absent frommost of the siteswhere Last Glacial age was ascertained (Dimitrijevic, 1997). Thefallow deer nds from layers 3 and 2 correspond in size to LastInterglacial Dama dama, the species considered characteristic of theUpper Pleistocene interglacials (Gibbard, 2003). The appearance ofmurids (Apodemus sp.) suggests interglacial afnities for the lowerportion of the sequence, as cave deposits of the Last Glacial inSerbia are dominated by steppe species of arvicolids and cricetids(Dimitrijevic, 1997). The presence of the typical steppe speciesOchotona pusilla in the upper portion of the sequence indicateschanges towards a more open landscape.

A possible interglacial origin for layers 3ce3a would also besupported by the sedimentology, as the ne-grained sediments of3c immediately below the layers from which the mandible wasfound, suggest a warmer, wetter climatic regime with a coolingtrend towards upper levels of the sequence. Calcium carbonatelevels appear to increase from 3b to 3a, which could indicatea reduction in the throughput of percolating groundwater, alsosuggested by the increase in angularity of the gravel noticeable inlevels 3a up to 2g.

Materials and methods

The mandibular preservation and morphology are describedfollowing the terminology of Rosas (1995). The CT scan was per-formed at the Centre for Radiological Diagnostics (University ofBelgrade) using a Siemens multi-slice Somatom sensation 16scanner to obtain sections (interslice distance 0.75 mm) in axial,sagittal and frontal planes, and were used subsequently to createa 3-d reconstruction.

The radiometric date of the mandible was obtained by theU-series method and, in particular, the disequilibrium between theuranium and thorium radioelements (Table 2). We applied a non-destructive approach by detecting the gamma rays emitted fromthe specimen itself by the decay of radioelements of the U-serieschain. The mandible was placed directly on a broad energyGermanium detector (thickness 30 mm, diameter 76 mm) foralmost two weeks. As gamma rays have a long freepath throughmatter, they can be detected with a low background Germaniumdetector; the analysis is consequently non-destructive. The leadscreen surrounding the detector and the mandible allowed us todetect the following gamma ray emissions: 234Th (63.3 and

92.8 keV), 234U (53.2 keV), 234mPa (1001.0 keV), 235U (185.8 keV),230Th (67.7 keV), 214Pb (53.2, 295.1 and 351.9 keV), 214Bi (609.3 and1120.3 keV) and 210Pb (46.5 keV). In addition, we recorded thegamma rays coming from radioelements of the Th-series chain(228Ac, 212Bi, 212Pb, 208Tl). To obtain a reference standard, wesubmitted a cast of the specimen made of a natural clay rich inradioelements of the U-series chain. This clay is used as a referencestandard because its radioisotopic contents are well known. Sincethe cast had the same shape and size as the mandible, the gammaspectrum recorded during the measurement of the mandible couldbe compared with the gamma spectrum recorded for the cast. Asthe radioisotopic contents of the cast are known, by comparison ofthese two spectra, it is possible to deduce the radioisotopiccontents of the mandible, and consequently its age (see Table 2).The age estimate of the mandible was calculated assuming an earlyuptake model for the uranium, i.e., one in which this radioelementpenetrated the fossil in a relatively short time in comparison to theburial duration. Since this assumption cannot be conrmed inde-pendently, the radiological age should be understood as theminimum date for the specimen. The date obtained was comparedto faunal and geoarchaeological data to help estimate the age of themandibular specimen.

Statistical procedures

Cluster analysis was run for morphological traits of BH-1 and 26specimens reported in Mounier et al. (2009) that had all of the 16variables observable in BH-1: variables IeL and NeU and variablesOO, PP, QQ and UU (as dened inMounier et al., 2009: Table 5, Fig. 1and Table 11, Fig. 1, respectively). An agglomerative hierarchicalclustering procedure was applied using the average linkage crite-rion, which measures the similarity between any two clusters asthe mean of the similarities between the objects in one cluster andthe objects in the other cluster. The distance measure wasEuclidean distance, applied to non-standardized data. To evaluatethe extent to which the dendrogram reects the relationships inthe original distance matrix, we calculated the coefcient ofcophenetic correlation, which represents the linear correlationbetween entries of the original distance matrix and corresponding

Table 2Activities of 234Th, 234U, 234mPa, 235U, 230Th and 214Bi were determined in analyzingthe gamma ray lines whose energies are given in the text.

U-238 (p.p.m.) U-234/Th-232 Th-230/U-234 Age (ka)

2.86 0.04 80 0.649 0.170 113 72 43The radioisotopic contents of the natural clay used for making the cast were alsodetermined by gamma spectrometry in using the GSN (granite) standard and cor-rected for taking account of the difference in densities between the clay and the GSNstandard.

Table 3Hominin fossils used in cluster analysis with assigned groupings. FromMounier et al. (2009).

Early Pleistocene (EP)Homo erectus s.l.: D211, D2600, Sangiran1b (S1b), KNM-ER 992Homo antecessor: ATD6-96

Middle Pleistocene (MP)Homo erectus: (s.l.) Tighenif 1 (T1), Tighenif 2 (T2), Tighenif 3 (T3),

Sinanthropus H1 (SH1)Homo heidelbergensis or Pre-Neandertals: Mauer, AT-888, AT-950,

Arago II (ARII), Arago XIII (AR XIII), Montmaurin, Ehringsdorf F (Eh F)

Upper Pleistocene: Neandertal (NT)(NT): Krapina J, Krapina G, Spy 1, Shanidar I, Regourdou, Baolas,

La Ferrassie 1, La Quina H5, Amud 1, Zafarraya



entries of the cophenetic matrix of merge distances betweentaxonomic units (Sneath and Sokal, 1973). The specimens that wereavailable for statistical analysis are listed in Table 3 and 4.

Results

Radiometric dating of the specimen

Despite the outlined limitations of the dating method, themandible can be attributed a minimum age of 113 72 43 ka.This large uncertainty has two main origins: the counting statisticsof the 230Th (67.7 keV) peak remains low despite the two weekduration of the experiment, and the 234U (53.2 keV) peak is largelydominated (in a ratio of about 1:10) by 214Bi gamma rays emitted atalmost the same energy. This age estimate, however, must beconsidered as a minimum age since there is no independent eval-uation for the validity of the assumed early uptake model. Contraryto this assumption, the activities of the post-230Th radioelements(214Pb, 214Bi, 210Pb), which are about three times lower than the230Th activity, suggest that the 226Ra and/or its daughter, 222Rn,were mobile during at least the last 10 ky. Since there is nocomplementary information for older periods, we need to take intoaccount the possibility that part of the uranium was also mobileduring the burial time.

Lithic industry (Fig. 4)

Only layers 2ae2d show unequivocal evidence of human activityin the form of stone tools, charcoal fragments and cut-marks onanimal bones. Lithic analysis of the material from both caves of theBalanica complex identied the presence of different facies of theMousterian. The industry of Mala Balanica is limited, with only 102artefacts, of which 93% were excavated from layers 2ae2c, with anoverall depth of 20 cm. Artefacts made of quartz predominate(81.4%), the Levallois technique is completely absent, and retouchedartefacts represent 26.7% of the assemblage. Scrapers, some with

typical Quina retouch, are the most common tool type (62.1%), whiledenticulates represent 24.1% of the lithic sample. Though limited inscope, the industry of Mala Balanica is consistent with Charentian-type Mousterian (Fig. 4). This facies is ascertained on a much largerscale in the adjoining Velika Balanica cave (Mihailovic, 2008, 2009).Charentian-type Mousterian, present in both Balanica caves, has notbeen previously conrmed south of the Sava and the Danube Rivers,although it is known in adjoining areas, both in Central Europe(Betalov Spodmol, Erd, Krapina) and in Anatolia at Karain Cave. Thisfacies cannot be associated with a particular chronological period;the Proto-Charentian at Karain (complex BeE) was tentatively datedto 300e330 ka (Koz1owski, 2002), Krapinawas dated to 130 ka (Rinket al., 1995; Simek and Smith, 1997), while Betalov Spodmol and Erdcould be as late as 40 ka (Gbori-Csnk, 1968; Osole, 1991). TheCharentian industry found at the site could represent an early phasein the development of the Middle Paleolithic in the Central Balkans,a regional facies, or a particular type of site use by human pop-ulations in the area.

Geoarchaeological, archaeological, and faunal data seem toindicate an Early Upper Pleistocene age for the entire sequence. Thelower portion of the sequence (layers 3ce3a) is consistent witha wooded habitat and likely represents a relatively mild and wetperiod compatible with OIS5 (e, c, a). In the upper portion of thesequence, we observe a cooling trend and the presence of steppespecies, indicating changes towards a more open landscape. Thiscould be related to environmental changes at the beginning of theLast Glacial, i.e., OIS 4. This would be in accordance with theradiometric date of 113 72 -43 years for the lower layers.However, until the ESR and U-series dates are available, we cannotexclude the possibility that the nd could be older.

The BH-1 specimen

The BH-1 specimen is a 67 mm long left hemi-mandible,preserved from the posterior margin of the canine alveolus to themesial aspect of the ascending ramus with all three molars present

Table 4Data used in the cluster analysis.

# G Specimen I J K L N O P Q R S T U OO PP QQ UU

1 UU BH-1 3 1 1 2 2 1 1 2 1 2 2 3 2 2 2 12 EP D211 3 2 1 1 2 1 2 2 1 2 3 2 1 2 2 13 EP D2600 1 2 1 1 3 2 2 2 2 2 2 2 2 1 2 14 EP Sangiran1b 3 2 1 2 2 2 1 2 1 2 2 2 2 2 2 15 EP KNM-ER992 3 1 1 3 2 2 1 3 1 2 2 2 1 1 2 16 EP ATD6-96 3 2 1 2 2 1 1 2 1 2 2 2 2 1 2 17 MP Tighenif 1 3 2 1 1 2 1 2 3 1 2 1 2 1 1 2 18 MP Tighenif 2 3 1 1 2 2 1 2 2 2 2 2 2 2 1 2 19 MP Tighenif 3 3 2 2 2 3 2 2 3 2 2 1 3 1 1 2 110 MP Mauer 2 2 2 2 3 2 2 3 3 2 1 3 1 1 2 111 MP AT-888 3 1 3 1 2 1 2 2 3 3 1 2 3 1 2 112 MP AT-950 3 2 2 1 3 2 2 3 3 3 1 2 1 1 2 213 MP Arago II 3 1 3 1 2 2 1 3 3 2 1 3 1 2 2 214 MP Arago XIII 3 2 2 1 2 1 2 3 2 2 1 2 1 1 2 215 MP Montmaurin 3 2 2 2 2 2 1 2 2 2 1 2 2 1 2 216 MP Sinanthropus SH1 3 2 2 2 3 2 2 2 2 3 2 1 2 2 2 117 MP Ehringsdorf F 3 2 3 2 2 1 2 1 3 3 1 1 1 2 2 218 NT Krapina J 3 2 3 1 3 2 2 2 3 3 1 1 3 1 1 119 NT Krapina G 3 2 3 2 3 2 2 1 3 3 1 1 3 3 2 220 NT Spy 1 2 1 3 2 1 1 1 2 3 3 1 2 3 2 1 221 NT Shanidar I 2 1 2 1 3 2 2 2 3 3 1 2 3 1 1 222 NT Regourdou 3 2 3 1 2 1 2 1 3 3 1 2 3 1 1 123 NT Banolas 3 1 2 3 3 2 2 3 2 3 2 1 2 1 1 224 NT La Ferrassie 1 3 2 3 2 2 2 1 2 3 3 1 1 3 3 1 225 NT La Quina H5 3 1 2 1 2 1 2 1 3 3 1 2 3 3 1 226 NT Amud1 3 1 3 1 2 1 2 1 3 3 1 2 3 1 1 127 NT Zafarraya 3 2 3 1 3 2 2 1 2 3 1 1 3 2 1 1

G (Grouping): UU (Unknown), EP (Early Pleistocene), MP (Middle Pleistocene), NT (Neandertal). Data for 27 specimens on 16 variables representing 12 selected morphologicalcharacteristics of the lateral face of the corpus (I through L, and N through U) and four morphological characteristics (OO, PP, QQ and UU) of the medial face of the mandibularcorpus described by Mounier et al. (2009).



in their sockets. The lower half of the mesiolingual root of the M3 ismissing and the remaining roots are exposed due to the destructionof the adjacent endomandibular lamina. The mesial portion of themandible shows an old breakage lled with sediment, whereas allof the breaks on the distal end are fresh. The alveoli of the P3 and P4are complete and are for the most part lled with sediment, whilethe posterior portion seems to have been subject to water inl-tration resulting in substantial fragility that, together with thedamage sustained during excavation, could explain its poor

preservation. The posterior portion of the mandible was recon-structed by retting the fragments with small amounts of ParaloidB72 dissolved in acetone. One positively identied small fragmentcould not be retted because it had no direct contact with the restof the bone.

Age and sex

Complete eruption and closure of the root apex of the M3 indi-cate an adult individual, while minimal wear on the M3 and slightto moderate wear on theM1 andM2 each suggest a relatively youngadult. Given the mandibles unclear taxonomic position, it isimpossible to determine the sex of the individual.

Exomandibular aspect (Fig. 5a)

The BH-1 mandible is lacking the symphyseal region and thepresence/absence of themental eminence could not be ascertained.In the lateral view, the basal and alveolar margins are almostparallel. The mandible shows only very faint relief in the exo-mandibular view. The superior marginal torus is poorly dened. Itis represented by a slight change in the orientation of the lamina tothe axes of the horizontal branch above and below the mentalforamen. It transitions smoothly into the lateral prominence,located at the level of M1/M2, equidistant from the alveolar andbasal margins. The ascent of the oblique line begins just above theposterior marginal tubercle, 18.5 mm below the alveolar border atthe level of M1/M2 vertically, and the mental foramen horizontally.While the position is the same as in a comparative sample ofmodern humans, the ascent is not as steep. The lateral prominenceis more anterior than in Neandertal and pre-Neandertal samples,where it is commonly located under the M3 (Rosas, 2001). Thefragment of the exomandibular lamina of the vertical branch, whichcould not be retted but could be identied on the basis of thevisible interior structure of the mandibular canal, shows very slightrelief at the masseteric fossa, with no pronounced rugosities.The reconstructed root of the vertical branch does not indicate the

Figure 4. A sample of tools from Mala Balanica layers 2a-2c: Transverse (a,b) andlateral scrapers (c,d) made of quartz (a) and int (bed).

Figure 5. The BH-1 specimen: (a) exomandibular view, (b) endomandibular view, (c) occlusal view, (d) dentition: from left to right M1, M2 and M3. Mesial (m) is up, distal (d) isdown, buccal (b) is left, and lingual (l) is right. Scale in centimetres.



presence of a retromolar space. However, it does not obscure theM3in lateral view. This is most likely due to a wide extramolar sulcus,as the vertical branch overlaps with the edge of the M3 in theocclusal view.

The mental foramen is situated below the P4 alveolus, 17.0 mmfrom the alveolar margin and 16.4 mm from the basal margin. It isoval in shape, set obliquely to the sagittal and transverse planes,andmeasures 5.2mmby 2.9mm. In contrast, themental foramen islocated under theM1 in up to 80% of Neandertal specimens and 54%of the Middle Pleistocene samples from Sima de los Huesos (Rosas,2001). This position is often interpreted to be a reection of thedevelopment of marked midfacial prognathism (Quam and Smith,1998). The more anterior position of the mental foramen in thisspecimen and the possible absence of a retromolar space, bothplesiomorphic traits observable in Homo erectus, indicate that themandible lacks autapomorphies of Neandertals and their MiddlePleistocene precursors. Similarly plesiomorphic is the equidistantposition of the mental foramen in relation to the alveolar and thebasal margins. The anterior marginal tubercle could not beobserved in this specimen, as the basal margin is missing mesiallyfrom below the mental foramen.

Endomandibular aspect (Fig. 5b)

The internal lamina is preserved from the canine alveolus to theM2/M3 septum in the alveolar portion, and from below the P3/M1septum to below the mesial edge of the M3 alveolus in the basilarborder. There is visible aking and root etching all over the endo-mandibular surface. The mesiolingual root of the M3, the linguallamina of the M3 alveolus, and the adjacent area above the basilaredge are missing. A trowel mark can be observed on the M3 and theinterior lamina.

While the bone is robust, the relief of the internal surface is notmarked. The alveolar border shows thickening on the lingual sidefrom P3 toM2 (and possibly beyond), forming amandibular torus justbelow the alveolar process. The width of the alveolar processdecreases mesially. The width of the subalveolar plane increasestowards themiddle portion of themandible, forming a shelf-like area(planumalveolare) thatextends frombelowtheP3 towards the caninesand the symphysis, best observed in the occlusal view (Fig. 5c). Themesial endomandibular increase in width is observable towards theupper third of themandibular height below the alveolar border. Sincethe lower portion of the mandible is broken in the canine area, wehave combined overlapping CT images at the canine alveolus and atthemental foramen showing thickening at the level of the canine andan oblique rather than subvertical alveolar planum (Fig. 6).

The subalveolar plane (sublingual fossa) is at rather thanconcave. The prole of the submandibular fossa is moderatelyconcave. The expression of the mylohyoid line is moderate, and is

noted as a change in orientation between the subalveolar plane andthe submandibular fossa rather than a sharply delineated line. Thelevel at which it begins cannot be ascertained as the lower portionof the endomandibular face is destroyed in that area. However, itseems to extend towards the P3. Its ascent is not steep and it is stillpresent at the level of the mesial alveolar margin of the M3 beyondwhich it can no longer be observed due to the breakage. The linerises from 27.6 mm below the mesial edge of the M1 alveolus to12.0 mm from the distal edge of the M2 alveolus.

Occlusal view (Fig. 5c)

The mandible is very thick in the buccolingual dimension. Themesial thickening is endomandibular while the distal thickening isexomandibular with respect to the dental arcade. The occlusal viewshows that the mandibular torus decreases in width from the M3 toP3, while the shelf-like thickening of the alveolar plane increases inwidth from the M1 towards the symphysis, and the ridge formeddescends towards themid-symphyseal region. This latter structure isresponsible for the endomandibular thickening of the bone towardsthe symphysis. The retromolar trigone could not be observed due tobreakage. The extramolar sulcus is very wide, accentuated by a lowand non-steep oblique line. The substantial width of the extramolarsulcus is further accentuated bya pronounced curvature of the dentalarcade towards the sagittal plane.

The mandible measures 34.2 mm in height at the mandibularforamen, recedes slightly towards the M3 where it measures31.2 mm, and is most consistent with a parallel character state foralveolar margin orientation. The width of the mandible varies from19.1 mm at the canine alveolus, becoming more restricted towardsthe mandibular foramen (17.8 mm) and M1 (17.5 mm) andincreasing towards the M2 (18.4 mm) and the M3 (23. 8 mm).

Dentition (Fig. 5d and Fig.7)

Only the three left molars are present in the BH-1 specimen. Theteeth are well preserved except for the mesiolingual root of the M3,which shows recent breakage. The occlusal outline is sub-rectangularand elongated mesiodistally. The teeth are not occlusally complex asthey show no extra ssures or crests. All three teeth have the vemain cusps (protoconid, metaconid, hypoconid, entoconid andhypoconulid). M1 amdM2 have a Y groove pattern,whileM3 showsa pattern. The hypoconulid is large and buccally aligned. There isan easily observed, wedge-shaped cusp 7 (tuberculum intermedium)(Scott and Turner, 1997), separated by clear ssures in all threemolars. A protostylid is not present on any of the teeth. The mesialmarginal ridge shows a proper ridge in M1 with no anterior fovea.This feature is continuous and depressed (very low) in M2 andaccompanied by an anterior fovea that is relatively poorly dened. Itis represented by a wide depression rather than a deep triangulardepression, as described by Scott and Turner (1997). The mesialmarginal ridge shows a tubercle on the M3 and a possible but notclear anterior fovea (Hillson,1996). Awell developed anterior fovea iscommon in Neandertals (87% according to Bailey, 2002) and variablein modern humans with a 83% frequency in a sample of modernCroatians (Gauta et al., 2010) and a frequency of 92% in a sample ofmodern Javanese (Artaria, n.d.). The M2 and M3 present a distaltrigonid crest that can be assessed by a short transverse ssure,slightly oblique to the buccolingual ssure. The M2 and M3 show thesame number of cusps as the M1, with less advanced degree of wearon M2 and no wear on M3. None of the teeth show the continuousmidtrigonid crest e considered to be indicator of Neandertal afnityas it occurs in 96% of Neandertals (Bailey, 2002). The presence of cusp7 is non-diagnostic. While not unknown in Neandertals (18.8%), it ismuch more common both in Homo erectus (40%) and is extremely

Figure 6. Cross-section of the mandible showing the alveolar planum. The gure isbased on two superimposed CT cross sections: one at the level of the canine and theother at the level of the mental foramen. The photos were inverted and rendered ingrey-scale in Photoshop CS2.



variable in modern human populations (3e61%) (Bailey, 2002), withhighest frequencies recorded in Africa (Scott and Turner, 1997). Theexpression of the distal trigonid crest is highly variable (Scott andTurner, 1997) and according to Martinn-Torres et al. (2008) oftenunderscored. It is, however, expressed in higher frequencies inDmanisi and Sangiran populations (Martinn-Torres et al., 2008).While the M1 and M2 have the same buccolingual width (10.9 mm)and mesiodistal length (11.5 mm), the M3 is longer mesiodistally(12.1 mm) and narrower buccolingually (10.5 mm).

Radiological features (Fig. 7)

The CT scan of the mandible reveals a very dense subcorticalbone of almost homogenous structure (1600-1800H, correspondingto massa compacta). The thickness varies in both buccolingual, andmesiodistal directions; the area adjacent to the lingual corticallamina is almost twice the width of the buccal one (Fig. 7b) and thethickness increases from themolars towards the symphyseal region(Fig. 7c). Trabeculation of the spongious bone is visible only in thecentral part of the mandibular body superior to the mandibularcanal; the trabeculae are coarse with prominent marrow spaces.There is no visible thickening of the lamina dura, nor the walls ofthe mandibular canal.

The CT scan of the P4 alveolus shows a clear separation towardsthe distal portion of the root socket, however, only the apex ofthe root is clearly bifurcated. This could indicate a possible (orpartial) root bifurcation, or alternatively, a groove on the distal sideof the root (Fig. 7d). Since the root itself is missing, it is not possibleto ascertain the presence or absence of two diverticles in the P4. TheM2 and M3 are mesotaurodontic (Mena, 1971). The M1 has twomesial and twodistal diverticles (Fig. 7c). All three aspects of the rootmorphology are primitive.While taurodontism has often been citedas a Neandertal trait, its varying frequencies in many differentmodern human populations (Terezhalmy et al., 2001), as well as itsappearance in the Atapuerca sample (Bermdez de Castro et al.,1997, 1999) and Homo erectus (Conroy, 1997) indicate that it

should be considered as a plesiomorphic trait in the Homo lineage(Ackerman et al., 1973). Notable is the substantial distance betweenroot apices and the mandibular canal, which could be explained bya reduction in tooth size coupledwith the large size of themandible.

Discussion

While the shape of the dental arcade and molar morphologyplace BH-1 in the genus Homo, its fragmentary nature and plesio-morphic character of its traits preclude a more precise taxonomicdesignation for this specimen (Carcraft, 1989). We assign it atpresent to Homo sp. The presence of the alveolar planum and theoverall robusticity of the specimen indicate a non-modernmorphology andwe can narrow the designation to an archaicHomosp. We compared available measurements and character states ofthe mandibular body with specimens from the Early, Middle andUpper Pleistocene (Table 3) published in two recent articles thatboth claim to be able to differentiate among species on the basis ofa set of metric (Lague et al., 2008) and morphological traits(Mounier et al., 2009) of the mandible. While the comparativesamples in these two articles are not ideally suited to examine theposition of BH-1 on the hominin spectrum, they provide a good rstview of the afnities of the specimen. Raw data on mandibularheight, width and robusticity (Table 5) were compared with datafrom Carbonell et al. (2005). A principal components analysis ofmetric data from Lague et al. (2008) (measurements were kindlyprovided by Nicole Collard) did not provide any further insight. Thescores for the BH-1 specimen show that the specimen lies at thevery margin of the spread for Neandertals and anatomicallymodern humans (AMH), in the area where they overlap, and veryclose to the H. erectus range. On the basis of this, the specimencannot be excluded from any of the three groups.

When compared with the table provided by Carbonell et al.(2005), the height of the mandible falls within the range of Nean-dertals and H. heidelbergensis. The corpus thickness, however,exceeds the limits of the Neandertal range and falls towards theupper limit of the H. heidelbergensis values. Corpus thickness, ratherthan corpus height seems to show a general trend of decrease withtime in thehuman lineage.Mesiodistal andbuccolingual diameters ofthe teeth fall within the range of variation for European Neandertal,Krapina, and Atapuerca samples (Wolpoff, 1979; Bermdez de Castroet al., 2001).

Cluster analysis (Fig. 8) shows clear Early, Middle and LatePleistocene clusters. The cophenetic correlation coefcientobtained equals 0.78, which is very close to taxonomic validity,usually considered as 0.8 (Rohlf and Fisher, 1968; Sneath and Sokal,1973). BH-1 clusters with the Early Pleistocene sample, includingspecimens from Sangiran (1b), Atapuerca (ATD6-96), Dmanisi(D211) and Koobi Fora (KNM-ER 992), as well as a Middle Pleisto-cene specimen from Tighenif (2) and slightly later in the sequence

Figure 7. CT scan of the mandible in: (a) mesiodistal (med) cross-section, (b) bucco-lingual (bel) slice at the root of M1 showing substantial subcortical thickening anda mesotaurodontic M1, (c) horizontal slice showing four diverticles of the M1 root, (d)Three superimposed CT sections showing the morphology of the P4 alveolar socketwith possible root bifurcation. Scale in centimetres.

Table 5Comparison of mandibular thickness, height and robustness of BH-1 with differentspecies of Homo as reported by Carbonell et al. (2005: Table 2).

Species Thickness, mm (n) Height, mm (n) Robustness (n)

Homo habilis 19.7 2.3 (5) 29.3 2.2 (4) 64.5 5.3 (4)H. ergaster 19.8 1.4 (8) 31.2 2.8 (8) 63.8 5.0 (8)H. erectus 19.8 2.6 (4) 36.3 1.1 (4) 54.7 7.4 (4)H. mauritanicus 18.0 1.1 (4) 35.8 1.5 (4) 50.2 1.8 (4)H. pekinensis 16.5 1.8 (7) 28.6 3.3 (7) 58.0 5.6 (7)H. antecessor 16.4 (2) 27.6 (2) 62.6 (2)H. heidelbergensis 16.4 1.7 (16) 30.8 3.4 (16) 53.4 5.1 (16)H. neanderthalensis 15.3 1.7 (21) 32.1 3.3 (21) 47.9 5.1 (21)BH-1 17.5 (1) 33.1 (1) 52.8 (1)



with SinanthropusH1 and Neandertal Baolas specimen. This resultis consistent with the absence of observable derived Neandertaltraits in BH-1 and the presence of the alveolar planum, four diver-ticles in M1 and a possible bifurcation of the P4, all three of whichare primitive traits inconsistent with Neandertals and AMH speci-mens. When considering raw data, BH-1 shares 13/16 traits withSangiran (1b) and Atapuerca (ATD6-96), 12/16 with Tighenif (2),and 10/16 with Dmanisi (211) and Koobi Fora KNM-ER 992. Whilethe Baolas mandible clusters relatively closely, it shares only fourcharacter states with the BH-1 mandible.

Comparative analysis of the specimen indicates a number ofprimitive traits: the alveolar planum, possible bifurcation of the P4,four diverticles inM1 and an anteriorly positioned single mandibularforamen thatmay signal the absence ofmidfacial prognathism. GiventheassociatedUpperPleistocenedate, it ispossible that this specimenis a primitive Neandertal. However, the complete lack of derivedNeandertal traits and clustering of BH-1 with the Early Pleistocenespecimens requires us to examine other plausible explanations.

While the paucity of remains from the area precludes any furtherdiscussion of the meaning of this partial specimen, the particularitiesof the Balkan Peninsula as a refugium for temperate deciduous forestsand associated biota (Eastwood, 2004; Tzedakis, 2004) and a hotspotof biodiversity (Lesbarreres, 2008) warrant further research. Of thethree southern European peninsulas that were the source of mostrepopulation of Europe for both animals and plants, the Balkan

Peninsula emerges as the source of all of the species of the East andmany of the West of northern Europe (Hewitt, 2000, 2004; Tzedakis,2004). It shows substantial faunal heterogeneity (Grifths et al.,2004) and high levels of endemism (Zima, 2004). While the role thatrefugial areas of the Iberian andApennine Peninsulas played inhumanevolutionduringglaciations in theNorthernhemispherehasbeenwellestablished in recent research (Finlayson, 2004; Finlayson et al., 2008),the importance of Southeastern Europe in providing glacial refugiumand maintaining gene ow between continents, while proposed fora number of animal species (Grifths et al., 2004), is rarely discussedwith regards to human evolution. High levels of biodiversity in theBalkans (Hewitt, 2004) and the refugial character of its ora(Eastwood, 2004; Tzedakis, 2004), coupled with a lack of isolatingmechanisms during Pleistocene glaciations, could have played animportant role in preserving variability, maintaining relic species, andallowing gene ow throughout the Pleistocene for all biota, includinghominins. This lack of isolatingmechanisms in the Balkans could haveresulted in the preservation of the primitivemorphology seen in BH-1,or the group of archaic humans it belonged to.

Conclusion

The recent discovery of a mandible BH-1, from Mala Balanica(Serbia), with primitive character states comparable with theEarly Pleistocene mandibular specimens, is associated with

Figure 8. Cluster analysis on mandibular body character states using Average Linkage, Euclidean Distance. UU: unknown age, EP: Early Pleistocene, MP Middle Pleistocene, NT:Neandertals. The coefcient of cophenetic correlation 0.78.



a minimum date of 113 72 43 ka. The BH-1 specimen, despitegeographic proximity and possible contemporaneity with theKrapina Neandertals, does not share any observable derivedNeandertal traits. BH-1 clearly represents an individual from anarchaic Homo sp., possibly non-Neandertal population, witha suite of features falling at the primitive end of the range ofvariation for the genus Homo.

Acknowledgements

The research was supported by a grant from the ofces of the VPAcademic and VP Research at the University of Winnipeg, an NSERCgrant (371077-2010) to MR, and a grant from the Ministry ofCulture and the Ministry of Science and Technological Develop-ment of the Republic of Serbia (177023) to DM. MR wishes to thankMary Silcox, Fred Smith and Katerina Harvati for comments on therst draft, Nicole Collard for mandibular measurements, WilliamSanders and Zoran Pavlovic for help with conservation, Rob Hoppaand his team for a 3-D printout of the specimen and anonymousreviewers for their valuable comments.

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