Neanderthal Teeth from Moula-Guercy Ardeche France

Leslea J Hlusko1 Joshua P Carlson1 Debbie Guatelli-Steinberg2 Kristin L Krueger3 Ben Mersey1

Peter S Ungar4 and Alban Defleur5

1Human Evolution Research Center University of California Berkeley 3101 Valley Life Sciences Building BerkeleyCA 947202Department of Anthropology 4034 Smith Laboratory The Ohio State University 174 West 18th Columbus OH43210-11063Department of Anthropology Loyola University Chicago Chicago IL 606604Department of Anthropology University of Arkansas Fayetteville AR 727015CNRS UMR 5276 Laboratoire de Geologie de Lyon Ecole Normale Superieure de Lyon 46 Allee drsquoItalie 69364Lyon Cedex 07 France

KEY WORDS evolution dental variation paleontology Hominidae

ABSTRACT Here we describe dental remains from aNeanderthal fossil assemblage from Moula-GuercyFrance Our report demonstrates that the Moula-Guercyhominid remains contribute important morphologicaldevelopmental and behavioral data to understandingNeanderthal evolutionary history We include gross com-parative morphological descriptions and enamel surfacemicrostructure and microwear data These teeth revealnumerous characteristics that are diagnostic of Neander-thals and provide no evidence for the presence of anyother hominid taxa Enamel growth increment datafrom the Moula-Guercy specimens yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation The presence of a

significant number of linear enamel hypoplasias indi-cates that these individuals were stressed during child-hood Molar microwear data suggest that theseNeanderthals did not differ significantly from modernhumans in terms of the fracture properties of the foodthey were consuming The incisor microwear and macrostriations provide evidence that these individuals mayhave been using their anterior teeth as tools similar tothe practices of several modern human populations suchas the Inuit Ipiutak and Australian Aboriginals andreminiscent of evidence from other Neanderthals fromKrapina Croatia as well as the 600000 year old homi-nids from Sima de los Huesos Spain Am J PhysAnthropol 151477ndash491 2013 VC 2013 Wiley Periodicals Inc

Ever since the first extensive study of Neanderthalskeletal variation (Gorjanovic-Kramberger 1906) thedentition has proven to be highly informative of Nean-derthal origins adaptation and evolution (eg Kallay1951 Carbonell 1965 Dean et al 1986 Brace et al1987 Stringer et al 1997 Irish 1998 Bailey2006aab) New discoveries continue to be made in thefield laboratory and also in museum collections (egWalker et al 2008 Crevecoeur et al 2010 Smith et al2010 Benazzi et al 2011 Walker et al 2011) makingNeanderthals one of the most important extinct homi-nids for studying species paleobiology Here we describefor the first time the Neanderthal fossil dental assem-blage from Moula-Guercy France Our analysis includesthree approaches to understanding these remains (1)comparative descriptions of the fossil material (2)enamel surface microstructure and (3) microwearOther anatomical components of the skeleton areforthcoming

STRATIGRAPHIC CHRONOLOGICALECOLOGICAL AND ARCHEOLOGICAL

CONTEXTS

Discovered in 1972 Moula-Guercy cave overlooks theRhone River 10 km south of the city of Valence inthe parish of Soyons Ardeche France Initial work at thesite between 1975 and 1982 uncovered 5 m of infill char-acterized by a Mousterian assemblage associated withfauna indicating a cold climate (Defleur et al 1993aa)Subsequent excavations spanning from 1991ndash1999

extended the sequence to a total of 7 m and revealed thefirst Neanderthal remains (Defleur et al 1998) Strati-graphic analysis led to the division of the sequence into20 layers grouped into three climatic phases correspond-ing to marine isotope stages 4ndash6 (Desclaux and Defleur1997 Defleur et al 1998 Defleur et al 2001) The upperunit Phase I comprises Layers VIndashXI A date of 72 6 12ka has been assigned to a volcanic ash (Layer VI) abovethe hominid level (Sanzelle et al 2000) Fauna from thisPhase includes Mammuthus primigenius and Rangifertardanus Together with associated micromammals thesetaxa indicate a cold climate consistent with MIS 4 Theunderlying unit Phase II consists of Layers XIIndashXVI andincludes the majority of the archeological material all of

Additional Supporting Information may be found in the online ver-sion of this article

Grant sponsor KLK and PU NSF BCS-0925818 DDIG DGSNSF BCS-0607520

Correspondence to Leslea J Hlusko Human EvolutionResearch Center University of California Berkeley 3101 Valley LifeSciences Building Berkeley CA 94720 USAE-mail hluskoberkeleyedu

Received 1 August 2012 accepted 16 April 2013

DOI 101002ajpa22291Published online 4 June 2013 in Wiley Online Library

(wileyonlinelibrarycom)

2013 WILEY PERIODICALS INC

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 151477ndash491 (2013)

the Neanderthal remains and fauna and charcoal con-sistent with a more temperate climate Biostratigraphy ofmicromammals indicates a date of 100ndash120 ka for PhaseII consistent with MIS 5 The base of the sequencePhase III includes Layers XVIIndashXX These containmicromammal remains indicating a cold steppe environ-ment consistent with MIS 6

When excavations were halted in 1999 108 hominidremains (45 craniodental and 63 postcranial specimens)had been recovered from Layer XV The best preservedof the elements are two partial crania a partial femurteeth and many complete hand and foot bones Asreported previously (Defleur et al 1993b Defleur et al1999) the remains conform to typical Neanderthal mor-phology and diagnostic characters include Neanderthalapomorphies These remains also show significant peri-mortem damage consistent with the nutritional exploita-tion of a minimum of six individuals four juvenileschildren two adults (Defleur et al 1999) Shortly afterthe publication of these remains (Defleur et al 1999)excavations were halted by local officials As only 30 ofthe primary layer (Layer XV) had been excavated priorto this full taphonomic assessment and determination ofthe minimum number of individuals is being withheldpending resumption and completion of the excavationwork However we do note that our reassessment doesnot counter the original interpretation of six individualstwo were 15ndash16 years of age at death two were 6ndash7years of age at death and there are two adult specimensrepresenting one large and one small individual (Defleuret al 1999)

THE STUDY OF NEANDERTHAL DENTALREMAINS

The gross morphological structure of teeth providesenormous information about an organismrsquos adaptive re-gime and evolutionary history Given their largely inor-ganic content teeth are often the only remaining bodypart we have for many extinct animals Neanderthalsare no exception as numerous studies of their phylogenyand paleobiology have relied on tooth crown shape (egBoule 1921 Bailey 2006ab) Trinkausrsquo summary ofprimitive versus derived traits in Neanderthals com-pared to Early and Late Modern humans found thatNeanderthals have at least three autapomorphic dentaltraits and lack the seven or eight derived dental traitsseen in early and late modern humans respectively(2006) These traits and others provide the basis for themorphological descriptions presented here as we investi-gate whether or not the hominid dental remains fromMoula-Guercy align more closely with the Neanderthalsas determined previously (Defleur et al 1999) or havea closer affinity with Early Modern Humans

Enamel surface microstructures also provide insightinto an organismrsquos growth rates and patterns and dis-ruptions to growth (eg Hillson and Bond 1997) Weinvestigated two components of enamel microstructureof the Moula-Guercy remains perikymata and linearenamel hypoplasia

Perikymata are enamel surface manifestations of in-ternal growth increments known as striae of Retzius(Hillson 1996) representing 7 or 8 daysrsquo worth of enamelgrowth in Neanderthals (Macchiarelli et al 2006 Smithet al 2009 Smith et al 2010) Perikymata cover thesurface of lateral enamel forming shallow grooves or

waves approximately 100 lm apart (Hillson and Bond1997) In the cuspal region of the tooth striae of Retziusdo not emerge onto the enamel surface such that thisportion of enamel growth is hidden from a surface viewHowever the time lateral enamel takes to form repre-sents approximately 85 or more of the overall enamelformation time of anterior teeth at least in modernhumans (Reid and Dean 2006) Thus the number ofperikymata on anterior teeth reflects a large percentageof the time it took for the crown to form Perikymatacounts on Neanderthal teeth tend to fall within therange of modern human variation but are at the lowend of that range for particular teeth (the upper incisorsand lower canines Guatelli-Steinberg and Reid 2008anterior teeth Ramirez-Rozzi and Bermudez de Castro2004) In addition in Neanderthals perikymata are moreevenly distributed across the enamel surface than theyare in modern humans (Guatelli-Steinberg et al 2007Guatelli-Steinberg and Reid 2008)

Linear enamel hypoplasia (LEH) appears as a linegroove or furrow in the enamel surface reflecting peri-ods of disrupted growth caused by systemic physiologicalstress such as malnutrition and disease (Goodman andRose 1990 Ten Cate 1994) Systemic physiologicalstress is likely to affect all of the teeth of an individualdeveloping at the time of the stress episode (Hillson andBond 1997) Growth increments on the surface of theroot known as periradicular bands also may becomeaccentuated presumably as a result of growth disrup-tion (Smith et al 2007)

While the enamel microstructure of a tooth is informa-tive of the development and health of an individual wecan add to our reconstruction of an organismrsquos life his-tory by investigating the damage to the crown surfaceduring life We have also undertaken an investigation ofdental wearmdashthe study of microscopic scratches and pitsthat form on a toothrsquos surface as the result of its useSuch analyses of nonhuman primates and recent humanforagers indicate that microwear patterns on incisorsvary with front tooth behaviors and those on molarsvary with the fracture properties of foods eaten (seeUngar et al 2007 for review) Dental microwear pat-terns have also been shown to distinguish fossil homi-nids suggesting their value for inferring diet and toothuse in these taxa (eg Grine 1987 Ungar 2011) Herewe include a description of the dental microwear of theNeanderthal specimens from Moula-Guercy

A summary and brief contextualization of the resultsis provided in the discussion section

MATERIALS

Original hominid fossil material from Moula-GuercyCave France was used for the morphological descrip-tions Replicas (described in detail below) were used forthe enamel microstructure and dental microwear analy-ses The original specimens are shown in Figure 1 andbasic linear measurements are presented in Table 1Comparative metrics for mandibular canines and firstmolars are presented in Figure 2

Isolated teeth are described individually and haveunique specimen numbers Teeth still rooted in jaws weregiven the same specimen number and are described inthe same paragraph Appendix 1 (Supporting Informa-tion) lists all cast material used for comparison all

478 LJ HLUSKO ET AL

American Journal of Physical Anthropology

available at the Human Evolution Research Center at theUniversity of California Berkeley

ABBREVIATIONS

Specimen numbers were assigned as follows ldquoMrdquo des-ignates Moula-Guercy cave followed by a two-characteralphanumeric code corresponding to the excavation grid

square from which the specimen came then a sequentialspecimen number or arbitrary identifier For specimensthat could not be located to a specific square a longercode was given to indicate the range of possible sourcegrid squares An ldquoSrdquo in this position indicates a speci-men recovered from a pit dug outside the standard grid(S 5 ldquosondagerdquo or test pit in French) The sequentialspecimen number stems from the count of all specimens(hominid and non-hominid) within the indicated gridsquare Where a sequential number could not beassigned an arbitrary code was given For example M-G2-419 a mandible fragment is the 419th specimenrecovered from grid square G2 whereas M-L4-TNN5was recovered from square L4 but not assigned a speci-men number until this study began (and so received anarbitrary ldquonew numberrdquo designation) An exception tothis is M--TNN2 which was recovered from the backfillfrom layer XV and cannot be allocated to a grid square

Tooth identification abbreviations follow the conven-tion in which numerical subscripts indicate mandibularand superscripts indicate maxillary (thus a maxillaryright second molar is abbreviated RM2 and a left man-dibular third premolar is LP3) Deciduous teeth aredenoted with a lowercase ldquodrdquo after the designation ofright or left and the tooth type in lowercase eg man-dibular right deciduous second molar is Rdm2

METHODS

Morphological descriptions

Descriptions of hominid material are most useful andrelevant when comparative (White et al 2000) Thedescriptions included here were done through comparisonwith a large cast collection in the Human EvolutionResearch Center at the University of California Berkeleyand against published descriptions (in addition to the pub-lications cited within the descriptions that follow thesemonographs and chapters were studied Martin 19231926 Patte 1957 Sakura 1970 Tillier and Genet-Varcin1980 Heim 1982 Radovcic et al 1988 Madre-Dupouy1992 Condemi 2001 Maureille et al 2001 Bilsboroughand Thompson 2005 Garralda et al 2008) See the Sup-porting Information for list of comparative specimens (allcasts) that were used (this table does not include materialfor which only published data were employed only the listof casts studied) Best-matches were identified and areincluded in the descriptions along with the ways in whichthe Moula specimen differs from the best-match

As part of the morphological descriptions weemployed five descriptive standards that facilitate com-parisons between specimens For describing non-linearshape variation we refer to Crummettrsquos (1994 93)stages for incisor shoveling the Arizona State UniversityDental Anthropology System (ASUDAS Turner et al1991) for describing traits such as the distal accessoryridge and Baileyrsquos (2002) scoring system for postcaninetraits not encompassed by the ASUDAS range of varia-tion which is based only on modern humans Liversidgeand Molleson (2004) provide useful crown and root for-mation stages for deciduous teeth and Demirjian et al(1973) outlined the same for the permanent dentitionWe employ these when relevant

Enamel surface microstructure

To count perikymata in the Moula-Guercy sample rep-licas of 11 of the crowns with the best preservation were

Fig 1 Moula-Guercy Neanderthal mandibular (left panel)and maxillary (right panel) dental material From left to rightocclusal [mesial is up except (A) and (I)] buccallabial and lin-gual views with the exception of (J) where the distal view ispictured Mandible (A) M-G2-419 (B) M-D1-230 (C) M-L4-TNN5 (D) M-G3-251 (E) M-J5-TNN4 (F) M--TNN2 (G) M-G4-144 (H) M-S-TNN1 Maxilla (I) M-I4-55 (J) M-G2-117 (K)M-F3-215 (L) M-H3-73 (M) M-I4-TNN3 (N) M-D2-588 (O) M-D1-259 (P) M-S-27

MOULA-GUERCY DENTITION 479

American Journal of Physical Anthropology

placed on the stage of a measuring microscope (SpectraServices) Under a magnification of 50x along the midlineof the toothrsquos labial surface the positions of perikymatawere recorded using the Vision Gauge software associatedwith the microscope In some instances perikymatacounts were double-checked using counts made from SEMimages In this dental sample the anterior teeth wereminimally worn with the exception of M-D2-588 a LI1

with an oblique incisal edge created by wear Because theteeth were minimally worn perikymata were countedwithin deciles of measured crown height numbered from1 to 10 from the cusp tip to the cement-enamel junction(CEJ) This protocol differs slightly from that establishedby Dean and Reid (2001) which also included decilelengths based on crown height reconstructions from wornteeth For the worn upper LI1 the crown height wasassumed to be the height of the crown along the mesial

edge the least worn When perikymata could not beclearly seen due for example to abrasion they were notcounted All perikymata counts were done by one personwho reported an average percentage difference betweenfirst and second counts as 555 on a set of various non-human primate teeth on which perikymata were countedusing the same microscope used here (Guatelli-Steinberget al 2009) Linear enamel hypoplasias (LEHs) wereidentified using oblique lighting with the aid of a 10xhand lens The locations of LEH defects were marked onthe tooth replica surface Using the measuring micro-scope distances of LEH defects were measured from theCEJ to the midpoint of each defect Widths of defects werealso measured from the cervical to occlusal border of anLEH groove Where possible perikymata were alsocounted within a defect to gain insight into the durationof growth disruption

Fig 2 Mesiodistal and buccolingual lengths for mandibular canines and first molars of Neanderthals (N) Middle PaleolithicHomo sapiens (MHPS) European Upper Paleolithic Homo sapiens (UPHS) Modern Homo sapiens (MHS) and Moula-Guercy (MG)Figure is modified from Benazzi et alrsquos (2011) Figure 4 using data presented and cited therein Note that Moula-Guercy specimensare in the center of the cluster in each panel

TABLE 1 Measurements for all Moula-Guercy Neanderthal Teetha

Specimen number Tooth identification Buccolingual Mesiodistal Cervicoincisal

M-G2-419 RM1 1045 (103)M-G2-419 RM2 111 (116)M-G2-419 RM3 105 (113)M-D1-230 RM1 106 (116)M-L4-TNN5 LM1 109 (119)M-G3-251 Rdm2 90 (98)M-J5-TNN4 Ldm2 00 (104)M--TNN2 LC1 82 76 109M-G4-144 LC1 81 79 116M-S-TNN1 RC1 89 71 114M-I4-55 Rdm2 101 92M-I4-55 RM1 111 114M-F3-215 RM2 116 106M-G2-117 RM2 120 104M-H3-73 Rdm1 00 74M-I4-TNN3 RC1 95 86 (116)M-D2-588 LI1 84 00 00M-D1-259 RI2 85 80 108M-S-27 LP3 107 75

a measurements presented in mm estimates in parentheses00 indicates that the tooth is broken or too worn to accurately assess this measurementTooth identifications follow the same convention as the text Measurement protocols followed Suwa et al (2009 see their SOM)

480 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Dental microwear analysis

Specimens were prepared and analyzed using stand-ard dental microwear texture analysis protocols Moldswere made using Presidentrsquos Jet polyvinylsiloxane den-tal impression material (Coltene-Whaledent) and high-resolution casts were prepared using Epotek 301 epoxyand hardener (Epoxy Technologies) Data were collectedfor all available specimens that had sufficient areas ofunobscured antemortem microwear (Table 2) Microwearsurface preservation for the Moula-Guercy individualswas typically good when compared with many other fos-sil hominids most teeth excluded from this study wereeither unworn or were overwhelmed by postmortemcracks

Nine individuals preserved unobscured antemortemmicrowear (Table 2) Data are reported for a dm2 and aM1 (M-I4-55) three M1s (M-D1-230 M-G2-419 and M-L4-TNN5) two C1s (M-G4-144 and M-S-TNN1) a P3 (M-S-27) an I2 (M-D1-259) and an I1 (M-D2-588) We reportdata here for both specimens of M-I4-55 because both ofthese teeth preserved antemortem microwear

Specimens were analyzed using a Sensofar Pll white-light confocal profiler with an integrated vertical scan-ning interferometer and a 100x long-working-distanceobjective (Solarius) Elevation data were collected fromfour adjacent fields of view each measuring 138 lm 3102 lm for a total work area of 276 lm 3 204 lm foreach tooth Point clouds were generated using a lateralsampling interval of 018 lm and a vertical resolution of005 lm The cheek teeth were sampled for microwearon ldquoPhase IIrdquo facets 9 or 10n and the incisors and can-ines were sampled on the labial surface just above theincisal edge These locations were chosen following con-vention (see Krueger et al 2008 Krueger and Ungar2010) Points representing artifacts such as dust weredeleted prior to analysis

Point clouds were analyzed using Toothfrax and SFraxscale-sensitive fractal analysis software packages (Surf-ract Corp) and data were generated for the five textureattributes that have proven to be particularly useful forcharacterizing microwear surfaces area-scale fractalcomplexity (Asfc) scale of maximum complexity (Smc)heterogeneity of complexity (HAsfc) textural fill volume(Tfv) and length-scale anisotropy of relief (epLsar)HAsfc was calculated by dividing each field of view usingboth 3 3 3 and 9 3 9 grids (HAsfc9 and HAsfc81 respec-tively) Median values for the four fields of view sampledin each tooth are presented here

Detailed descriptions of each of these variables can befound in Scott et al (2006) and Ungar et al (2007)

Complexity is a measure of how surface roughness theratio of surface area to planimetric area changes withscale of observation Complex surfaces are those thatshow increasing roughness at progressively finer scalesof observation a heavily pitted surface with overlappingfeatures of many sizes has a high Asfc value The scaleof maximum complexity reflects the point at which asurface no longer gets rougher with progressively finerscales of observation a surface dominated by large fea-tures but lacking smaller ones would have a high Smcvalue Heterogeneity is measured by dividing each fieldinto a number of equal size subfields and calculatingvariation in Asfc among them heterogeneous surfaceshave higher HAsfc values than do homogeneous onesTextural fill volume is a measure of the summed volumeof small squared cuboids (in this case 2 lm on a side)that would fill a surface divided by that of large squaredcuboids (10lm on a side) an area with many deep mod-erate-size microwear features (between 2 lm and 10 lmin diameter) would have a high Tfv value Finally ani-sotropy is a measure of directionality of surface rough-ness Average relative lengths of transects (ratios ofsummed 18 lm segments to straight-line distancesbetween endpoints) are sampled at different orientations(5 intervals) across each surface Greater variation inthose lengths indicates greater anisotropy a surfacedominated by parallel striations has a higher epLsarvalue than one with randomly oriented scratches or pits

RESULTS

Morphological descriptions

Mandibular M-G2-419 is a right mandibular frag-ment with M1-2 erupted and M3 in the crypt (Fig 1A)The mandibular body is described in detail elsewhere(Defleur et al in preparation) The first molar has anX5 cusp pattern that is only slightly worn with no den-tine exposed The M2 and M3 are unworn although M2

is fully erupted The M2 is relatively unusual for a Ne-anderthal in having only four cusps in the cruciformcusp configuration (Scott and Turner 1997 p 50 Bailey2002) The M3 has a Y5 cusp pattern and root formationto 69 mm (incomplete) An anterior fovea and mid-trigo-nid crest is present on all three molars (score of 2 for allthree molars) a common Neanderthal trait infrequentlyseen on modern human M1s and rare on modern humanM2s and M3s (Bailey 2002) The M1 and M2 are mostsimilar in size and shape to those preserved on theRegourdou mandible though less worn The Moula-Guercy M3 is more rounded and slightly smaller moresimilar in overall size and shape to Hortus VI and Vin-dija 206 and a little smaller than the RM3 of Krapinamandible G

M-D1-230 is a right M1 with a Y5 cusp pattern slightwear on the lingual cusps but no dentine exposed (Fig1B) It has a clear anterior fovea and mid-trigonid crestwith a score of 1 (Bailey 2002) The root is incompletelydeveloped to 2 mm below cervix and fractured on the lin-gual side (Stage E Demirjian et al 1973) Its morphol-ogy is very similar to Vindija 206 (RM1) but less worn

M-L4-TNN5 (Fig 1C) is a left M1 with X5 cusp pat-tern anterior fovea and slight mid-trigonid crest (scoreof 1 Bailey 2002) and Stage G root development (Demi-rjian et al 1973) The buccal cusps are slightly wornbut no dentine is exposed There is a mesial contactfacet but no distal interstitial facet This crown is lessworn than the M-G2-419 M1 and larger with a much

TABLE 2 Dental microwear texture data for Neanderthalspecimens from Moula-Guercy

Specimen Tooth Asfc eplsar Smc Tfv HAsfc9 HAsfc81

M-I4-55 Rdm2 295 00030 015 1023919 045 089M-I4-55 RM1 431 00012 015 1420211 054 088M-D1-230 RM1 101 00025 027 463241 037 056M-G2-419 RM1 135 00016 027 1087593 051 064M-L4-TNN5 LM1 251 00042 027 1081540 066 116M-S-27 LP3 387 00022 021 1181266 048 063M-G4-144 LC1 139 00025 027 1910202 043 067M-S-TNN1 RC1 088 00043 042 1080662 046 055M-D1-259 RI2 190 00022 021 1160083 056 117M-D2-588 LI1 433 00013 015 1506999 070 156

MOULA-GUERCY DENTITION 481

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

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Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

the Neanderthal remains and fauna and charcoal con-sistent with a more temperate climate Biostratigraphy ofmicromammals indicates a date of 100ndash120 ka for PhaseII consistent with MIS 5 The base of the sequencePhase III includes Layers XVIIndashXX These containmicromammal remains indicating a cold steppe environ-ment consistent with MIS 6

When excavations were halted in 1999 108 hominidremains (45 craniodental and 63 postcranial specimens)had been recovered from Layer XV The best preservedof the elements are two partial crania a partial femurteeth and many complete hand and foot bones Asreported previously (Defleur et al 1993b Defleur et al1999) the remains conform to typical Neanderthal mor-phology and diagnostic characters include Neanderthalapomorphies These remains also show significant peri-mortem damage consistent with the nutritional exploita-tion of a minimum of six individuals four juvenileschildren two adults (Defleur et al 1999) Shortly afterthe publication of these remains (Defleur et al 1999)excavations were halted by local officials As only 30 ofthe primary layer (Layer XV) had been excavated priorto this full taphonomic assessment and determination ofthe minimum number of individuals is being withheldpending resumption and completion of the excavationwork However we do note that our reassessment doesnot counter the original interpretation of six individualstwo were 15ndash16 years of age at death two were 6ndash7years of age at death and there are two adult specimensrepresenting one large and one small individual (Defleuret al 1999)

THE STUDY OF NEANDERTHAL DENTALREMAINS

The gross morphological structure of teeth providesenormous information about an organismrsquos adaptive re-gime and evolutionary history Given their largely inor-ganic content teeth are often the only remaining bodypart we have for many extinct animals Neanderthalsare no exception as numerous studies of their phylogenyand paleobiology have relied on tooth crown shape (egBoule 1921 Bailey 2006ab) Trinkausrsquo summary ofprimitive versus derived traits in Neanderthals com-pared to Early and Late Modern humans found thatNeanderthals have at least three autapomorphic dentaltraits and lack the seven or eight derived dental traitsseen in early and late modern humans respectively(2006) These traits and others provide the basis for themorphological descriptions presented here as we investi-gate whether or not the hominid dental remains fromMoula-Guercy align more closely with the Neanderthalsas determined previously (Defleur et al 1999) or havea closer affinity with Early Modern Humans

Enamel surface microstructures also provide insightinto an organismrsquos growth rates and patterns and dis-ruptions to growth (eg Hillson and Bond 1997) Weinvestigated two components of enamel microstructureof the Moula-Guercy remains perikymata and linearenamel hypoplasia

Perikymata are enamel surface manifestations of in-ternal growth increments known as striae of Retzius(Hillson 1996) representing 7 or 8 daysrsquo worth of enamelgrowth in Neanderthals (Macchiarelli et al 2006 Smithet al 2009 Smith et al 2010) Perikymata cover thesurface of lateral enamel forming shallow grooves or

waves approximately 100 lm apart (Hillson and Bond1997) In the cuspal region of the tooth striae of Retziusdo not emerge onto the enamel surface such that thisportion of enamel growth is hidden from a surface viewHowever the time lateral enamel takes to form repre-sents approximately 85 or more of the overall enamelformation time of anterior teeth at least in modernhumans (Reid and Dean 2006) Thus the number ofperikymata on anterior teeth reflects a large percentageof the time it took for the crown to form Perikymatacounts on Neanderthal teeth tend to fall within therange of modern human variation but are at the lowend of that range for particular teeth (the upper incisorsand lower canines Guatelli-Steinberg and Reid 2008anterior teeth Ramirez-Rozzi and Bermudez de Castro2004) In addition in Neanderthals perikymata are moreevenly distributed across the enamel surface than theyare in modern humans (Guatelli-Steinberg et al 2007Guatelli-Steinberg and Reid 2008)

Linear enamel hypoplasia (LEH) appears as a linegroove or furrow in the enamel surface reflecting peri-ods of disrupted growth caused by systemic physiologicalstress such as malnutrition and disease (Goodman andRose 1990 Ten Cate 1994) Systemic physiologicalstress is likely to affect all of the teeth of an individualdeveloping at the time of the stress episode (Hillson andBond 1997) Growth increments on the surface of theroot known as periradicular bands also may becomeaccentuated presumably as a result of growth disrup-tion (Smith et al 2007)

While the enamel microstructure of a tooth is informa-tive of the development and health of an individual wecan add to our reconstruction of an organismrsquos life his-tory by investigating the damage to the crown surfaceduring life We have also undertaken an investigation ofdental wearmdashthe study of microscopic scratches and pitsthat form on a toothrsquos surface as the result of its useSuch analyses of nonhuman primates and recent humanforagers indicate that microwear patterns on incisorsvary with front tooth behaviors and those on molarsvary with the fracture properties of foods eaten (seeUngar et al 2007 for review) Dental microwear pat-terns have also been shown to distinguish fossil homi-nids suggesting their value for inferring diet and toothuse in these taxa (eg Grine 1987 Ungar 2011) Herewe include a description of the dental microwear of theNeanderthal specimens from Moula-Guercy

A summary and brief contextualization of the resultsis provided in the discussion section

MATERIALS

Original hominid fossil material from Moula-GuercyCave France was used for the morphological descrip-tions Replicas (described in detail below) were used forthe enamel microstructure and dental microwear analy-ses The original specimens are shown in Figure 1 andbasic linear measurements are presented in Table 1Comparative metrics for mandibular canines and firstmolars are presented in Figure 2

Isolated teeth are described individually and haveunique specimen numbers Teeth still rooted in jaws weregiven the same specimen number and are described inthe same paragraph Appendix 1 (Supporting Informa-tion) lists all cast material used for comparison all

478 LJ HLUSKO ET AL

American Journal of Physical Anthropology

available at the Human Evolution Research Center at theUniversity of California Berkeley

ABBREVIATIONS

Specimen numbers were assigned as follows ldquoMrdquo des-ignates Moula-Guercy cave followed by a two-characteralphanumeric code corresponding to the excavation grid

square from which the specimen came then a sequentialspecimen number or arbitrary identifier For specimensthat could not be located to a specific square a longercode was given to indicate the range of possible sourcegrid squares An ldquoSrdquo in this position indicates a speci-men recovered from a pit dug outside the standard grid(S 5 ldquosondagerdquo or test pit in French) The sequentialspecimen number stems from the count of all specimens(hominid and non-hominid) within the indicated gridsquare Where a sequential number could not beassigned an arbitrary code was given For example M-G2-419 a mandible fragment is the 419th specimenrecovered from grid square G2 whereas M-L4-TNN5was recovered from square L4 but not assigned a speci-men number until this study began (and so received anarbitrary ldquonew numberrdquo designation) An exception tothis is M--TNN2 which was recovered from the backfillfrom layer XV and cannot be allocated to a grid square

Tooth identification abbreviations follow the conven-tion in which numerical subscripts indicate mandibularand superscripts indicate maxillary (thus a maxillaryright second molar is abbreviated RM2 and a left man-dibular third premolar is LP3) Deciduous teeth aredenoted with a lowercase ldquodrdquo after the designation ofright or left and the tooth type in lowercase eg man-dibular right deciduous second molar is Rdm2

METHODS

Morphological descriptions

Descriptions of hominid material are most useful andrelevant when comparative (White et al 2000) Thedescriptions included here were done through comparisonwith a large cast collection in the Human EvolutionResearch Center at the University of California Berkeleyand against published descriptions (in addition to the pub-lications cited within the descriptions that follow thesemonographs and chapters were studied Martin 19231926 Patte 1957 Sakura 1970 Tillier and Genet-Varcin1980 Heim 1982 Radovcic et al 1988 Madre-Dupouy1992 Condemi 2001 Maureille et al 2001 Bilsboroughand Thompson 2005 Garralda et al 2008) See the Sup-porting Information for list of comparative specimens (allcasts) that were used (this table does not include materialfor which only published data were employed only the listof casts studied) Best-matches were identified and areincluded in the descriptions along with the ways in whichthe Moula specimen differs from the best-match

As part of the morphological descriptions weemployed five descriptive standards that facilitate com-parisons between specimens For describing non-linearshape variation we refer to Crummettrsquos (1994 93)stages for incisor shoveling the Arizona State UniversityDental Anthropology System (ASUDAS Turner et al1991) for describing traits such as the distal accessoryridge and Baileyrsquos (2002) scoring system for postcaninetraits not encompassed by the ASUDAS range of varia-tion which is based only on modern humans Liversidgeand Molleson (2004) provide useful crown and root for-mation stages for deciduous teeth and Demirjian et al(1973) outlined the same for the permanent dentitionWe employ these when relevant

Enamel surface microstructure

To count perikymata in the Moula-Guercy sample rep-licas of 11 of the crowns with the best preservation were

Fig 1 Moula-Guercy Neanderthal mandibular (left panel)and maxillary (right panel) dental material From left to rightocclusal [mesial is up except (A) and (I)] buccallabial and lin-gual views with the exception of (J) where the distal view ispictured Mandible (A) M-G2-419 (B) M-D1-230 (C) M-L4-TNN5 (D) M-G3-251 (E) M-J5-TNN4 (F) M--TNN2 (G) M-G4-144 (H) M-S-TNN1 Maxilla (I) M-I4-55 (J) M-G2-117 (K)M-F3-215 (L) M-H3-73 (M) M-I4-TNN3 (N) M-D2-588 (O) M-D1-259 (P) M-S-27

MOULA-GUERCY DENTITION 479

American Journal of Physical Anthropology

placed on the stage of a measuring microscope (SpectraServices) Under a magnification of 50x along the midlineof the toothrsquos labial surface the positions of perikymatawere recorded using the Vision Gauge software associatedwith the microscope In some instances perikymatacounts were double-checked using counts made from SEMimages In this dental sample the anterior teeth wereminimally worn with the exception of M-D2-588 a LI1

with an oblique incisal edge created by wear Because theteeth were minimally worn perikymata were countedwithin deciles of measured crown height numbered from1 to 10 from the cusp tip to the cement-enamel junction(CEJ) This protocol differs slightly from that establishedby Dean and Reid (2001) which also included decilelengths based on crown height reconstructions from wornteeth For the worn upper LI1 the crown height wasassumed to be the height of the crown along the mesial

edge the least worn When perikymata could not beclearly seen due for example to abrasion they were notcounted All perikymata counts were done by one personwho reported an average percentage difference betweenfirst and second counts as 555 on a set of various non-human primate teeth on which perikymata were countedusing the same microscope used here (Guatelli-Steinberget al 2009) Linear enamel hypoplasias (LEHs) wereidentified using oblique lighting with the aid of a 10xhand lens The locations of LEH defects were marked onthe tooth replica surface Using the measuring micro-scope distances of LEH defects were measured from theCEJ to the midpoint of each defect Widths of defects werealso measured from the cervical to occlusal border of anLEH groove Where possible perikymata were alsocounted within a defect to gain insight into the durationof growth disruption

Fig 2 Mesiodistal and buccolingual lengths for mandibular canines and first molars of Neanderthals (N) Middle PaleolithicHomo sapiens (MHPS) European Upper Paleolithic Homo sapiens (UPHS) Modern Homo sapiens (MHS) and Moula-Guercy (MG)Figure is modified from Benazzi et alrsquos (2011) Figure 4 using data presented and cited therein Note that Moula-Guercy specimensare in the center of the cluster in each panel

TABLE 1 Measurements for all Moula-Guercy Neanderthal Teetha

Specimen number Tooth identification Buccolingual Mesiodistal Cervicoincisal

M-G2-419 RM1 1045 (103)M-G2-419 RM2 111 (116)M-G2-419 RM3 105 (113)M-D1-230 RM1 106 (116)M-L4-TNN5 LM1 109 (119)M-G3-251 Rdm2 90 (98)M-J5-TNN4 Ldm2 00 (104)M--TNN2 LC1 82 76 109M-G4-144 LC1 81 79 116M-S-TNN1 RC1 89 71 114M-I4-55 Rdm2 101 92M-I4-55 RM1 111 114M-F3-215 RM2 116 106M-G2-117 RM2 120 104M-H3-73 Rdm1 00 74M-I4-TNN3 RC1 95 86 (116)M-D2-588 LI1 84 00 00M-D1-259 RI2 85 80 108M-S-27 LP3 107 75

a measurements presented in mm estimates in parentheses00 indicates that the tooth is broken or too worn to accurately assess this measurementTooth identifications follow the same convention as the text Measurement protocols followed Suwa et al (2009 see their SOM)

480 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Dental microwear analysis

Specimens were prepared and analyzed using stand-ard dental microwear texture analysis protocols Moldswere made using Presidentrsquos Jet polyvinylsiloxane den-tal impression material (Coltene-Whaledent) and high-resolution casts were prepared using Epotek 301 epoxyand hardener (Epoxy Technologies) Data were collectedfor all available specimens that had sufficient areas ofunobscured antemortem microwear (Table 2) Microwearsurface preservation for the Moula-Guercy individualswas typically good when compared with many other fos-sil hominids most teeth excluded from this study wereeither unworn or were overwhelmed by postmortemcracks

Nine individuals preserved unobscured antemortemmicrowear (Table 2) Data are reported for a dm2 and aM1 (M-I4-55) three M1s (M-D1-230 M-G2-419 and M-L4-TNN5) two C1s (M-G4-144 and M-S-TNN1) a P3 (M-S-27) an I2 (M-D1-259) and an I1 (M-D2-588) We reportdata here for both specimens of M-I4-55 because both ofthese teeth preserved antemortem microwear

Specimens were analyzed using a Sensofar Pll white-light confocal profiler with an integrated vertical scan-ning interferometer and a 100x long-working-distanceobjective (Solarius) Elevation data were collected fromfour adjacent fields of view each measuring 138 lm 3102 lm for a total work area of 276 lm 3 204 lm foreach tooth Point clouds were generated using a lateralsampling interval of 018 lm and a vertical resolution of005 lm The cheek teeth were sampled for microwearon ldquoPhase IIrdquo facets 9 or 10n and the incisors and can-ines were sampled on the labial surface just above theincisal edge These locations were chosen following con-vention (see Krueger et al 2008 Krueger and Ungar2010) Points representing artifacts such as dust weredeleted prior to analysis

Point clouds were analyzed using Toothfrax and SFraxscale-sensitive fractal analysis software packages (Surf-ract Corp) and data were generated for the five textureattributes that have proven to be particularly useful forcharacterizing microwear surfaces area-scale fractalcomplexity (Asfc) scale of maximum complexity (Smc)heterogeneity of complexity (HAsfc) textural fill volume(Tfv) and length-scale anisotropy of relief (epLsar)HAsfc was calculated by dividing each field of view usingboth 3 3 3 and 9 3 9 grids (HAsfc9 and HAsfc81 respec-tively) Median values for the four fields of view sampledin each tooth are presented here

Detailed descriptions of each of these variables can befound in Scott et al (2006) and Ungar et al (2007)

Complexity is a measure of how surface roughness theratio of surface area to planimetric area changes withscale of observation Complex surfaces are those thatshow increasing roughness at progressively finer scalesof observation a heavily pitted surface with overlappingfeatures of many sizes has a high Asfc value The scaleof maximum complexity reflects the point at which asurface no longer gets rougher with progressively finerscales of observation a surface dominated by large fea-tures but lacking smaller ones would have a high Smcvalue Heterogeneity is measured by dividing each fieldinto a number of equal size subfields and calculatingvariation in Asfc among them heterogeneous surfaceshave higher HAsfc values than do homogeneous onesTextural fill volume is a measure of the summed volumeof small squared cuboids (in this case 2 lm on a side)that would fill a surface divided by that of large squaredcuboids (10lm on a side) an area with many deep mod-erate-size microwear features (between 2 lm and 10 lmin diameter) would have a high Tfv value Finally ani-sotropy is a measure of directionality of surface rough-ness Average relative lengths of transects (ratios ofsummed 18 lm segments to straight-line distancesbetween endpoints) are sampled at different orientations(5 intervals) across each surface Greater variation inthose lengths indicates greater anisotropy a surfacedominated by parallel striations has a higher epLsarvalue than one with randomly oriented scratches or pits

RESULTS

Morphological descriptions

Mandibular M-G2-419 is a right mandibular frag-ment with M1-2 erupted and M3 in the crypt (Fig 1A)The mandibular body is described in detail elsewhere(Defleur et al in preparation) The first molar has anX5 cusp pattern that is only slightly worn with no den-tine exposed The M2 and M3 are unworn although M2

is fully erupted The M2 is relatively unusual for a Ne-anderthal in having only four cusps in the cruciformcusp configuration (Scott and Turner 1997 p 50 Bailey2002) The M3 has a Y5 cusp pattern and root formationto 69 mm (incomplete) An anterior fovea and mid-trigo-nid crest is present on all three molars (score of 2 for allthree molars) a common Neanderthal trait infrequentlyseen on modern human M1s and rare on modern humanM2s and M3s (Bailey 2002) The M1 and M2 are mostsimilar in size and shape to those preserved on theRegourdou mandible though less worn The Moula-Guercy M3 is more rounded and slightly smaller moresimilar in overall size and shape to Hortus VI and Vin-dija 206 and a little smaller than the RM3 of Krapinamandible G

M-D1-230 is a right M1 with a Y5 cusp pattern slightwear on the lingual cusps but no dentine exposed (Fig1B) It has a clear anterior fovea and mid-trigonid crestwith a score of 1 (Bailey 2002) The root is incompletelydeveloped to 2 mm below cervix and fractured on the lin-gual side (Stage E Demirjian et al 1973) Its morphol-ogy is very similar to Vindija 206 (RM1) but less worn

M-L4-TNN5 (Fig 1C) is a left M1 with X5 cusp pat-tern anterior fovea and slight mid-trigonid crest (scoreof 1 Bailey 2002) and Stage G root development (Demi-rjian et al 1973) The buccal cusps are slightly wornbut no dentine is exposed There is a mesial contactfacet but no distal interstitial facet This crown is lessworn than the M-G2-419 M1 and larger with a much

TABLE 2 Dental microwear texture data for Neanderthalspecimens from Moula-Guercy

Specimen Tooth Asfc eplsar Smc Tfv HAsfc9 HAsfc81

M-I4-55 Rdm2 295 00030 015 1023919 045 089M-I4-55 RM1 431 00012 015 1420211 054 088M-D1-230 RM1 101 00025 027 463241 037 056M-G2-419 RM1 135 00016 027 1087593 051 064M-L4-TNN5 LM1 251 00042 027 1081540 066 116M-S-27 LP3 387 00022 021 1181266 048 063M-G4-144 LC1 139 00025 027 1910202 043 067M-S-TNN1 RC1 088 00043 042 1080662 046 055M-D1-259 RI2 190 00022 021 1160083 056 117M-D2-588 LI1 433 00013 015 1506999 070 156

MOULA-GUERCY DENTITION 481

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

available at the Human Evolution Research Center at theUniversity of California Berkeley

ABBREVIATIONS

Specimen numbers were assigned as follows ldquoMrdquo des-ignates Moula-Guercy cave followed by a two-characteralphanumeric code corresponding to the excavation grid

square from which the specimen came then a sequentialspecimen number or arbitrary identifier For specimensthat could not be located to a specific square a longercode was given to indicate the range of possible sourcegrid squares An ldquoSrdquo in this position indicates a speci-men recovered from a pit dug outside the standard grid(S 5 ldquosondagerdquo or test pit in French) The sequentialspecimen number stems from the count of all specimens(hominid and non-hominid) within the indicated gridsquare Where a sequential number could not beassigned an arbitrary code was given For example M-G2-419 a mandible fragment is the 419th specimenrecovered from grid square G2 whereas M-L4-TNN5was recovered from square L4 but not assigned a speci-men number until this study began (and so received anarbitrary ldquonew numberrdquo designation) An exception tothis is M--TNN2 which was recovered from the backfillfrom layer XV and cannot be allocated to a grid square

Tooth identification abbreviations follow the conven-tion in which numerical subscripts indicate mandibularand superscripts indicate maxillary (thus a maxillaryright second molar is abbreviated RM2 and a left man-dibular third premolar is LP3) Deciduous teeth aredenoted with a lowercase ldquodrdquo after the designation ofright or left and the tooth type in lowercase eg man-dibular right deciduous second molar is Rdm2

METHODS

Morphological descriptions

Descriptions of hominid material are most useful andrelevant when comparative (White et al 2000) Thedescriptions included here were done through comparisonwith a large cast collection in the Human EvolutionResearch Center at the University of California Berkeleyand against published descriptions (in addition to the pub-lications cited within the descriptions that follow thesemonographs and chapters were studied Martin 19231926 Patte 1957 Sakura 1970 Tillier and Genet-Varcin1980 Heim 1982 Radovcic et al 1988 Madre-Dupouy1992 Condemi 2001 Maureille et al 2001 Bilsboroughand Thompson 2005 Garralda et al 2008) See the Sup-porting Information for list of comparative specimens (allcasts) that were used (this table does not include materialfor which only published data were employed only the listof casts studied) Best-matches were identified and areincluded in the descriptions along with the ways in whichthe Moula specimen differs from the best-match

As part of the morphological descriptions weemployed five descriptive standards that facilitate com-parisons between specimens For describing non-linearshape variation we refer to Crummettrsquos (1994 93)stages for incisor shoveling the Arizona State UniversityDental Anthropology System (ASUDAS Turner et al1991) for describing traits such as the distal accessoryridge and Baileyrsquos (2002) scoring system for postcaninetraits not encompassed by the ASUDAS range of varia-tion which is based only on modern humans Liversidgeand Molleson (2004) provide useful crown and root for-mation stages for deciduous teeth and Demirjian et al(1973) outlined the same for the permanent dentitionWe employ these when relevant

Enamel surface microstructure

To count perikymata in the Moula-Guercy sample rep-licas of 11 of the crowns with the best preservation were

Fig 1 Moula-Guercy Neanderthal mandibular (left panel)and maxillary (right panel) dental material From left to rightocclusal [mesial is up except (A) and (I)] buccallabial and lin-gual views with the exception of (J) where the distal view ispictured Mandible (A) M-G2-419 (B) M-D1-230 (C) M-L4-TNN5 (D) M-G3-251 (E) M-J5-TNN4 (F) M--TNN2 (G) M-G4-144 (H) M-S-TNN1 Maxilla (I) M-I4-55 (J) M-G2-117 (K)M-F3-215 (L) M-H3-73 (M) M-I4-TNN3 (N) M-D2-588 (O) M-D1-259 (P) M-S-27

MOULA-GUERCY DENTITION 479

American Journal of Physical Anthropology

placed on the stage of a measuring microscope (SpectraServices) Under a magnification of 50x along the midlineof the toothrsquos labial surface the positions of perikymatawere recorded using the Vision Gauge software associatedwith the microscope In some instances perikymatacounts were double-checked using counts made from SEMimages In this dental sample the anterior teeth wereminimally worn with the exception of M-D2-588 a LI1

with an oblique incisal edge created by wear Because theteeth were minimally worn perikymata were countedwithin deciles of measured crown height numbered from1 to 10 from the cusp tip to the cement-enamel junction(CEJ) This protocol differs slightly from that establishedby Dean and Reid (2001) which also included decilelengths based on crown height reconstructions from wornteeth For the worn upper LI1 the crown height wasassumed to be the height of the crown along the mesial

edge the least worn When perikymata could not beclearly seen due for example to abrasion they were notcounted All perikymata counts were done by one personwho reported an average percentage difference betweenfirst and second counts as 555 on a set of various non-human primate teeth on which perikymata were countedusing the same microscope used here (Guatelli-Steinberget al 2009) Linear enamel hypoplasias (LEHs) wereidentified using oblique lighting with the aid of a 10xhand lens The locations of LEH defects were marked onthe tooth replica surface Using the measuring micro-scope distances of LEH defects were measured from theCEJ to the midpoint of each defect Widths of defects werealso measured from the cervical to occlusal border of anLEH groove Where possible perikymata were alsocounted within a defect to gain insight into the durationof growth disruption

Fig 2 Mesiodistal and buccolingual lengths for mandibular canines and first molars of Neanderthals (N) Middle PaleolithicHomo sapiens (MHPS) European Upper Paleolithic Homo sapiens (UPHS) Modern Homo sapiens (MHS) and Moula-Guercy (MG)Figure is modified from Benazzi et alrsquos (2011) Figure 4 using data presented and cited therein Note that Moula-Guercy specimensare in the center of the cluster in each panel

TABLE 1 Measurements for all Moula-Guercy Neanderthal Teetha

Specimen number Tooth identification Buccolingual Mesiodistal Cervicoincisal

M-G2-419 RM1 1045 (103)M-G2-419 RM2 111 (116)M-G2-419 RM3 105 (113)M-D1-230 RM1 106 (116)M-L4-TNN5 LM1 109 (119)M-G3-251 Rdm2 90 (98)M-J5-TNN4 Ldm2 00 (104)M--TNN2 LC1 82 76 109M-G4-144 LC1 81 79 116M-S-TNN1 RC1 89 71 114M-I4-55 Rdm2 101 92M-I4-55 RM1 111 114M-F3-215 RM2 116 106M-G2-117 RM2 120 104M-H3-73 Rdm1 00 74M-I4-TNN3 RC1 95 86 (116)M-D2-588 LI1 84 00 00M-D1-259 RI2 85 80 108M-S-27 LP3 107 75

a measurements presented in mm estimates in parentheses00 indicates that the tooth is broken or too worn to accurately assess this measurementTooth identifications follow the same convention as the text Measurement protocols followed Suwa et al (2009 see their SOM)

480 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Dental microwear analysis

Specimens were prepared and analyzed using stand-ard dental microwear texture analysis protocols Moldswere made using Presidentrsquos Jet polyvinylsiloxane den-tal impression material (Coltene-Whaledent) and high-resolution casts were prepared using Epotek 301 epoxyand hardener (Epoxy Technologies) Data were collectedfor all available specimens that had sufficient areas ofunobscured antemortem microwear (Table 2) Microwearsurface preservation for the Moula-Guercy individualswas typically good when compared with many other fos-sil hominids most teeth excluded from this study wereeither unworn or were overwhelmed by postmortemcracks

Nine individuals preserved unobscured antemortemmicrowear (Table 2) Data are reported for a dm2 and aM1 (M-I4-55) three M1s (M-D1-230 M-G2-419 and M-L4-TNN5) two C1s (M-G4-144 and M-S-TNN1) a P3 (M-S-27) an I2 (M-D1-259) and an I1 (M-D2-588) We reportdata here for both specimens of M-I4-55 because both ofthese teeth preserved antemortem microwear

Specimens were analyzed using a Sensofar Pll white-light confocal profiler with an integrated vertical scan-ning interferometer and a 100x long-working-distanceobjective (Solarius) Elevation data were collected fromfour adjacent fields of view each measuring 138 lm 3102 lm for a total work area of 276 lm 3 204 lm foreach tooth Point clouds were generated using a lateralsampling interval of 018 lm and a vertical resolution of005 lm The cheek teeth were sampled for microwearon ldquoPhase IIrdquo facets 9 or 10n and the incisors and can-ines were sampled on the labial surface just above theincisal edge These locations were chosen following con-vention (see Krueger et al 2008 Krueger and Ungar2010) Points representing artifacts such as dust weredeleted prior to analysis

Point clouds were analyzed using Toothfrax and SFraxscale-sensitive fractal analysis software packages (Surf-ract Corp) and data were generated for the five textureattributes that have proven to be particularly useful forcharacterizing microwear surfaces area-scale fractalcomplexity (Asfc) scale of maximum complexity (Smc)heterogeneity of complexity (HAsfc) textural fill volume(Tfv) and length-scale anisotropy of relief (epLsar)HAsfc was calculated by dividing each field of view usingboth 3 3 3 and 9 3 9 grids (HAsfc9 and HAsfc81 respec-tively) Median values for the four fields of view sampledin each tooth are presented here

Detailed descriptions of each of these variables can befound in Scott et al (2006) and Ungar et al (2007)

Complexity is a measure of how surface roughness theratio of surface area to planimetric area changes withscale of observation Complex surfaces are those thatshow increasing roughness at progressively finer scalesof observation a heavily pitted surface with overlappingfeatures of many sizes has a high Asfc value The scaleof maximum complexity reflects the point at which asurface no longer gets rougher with progressively finerscales of observation a surface dominated by large fea-tures but lacking smaller ones would have a high Smcvalue Heterogeneity is measured by dividing each fieldinto a number of equal size subfields and calculatingvariation in Asfc among them heterogeneous surfaceshave higher HAsfc values than do homogeneous onesTextural fill volume is a measure of the summed volumeof small squared cuboids (in this case 2 lm on a side)that would fill a surface divided by that of large squaredcuboids (10lm on a side) an area with many deep mod-erate-size microwear features (between 2 lm and 10 lmin diameter) would have a high Tfv value Finally ani-sotropy is a measure of directionality of surface rough-ness Average relative lengths of transects (ratios ofsummed 18 lm segments to straight-line distancesbetween endpoints) are sampled at different orientations(5 intervals) across each surface Greater variation inthose lengths indicates greater anisotropy a surfacedominated by parallel striations has a higher epLsarvalue than one with randomly oriented scratches or pits

RESULTS

Morphological descriptions

Mandibular M-G2-419 is a right mandibular frag-ment with M1-2 erupted and M3 in the crypt (Fig 1A)The mandibular body is described in detail elsewhere(Defleur et al in preparation) The first molar has anX5 cusp pattern that is only slightly worn with no den-tine exposed The M2 and M3 are unworn although M2

is fully erupted The M2 is relatively unusual for a Ne-anderthal in having only four cusps in the cruciformcusp configuration (Scott and Turner 1997 p 50 Bailey2002) The M3 has a Y5 cusp pattern and root formationto 69 mm (incomplete) An anterior fovea and mid-trigo-nid crest is present on all three molars (score of 2 for allthree molars) a common Neanderthal trait infrequentlyseen on modern human M1s and rare on modern humanM2s and M3s (Bailey 2002) The M1 and M2 are mostsimilar in size and shape to those preserved on theRegourdou mandible though less worn The Moula-Guercy M3 is more rounded and slightly smaller moresimilar in overall size and shape to Hortus VI and Vin-dija 206 and a little smaller than the RM3 of Krapinamandible G

M-D1-230 is a right M1 with a Y5 cusp pattern slightwear on the lingual cusps but no dentine exposed (Fig1B) It has a clear anterior fovea and mid-trigonid crestwith a score of 1 (Bailey 2002) The root is incompletelydeveloped to 2 mm below cervix and fractured on the lin-gual side (Stage E Demirjian et al 1973) Its morphol-ogy is very similar to Vindija 206 (RM1) but less worn

M-L4-TNN5 (Fig 1C) is a left M1 with X5 cusp pat-tern anterior fovea and slight mid-trigonid crest (scoreof 1 Bailey 2002) and Stage G root development (Demi-rjian et al 1973) The buccal cusps are slightly wornbut no dentine is exposed There is a mesial contactfacet but no distal interstitial facet This crown is lessworn than the M-G2-419 M1 and larger with a much

TABLE 2 Dental microwear texture data for Neanderthalspecimens from Moula-Guercy

Specimen Tooth Asfc eplsar Smc Tfv HAsfc9 HAsfc81

M-I4-55 Rdm2 295 00030 015 1023919 045 089M-I4-55 RM1 431 00012 015 1420211 054 088M-D1-230 RM1 101 00025 027 463241 037 056M-G2-419 RM1 135 00016 027 1087593 051 064M-L4-TNN5 LM1 251 00042 027 1081540 066 116M-S-27 LP3 387 00022 021 1181266 048 063M-G4-144 LC1 139 00025 027 1910202 043 067M-S-TNN1 RC1 088 00043 042 1080662 046 055M-D1-259 RI2 190 00022 021 1160083 056 117M-D2-588 LI1 433 00013 015 1506999 070 156

MOULA-GUERCY DENTITION 481

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

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Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

placed on the stage of a measuring microscope (SpectraServices) Under a magnification of 50x along the midlineof the toothrsquos labial surface the positions of perikymatawere recorded using the Vision Gauge software associatedwith the microscope In some instances perikymatacounts were double-checked using counts made from SEMimages In this dental sample the anterior teeth wereminimally worn with the exception of M-D2-588 a LI1

with an oblique incisal edge created by wear Because theteeth were minimally worn perikymata were countedwithin deciles of measured crown height numbered from1 to 10 from the cusp tip to the cement-enamel junction(CEJ) This protocol differs slightly from that establishedby Dean and Reid (2001) which also included decilelengths based on crown height reconstructions from wornteeth For the worn upper LI1 the crown height wasassumed to be the height of the crown along the mesial

edge the least worn When perikymata could not beclearly seen due for example to abrasion they were notcounted All perikymata counts were done by one personwho reported an average percentage difference betweenfirst and second counts as 555 on a set of various non-human primate teeth on which perikymata were countedusing the same microscope used here (Guatelli-Steinberget al 2009) Linear enamel hypoplasias (LEHs) wereidentified using oblique lighting with the aid of a 10xhand lens The locations of LEH defects were marked onthe tooth replica surface Using the measuring micro-scope distances of LEH defects were measured from theCEJ to the midpoint of each defect Widths of defects werealso measured from the cervical to occlusal border of anLEH groove Where possible perikymata were alsocounted within a defect to gain insight into the durationof growth disruption

Fig 2 Mesiodistal and buccolingual lengths for mandibular canines and first molars of Neanderthals (N) Middle PaleolithicHomo sapiens (MHPS) European Upper Paleolithic Homo sapiens (UPHS) Modern Homo sapiens (MHS) and Moula-Guercy (MG)Figure is modified from Benazzi et alrsquos (2011) Figure 4 using data presented and cited therein Note that Moula-Guercy specimensare in the center of the cluster in each panel

TABLE 1 Measurements for all Moula-Guercy Neanderthal Teetha

Specimen number Tooth identification Buccolingual Mesiodistal Cervicoincisal

M-G2-419 RM1 1045 (103)M-G2-419 RM2 111 (116)M-G2-419 RM3 105 (113)M-D1-230 RM1 106 (116)M-L4-TNN5 LM1 109 (119)M-G3-251 Rdm2 90 (98)M-J5-TNN4 Ldm2 00 (104)M--TNN2 LC1 82 76 109M-G4-144 LC1 81 79 116M-S-TNN1 RC1 89 71 114M-I4-55 Rdm2 101 92M-I4-55 RM1 111 114M-F3-215 RM2 116 106M-G2-117 RM2 120 104M-H3-73 Rdm1 00 74M-I4-TNN3 RC1 95 86 (116)M-D2-588 LI1 84 00 00M-D1-259 RI2 85 80 108M-S-27 LP3 107 75

a measurements presented in mm estimates in parentheses00 indicates that the tooth is broken or too worn to accurately assess this measurementTooth identifications follow the same convention as the text Measurement protocols followed Suwa et al (2009 see their SOM)

480 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Dental microwear analysis

Specimens were prepared and analyzed using stand-ard dental microwear texture analysis protocols Moldswere made using Presidentrsquos Jet polyvinylsiloxane den-tal impression material (Coltene-Whaledent) and high-resolution casts were prepared using Epotek 301 epoxyand hardener (Epoxy Technologies) Data were collectedfor all available specimens that had sufficient areas ofunobscured antemortem microwear (Table 2) Microwearsurface preservation for the Moula-Guercy individualswas typically good when compared with many other fos-sil hominids most teeth excluded from this study wereeither unworn or were overwhelmed by postmortemcracks

Nine individuals preserved unobscured antemortemmicrowear (Table 2) Data are reported for a dm2 and aM1 (M-I4-55) three M1s (M-D1-230 M-G2-419 and M-L4-TNN5) two C1s (M-G4-144 and M-S-TNN1) a P3 (M-S-27) an I2 (M-D1-259) and an I1 (M-D2-588) We reportdata here for both specimens of M-I4-55 because both ofthese teeth preserved antemortem microwear

Specimens were analyzed using a Sensofar Pll white-light confocal profiler with an integrated vertical scan-ning interferometer and a 100x long-working-distanceobjective (Solarius) Elevation data were collected fromfour adjacent fields of view each measuring 138 lm 3102 lm for a total work area of 276 lm 3 204 lm foreach tooth Point clouds were generated using a lateralsampling interval of 018 lm and a vertical resolution of005 lm The cheek teeth were sampled for microwearon ldquoPhase IIrdquo facets 9 or 10n and the incisors and can-ines were sampled on the labial surface just above theincisal edge These locations were chosen following con-vention (see Krueger et al 2008 Krueger and Ungar2010) Points representing artifacts such as dust weredeleted prior to analysis

Point clouds were analyzed using Toothfrax and SFraxscale-sensitive fractal analysis software packages (Surf-ract Corp) and data were generated for the five textureattributes that have proven to be particularly useful forcharacterizing microwear surfaces area-scale fractalcomplexity (Asfc) scale of maximum complexity (Smc)heterogeneity of complexity (HAsfc) textural fill volume(Tfv) and length-scale anisotropy of relief (epLsar)HAsfc was calculated by dividing each field of view usingboth 3 3 3 and 9 3 9 grids (HAsfc9 and HAsfc81 respec-tively) Median values for the four fields of view sampledin each tooth are presented here

Detailed descriptions of each of these variables can befound in Scott et al (2006) and Ungar et al (2007)

Complexity is a measure of how surface roughness theratio of surface area to planimetric area changes withscale of observation Complex surfaces are those thatshow increasing roughness at progressively finer scalesof observation a heavily pitted surface with overlappingfeatures of many sizes has a high Asfc value The scaleof maximum complexity reflects the point at which asurface no longer gets rougher with progressively finerscales of observation a surface dominated by large fea-tures but lacking smaller ones would have a high Smcvalue Heterogeneity is measured by dividing each fieldinto a number of equal size subfields and calculatingvariation in Asfc among them heterogeneous surfaceshave higher HAsfc values than do homogeneous onesTextural fill volume is a measure of the summed volumeof small squared cuboids (in this case 2 lm on a side)that would fill a surface divided by that of large squaredcuboids (10lm on a side) an area with many deep mod-erate-size microwear features (between 2 lm and 10 lmin diameter) would have a high Tfv value Finally ani-sotropy is a measure of directionality of surface rough-ness Average relative lengths of transects (ratios ofsummed 18 lm segments to straight-line distancesbetween endpoints) are sampled at different orientations(5 intervals) across each surface Greater variation inthose lengths indicates greater anisotropy a surfacedominated by parallel striations has a higher epLsarvalue than one with randomly oriented scratches or pits

RESULTS

Morphological descriptions

Mandibular M-G2-419 is a right mandibular frag-ment with M1-2 erupted and M3 in the crypt (Fig 1A)The mandibular body is described in detail elsewhere(Defleur et al in preparation) The first molar has anX5 cusp pattern that is only slightly worn with no den-tine exposed The M2 and M3 are unworn although M2

is fully erupted The M2 is relatively unusual for a Ne-anderthal in having only four cusps in the cruciformcusp configuration (Scott and Turner 1997 p 50 Bailey2002) The M3 has a Y5 cusp pattern and root formationto 69 mm (incomplete) An anterior fovea and mid-trigo-nid crest is present on all three molars (score of 2 for allthree molars) a common Neanderthal trait infrequentlyseen on modern human M1s and rare on modern humanM2s and M3s (Bailey 2002) The M1 and M2 are mostsimilar in size and shape to those preserved on theRegourdou mandible though less worn The Moula-Guercy M3 is more rounded and slightly smaller moresimilar in overall size and shape to Hortus VI and Vin-dija 206 and a little smaller than the RM3 of Krapinamandible G

M-D1-230 is a right M1 with a Y5 cusp pattern slightwear on the lingual cusps but no dentine exposed (Fig1B) It has a clear anterior fovea and mid-trigonid crestwith a score of 1 (Bailey 2002) The root is incompletelydeveloped to 2 mm below cervix and fractured on the lin-gual side (Stage E Demirjian et al 1973) Its morphol-ogy is very similar to Vindija 206 (RM1) but less worn

M-L4-TNN5 (Fig 1C) is a left M1 with X5 cusp pat-tern anterior fovea and slight mid-trigonid crest (scoreof 1 Bailey 2002) and Stage G root development (Demi-rjian et al 1973) The buccal cusps are slightly wornbut no dentine is exposed There is a mesial contactfacet but no distal interstitial facet This crown is lessworn than the M-G2-419 M1 and larger with a much

TABLE 2 Dental microwear texture data for Neanderthalspecimens from Moula-Guercy

Specimen Tooth Asfc eplsar Smc Tfv HAsfc9 HAsfc81

M-I4-55 Rdm2 295 00030 015 1023919 045 089M-I4-55 RM1 431 00012 015 1420211 054 088M-D1-230 RM1 101 00025 027 463241 037 056M-G2-419 RM1 135 00016 027 1087593 051 064M-L4-TNN5 LM1 251 00042 027 1081540 066 116M-S-27 LP3 387 00022 021 1181266 048 063M-G4-144 LC1 139 00025 027 1910202 043 067M-S-TNN1 RC1 088 00043 042 1080662 046 055M-D1-259 RI2 190 00022 021 1160083 056 117M-D2-588 LI1 433 00013 015 1506999 070 156

MOULA-GUERCY DENTITION 481

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Dental microwear analysis

Specimens were prepared and analyzed using stand-ard dental microwear texture analysis protocols Moldswere made using Presidentrsquos Jet polyvinylsiloxane den-tal impression material (Coltene-Whaledent) and high-resolution casts were prepared using Epotek 301 epoxyand hardener (Epoxy Technologies) Data were collectedfor all available specimens that had sufficient areas ofunobscured antemortem microwear (Table 2) Microwearsurface preservation for the Moula-Guercy individualswas typically good when compared with many other fos-sil hominids most teeth excluded from this study wereeither unworn or were overwhelmed by postmortemcracks

Nine individuals preserved unobscured antemortemmicrowear (Table 2) Data are reported for a dm2 and aM1 (M-I4-55) three M1s (M-D1-230 M-G2-419 and M-L4-TNN5) two C1s (M-G4-144 and M-S-TNN1) a P3 (M-S-27) an I2 (M-D1-259) and an I1 (M-D2-588) We reportdata here for both specimens of M-I4-55 because both ofthese teeth preserved antemortem microwear

Specimens were analyzed using a Sensofar Pll white-light confocal profiler with an integrated vertical scan-ning interferometer and a 100x long-working-distanceobjective (Solarius) Elevation data were collected fromfour adjacent fields of view each measuring 138 lm 3102 lm for a total work area of 276 lm 3 204 lm foreach tooth Point clouds were generated using a lateralsampling interval of 018 lm and a vertical resolution of005 lm The cheek teeth were sampled for microwearon ldquoPhase IIrdquo facets 9 or 10n and the incisors and can-ines were sampled on the labial surface just above theincisal edge These locations were chosen following con-vention (see Krueger et al 2008 Krueger and Ungar2010) Points representing artifacts such as dust weredeleted prior to analysis

Point clouds were analyzed using Toothfrax and SFraxscale-sensitive fractal analysis software packages (Surf-ract Corp) and data were generated for the five textureattributes that have proven to be particularly useful forcharacterizing microwear surfaces area-scale fractalcomplexity (Asfc) scale of maximum complexity (Smc)heterogeneity of complexity (HAsfc) textural fill volume(Tfv) and length-scale anisotropy of relief (epLsar)HAsfc was calculated by dividing each field of view usingboth 3 3 3 and 9 3 9 grids (HAsfc9 and HAsfc81 respec-tively) Median values for the four fields of view sampledin each tooth are presented here

Detailed descriptions of each of these variables can befound in Scott et al (2006) and Ungar et al (2007)

Complexity is a measure of how surface roughness theratio of surface area to planimetric area changes withscale of observation Complex surfaces are those thatshow increasing roughness at progressively finer scalesof observation a heavily pitted surface with overlappingfeatures of many sizes has a high Asfc value The scaleof maximum complexity reflects the point at which asurface no longer gets rougher with progressively finerscales of observation a surface dominated by large fea-tures but lacking smaller ones would have a high Smcvalue Heterogeneity is measured by dividing each fieldinto a number of equal size subfields and calculatingvariation in Asfc among them heterogeneous surfaceshave higher HAsfc values than do homogeneous onesTextural fill volume is a measure of the summed volumeof small squared cuboids (in this case 2 lm on a side)that would fill a surface divided by that of large squaredcuboids (10lm on a side) an area with many deep mod-erate-size microwear features (between 2 lm and 10 lmin diameter) would have a high Tfv value Finally ani-sotropy is a measure of directionality of surface rough-ness Average relative lengths of transects (ratios ofsummed 18 lm segments to straight-line distancesbetween endpoints) are sampled at different orientations(5 intervals) across each surface Greater variation inthose lengths indicates greater anisotropy a surfacedominated by parallel striations has a higher epLsarvalue than one with randomly oriented scratches or pits

RESULTS

Morphological descriptions

Mandibular M-G2-419 is a right mandibular frag-ment with M1-2 erupted and M3 in the crypt (Fig 1A)The mandibular body is described in detail elsewhere(Defleur et al in preparation) The first molar has anX5 cusp pattern that is only slightly worn with no den-tine exposed The M2 and M3 are unworn although M2

is fully erupted The M2 is relatively unusual for a Ne-anderthal in having only four cusps in the cruciformcusp configuration (Scott and Turner 1997 p 50 Bailey2002) The M3 has a Y5 cusp pattern and root formationto 69 mm (incomplete) An anterior fovea and mid-trigo-nid crest is present on all three molars (score of 2 for allthree molars) a common Neanderthal trait infrequentlyseen on modern human M1s and rare on modern humanM2s and M3s (Bailey 2002) The M1 and M2 are mostsimilar in size and shape to those preserved on theRegourdou mandible though less worn The Moula-Guercy M3 is more rounded and slightly smaller moresimilar in overall size and shape to Hortus VI and Vin-dija 206 and a little smaller than the RM3 of Krapinamandible G

M-D1-230 is a right M1 with a Y5 cusp pattern slightwear on the lingual cusps but no dentine exposed (Fig1B) It has a clear anterior fovea and mid-trigonid crestwith a score of 1 (Bailey 2002) The root is incompletelydeveloped to 2 mm below cervix and fractured on the lin-gual side (Stage E Demirjian et al 1973) Its morphol-ogy is very similar to Vindija 206 (RM1) but less worn

M-L4-TNN5 (Fig 1C) is a left M1 with X5 cusp pat-tern anterior fovea and slight mid-trigonid crest (scoreof 1 Bailey 2002) and Stage G root development (Demi-rjian et al 1973) The buccal cusps are slightly wornbut no dentine is exposed There is a mesial contactfacet but no distal interstitial facet This crown is lessworn than the M-G2-419 M1 and larger with a much

TABLE 2 Dental microwear texture data for Neanderthalspecimens from Moula-Guercy

Specimen Tooth Asfc eplsar Smc Tfv HAsfc9 HAsfc81

M-I4-55 Rdm2 295 00030 015 1023919 045 089M-I4-55 RM1 431 00012 015 1420211 054 088M-D1-230 RM1 101 00025 027 463241 037 056M-G2-419 RM1 135 00016 027 1087593 051 064M-L4-TNN5 LM1 251 00042 027 1081540 066 116M-S-27 LP3 387 00022 021 1181266 048 063M-G4-144 LC1 139 00025 027 1910202 043 067M-S-TNN1 RC1 088 00043 042 1080662 046 055M-D1-259 RI2 190 00022 021 1160083 056 117M-D2-588 LI1 433 00013 015 1506999 070 156

MOULA-GUERCY DENTITION 481

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

more pronounced cusp 5 suggesting that they are notantimeres This LM1 is most similar to Vindija 206 butless worn with the hypoconulid more prominent (likelydue to the reduced amount of wear on the Moula-Guercycrown) This tooth also has similarities to the LM1 of LeMoustier

Mesiodistal and buccolingual measurements for thesethree M1s are shown in Figure 2 relative to populationsof other Neanderthals modern Homo sapiens EuropeanUpper Paleolithic Homo sapiens and Middle PaleolithicHomo sapiens This figure is modified from Benazziet al (2011) and relies on data presented and citedtherein Note that the three Moula-Guercy specimensfall in the middle of the distribution for the three Homosapiens populations and the smaller half of the Neander-thal distribution

M-G3-251 and M-J5-TNN4 (Fig 1DE) are right andleft dm2s respectively M-J5-TNN4 is fractured and assuch is missing the lingual cusps However both crowns(M-G3-251 and M-J5-TNN4) have a similar estimatedmesiodistal length and are similar in morphology andwear stage Both teeth have anterior fovea and a mid-trigonid crest that although worn is a score of 1 Giventhe similar morphology these teeth are interpreted to beantimeres Roots are completely formed on M-G3-251(averaging 9 mm in length from the cervix root develop-ment stage H2 Liversidge and Molleson 2004) Thesetwo crowns are bigger than the dm2 from the Kebarainfant and a little smaller than K66

M--TNN2 (Fig 1F) is a left mandibular canine withthe root incompletely developed (29 mm in length StageE Demirjian et al 1973) The crown has a stronglydeveloped distal accessory ridge (approximately a scoreof 5 on the ASUDAS Turner et al 1991) and is shov-eled very similar in size and morphology to Hortus VIII

M-G4-144 is a left mandibular canine (LC1) with mor-phology and pattern of LEH defects that indicates it isthe antimere of M-S-TNN1 (RC1) (Fig 1G and H respec-tively) Both canines have fully developed roots (167mm and 174 mm from cervix left and right respec-tively Stage H Demirjian et al 1973) but only theright crown has slight apical wear the left is unwornThese two canines are most similar to though less wornthan Hortus VIII

The Moula-Guercy mandibular canines fall within themiddle of the size distribution of other Neanderthalsand European Upper Paleolithic Homo sapiens and to-ward the larger end of the range of variation reportedfor modern Homo sapiens (see Figs 2 and 4 Benazziet al 2011)

Maxillary M-I4-55 (Fig 1I) is a maxillary jaw withright deciduous second molar (dm2) and a permanentfirst molar (M1) As the crowns are still in the jaw rootlength could not be measured The M1 is relativelyskewed with internally compressed cusps This combi-nation of features differentiates Neanderthal maxillarymolars from modern humans (Bailey 2004) There is noCarabellirsquos cusp on the M1 although the dm2 is worn inthis area making it difficult to discern the full extent ofthe original morphology The M1 does have a small piton the lingual surface of the protocone The dm2 is verysimilar in size and shape to the Ldm2 from the Kebarainfant (though more worn) and Gibraltar 2 The M1 ismost similar to Hortus III although the distal aspect ismore rounded on the Moula-Guercy specimen

M-G2-117 is a RM2 with three roots (Fig 1J) Root for-mation is more extensive than is seen for M-F3-215(described below) with a maximum length of 86 mm(Stage F Demirjian et al 1973) This crown is not asskewed as is M-F3-215 although the hypocone is verysmall There is no Carabellirsquos cusp but the crown doeshave a crease and pit between the protocone and hypo-cone on the lingual surface This tooth is very similar insize and shape to Krapina 98 and 96

M-F3-215 (Fig 1K) is a right maxillary second molar(RM2) The root formation is slight with a maximumlength of 13 mm (Stage D Demirjian et al 1973) As iscommon in Neanderthals (Bailey 2004) the crown isvery skewed with the metacone centered buccolinguallybetween the protocone and paracone The hypocone ispresent but diminished and set lingually The crown isunworn with no Carabellirsquos cusp and a crease on the lin-gual surface between the protocone and hypocone LikeM-G2-117 this crown bears a striking resemblance toKrapina 98 and 96

M-H3-73 is a right deciduous maxillary first molar(dm1) with perimortem damage resulting in root andcrown fracture (Fig 1L) The buccal cusp is broken offand the crown is worn with significant dentine expo-sure The roots are fully formed (stage H2 Liversidgeand Molleson 2004) although the buccal roots are bro-ken the lingual root extends 78 mm from cervix Thiscrown is most similar to the Kebara infant although theMoula-Guercy crown is more worn

M-I4-TNN3 is a right maxillary canine with a fullydeveloped crown and an incomplete root that measuresonly 38 mm in length (Fig 1M) The lingual side of thecrown has a strongly expressed mesial lingual ridge andtuberculum dentale giving it a somewhat shoveled appear-ance This RC1 is most similar in morphology to the caninepreserved on Krapina Maxilla E (though less worn)

M-D2-588 (Fig 1N) is a maxillary left central incisor(LI1) The incisal edge is rounded as is typical of Nean-derthals (Crummett 1994 Bailey 2006bb) and lightlyworn exposing a thin line of dentine The distal corner isbroken and the lingual surface has a marked tripletuberculum extension (score of 2 following Crummettrsquos1994 system page 93) Shoveling on the lingual surfacealso approximates a score of 2 following Crummett(1994 93) Because this crown is only lightly worn itsoverall shape is most similar to Krapina Maxilla B par-ticularly when compared with other Neanderthal inci-sors that are often more worn The root is developed toStage G (Demirjian et al 1973)

There are superficial but macroscopic scratch markson the labial surface of M-D2-588 These marks are simi-lar to the vestibular striations on the more incisal andlateral edge of the crown reported for the younger (interms of ontogenetic age) hominid specimens from Simade los Huesos the 600000-year-old Homo heidelbergen-sis population (Lozano et al 2008) Lozano et al (2008)conducted a detailed investigation of this wear acrossthe large Sima de los Huesos fossil assemblage Theiranalysis supports the hypothesis that these scratchesare evidence of the use of the incisors as tools similar tohow Australian Aborigines use their incisors in the prep-aration of different types of materials including the re-moval of bark from branches and holding andstretching materials (Lozano et al 2008 and referencestherein) Similar scratches have also been reported fromNeanderthal specimens from Krapina (Lalueza Fox andFrayer 1997)

482 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

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Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

M-D1-259 (Fig 1O) is a maxillary right lateral incisor(RI2) with a labial convex incisal edge as is typical ofNeanderthals Lingual shoveling is present but notextreme the dominant lingual feature is a strong lingualtubercle with a score between 4 and 5 (Crummett 199493) another feature common to Neanderthals (Crum-mett 1994 Bailey 2006bb) This crown is relativelyunworn similar to M-D2-588 with a fully developed root(Stage H Demirjian et al 1973) Like M-D2-588 itresembles the RI2 of Krapina Maxilla B although it is abit larger and the lingual tubercle less developed com-pared to the Krapina specimen

M-S-27 (Fig 1P) is an unworn LP3 The root is broken75 mm beyond the cervix This crown is most similar inmorphology to the RP3 of Hortus IX although theMoula-Guercy crown is slightly larger and taller

RESULTS

Enamel surface microstructure

Perikymata counts and distribution Both lowercanines with counts of 115 and 118 (see Table 3) fallbelow the range given by Guatelli-Steinberg and Reid(2008) for Neanderthal lower canines (135ndash198 for tenlower canines) The upper canine perikymata total fallstoward the low end of the range for Neanderthal uppercanines given in Guatelli-Steinberg and Reid (2008)(114ndash157 for 14 upper canines) The I1 also falls closerto the low than to the high end of the Neanderthal rangegiven in Guatelli-Steinberg and Reid (2008) (121ndash161for ten I1s) In Figure 3 the Moula-Guercy counts (rep-resented by asterisks) are superimposed over the sum-mary statistics given in Guatelli-Steinberg and Reid(2008) These counts suggest that lateral enamel forma-tion times for these specimens depending on their peri-kymata periodicities may have been on the shorter endof the spectrum for Neanderthals However all of theteeth in this sample exhibited some minimal wear suchthat these perikymata count totals are less than thosethat would have been obtained from newly eruptedteeth These teeth also appear to exhibit a Neanderthalperikymata distribution pattern in which perikymataare less concentrated in the cervical half of the tooth

crown than they are in modern humans (Ramirez-Rozziand Bermudez de Castro 2004 Guatelli-Steinberg et al2007 Guatelli-Steinberg and Reid 2008)

For posterior teeth the percentage of overall enamelformation time represented by lateral enamel is smallerthan it is in anterior teethmdashapproximately 80 in pre-molars (Reid et al 2008) and 65ndash70 in molars (Reidand Dean 2006) Perikymata counts on the posteriorteeth are given in Table 3 Premolars counts are for thebuccal cusp For the molars perikymata were countedon the mesiobuccal cusps

For none of the posterior teeth was it possible toobtain complete perikymata counts owing primarily tosurface abrasion but also to some attrition Totals aregiven for the last 9 deciles of growth for two specimensin Table 3 It is notable that the M-L4-TNN5 LM1 has acount of 112 perikymata in just these 9 deciles Underan SEM used to double-check this number 113 periky-mata were counted on this tooth The Neanderthal rangeof perikymata given in Guatelli-Steinberg and Reid(2008) extends from 75 to 129 perikymata for the lowermolar mesiobuccal cusp placing M-L4-TNN5 toward thehigher end of the Neanderthal range Counts of periky-mata per decile in this tooth are higher than they are inthe RM1 M-D1-230 As can be determined by dividingthe number of perikymata in each decile by the length ofthe decile the spacing of perikymata on M-D1-230 isgenerally wider than it is on the M-L4-TNN5 LM1Under an SEM the perikymata subjectively appear tobe very closely spaced on the M-L4-TNN5 LM1 (Fig 2)Such close spacing might reflect a lower periodicity forthis tooth than that of M-D1-230 (Reid and Ferrell2006) These facts as well as others (see morphologicaldescription above and of hypoplasia below) suggest thatthese right and left molars do not belong to the sameindividual as periodicities are constant for all the teethof an individual (Fitzgerald 1998)

Linear enamel hypoplasia and accentuated perira-dicular bands Table 4 summarizes the number ofLEH defects in the Moula-Guercy sample and their ap-proximate locations given as the midpoint of a line or

TABLE 3 Perikymata counts for anterior (top) and posterior teeth (bottom)

Specimen ToothCH

(mm)

Deciles of crown height numbered from cusp to cervix

Sum

pk incervicalregion1 2 3 4 5 6 7 8 9 10

M-G4-144 LC1 116 11 13 12 12 12 12 16 15M-S-TNN1 RC1 113 11 11 10 10 10 11 11 13 13 15 115 548M--TNN2 LC1 109 9 8 10 9 10 10 12 11 18 21 118 610M-I4-TNN3 RC1 109 11 11 11 12 11 13 10 12 16 15 122 540M-D2-588 LI1 116 15 11 14 12 16 13 13 13 13 13 133 489M-D1-259 RI2 103 15 15 13 17 15

Deciles of crown height numbered from cusp to cervix

Specimen Tooth CH (mm) 1 2 3 4 5 6 7 8 9 10 Sum over 9 deciles

M-S-27 LP3 85 7 8 8 8 8 7 11 11 11 79M-D1-230 RM1 67 12 14 12 11 10 11 10 10M-L4-TNN5 LM1 75 7 6 8 13 15 17 18 16 12 112M-F3-215 RM2 69 7 6 7 6 9 10 12M-G2-117 RM2 72 11 11 22

CH measured crown height pk perikymata

MOULA-GUERCY DENTITION 483

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

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American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

groove from the CEJ For some teeth we were also ableto observe periradicular bands on portions of preservedroots For these teeth we give the location of theseaccentuated bands as a distance from the CEJ

As can be seen in Table 4 only the two M2s were lack-ing in LEH M-G4-144 (LC1) and M-S-TNN1 (RC1) havethe same number of LEH defects (4) and accentuatedperiradicular bands (1) on their partially preservedroots which also occur in similar locations Thesematching defects strongly support the designation ofthese teeth as antimeres (and see morphological descrip-tion above) Similarly the different location of LEH

defects on the right and LM1s (M-D1-230 and M-L4-TNN5 respectively) supports their attribution to differ-ent individuals as does the difference in perikymataspacing on these teeth noted above

The second defect (27 mm from the CEJ) on the M-L4-TNN5 LM1 is particularly interesting in that itencompasses approximately 15ndash20 perikymata (the exactnumber is unclear given difficulty in precisely identify-ing the borders of this defect) Linear enamel hypopla-sias can consist of one or many perikymata dependingupon the length of the growth disruption (Hillson andBond 1997) In furrow-form defects the number of

TABLE 4 Location of linear enamel hypoplasia

Distance from midpoint of LEH or accentuated periradicular band to CEJ (mm)

Specimen Tooth LEH1 LEH2 LEH3 LEH4Accentuated

band 1Accentuated

band 2

M-G4-144 LC1 28 53 69 88 36M-S-TNN1 RC1 30 50 71 90 36M--TNN2 LC1 23M-14-TNN3 RC1 30M-D2-588 LI1 57 80 49M-D1-259 RI2 77M-S-27 LP3 08 30M-D1-230 RM1 05 22M-L4-TNN5 LM1 13 27 31a 52a

M-F3-215 RM2

M-G2-117 RM2

a Observed on distal surface of distal root LEH linear enamel hypoplasia CEJ cementoenamel junction

Fig 3 (A) Moula-Guercy perikymata numbers (stars) plotted among means and 95 confidence intervals for other Neander-thals and for various modern human groups given in Guatelli-Steinberg and Reid (2008) SEM images in comparable regions ofMoula-Guercy first molars M-D1-230 shown as (B) M-L4-TNN5 shown as (C) Note the more closely spaced perikymata in M-L4-TNN5 especially in bracketed region

484 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

perikymata in the occlusal wall of the furrow representsthe period of disrupted growth while the number ofperikymata in the cervical wall appear to represent areturn to normal growth (Hillson and Bond 1997) It

was not possible to differentiate the occlusal and cervicalwalls of the M-L4-TNN5 LM1 defect Nevertheless adefect encompassing 15ndash20 perikymata represents a sig-nificant period of growth disruption

Fig 4 Three-dimensional axiomatic representations of microwear surfaces of specimens described in this study Each imagerepresents 138 lm 3 102 lm for (A) M-I4-55 dm2 (B) M-I4-55 M1 (C) M-D1-230 RM1 (D) M-G2-419 RM1 (E) M-L4-TNN5LM1 (F) M-S-27 P3 (G) M-G4-144 LC1 (H) M-S-TNN1 RC1 (I) M-D1-259 RI2 (J) M-D2-588 LI1

MOULA-GUERCY DENTITION 485

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

RESULTS

Dental microwear analysis

Microwear surface descriptions and texturedata The microwear texture data for the Moula-Guercy specimens are presented in Table 2 and illus-trated in Figures 4ndash6 While there are no comparativebaseline datasets available for premolars or deciduousteeth it is possible to compare the permanent anteriorand molar teeth with published and recently completedNeanderthal studies including the large sample fromKrapina (El Zaatari et al 2011 Krueger 2011 Kruegerand Ungar 2012) Moreover dental microwear textureanalyses of incisors and permanent molars have beenpublished for several bioarcheological groups (El Zaatari2010 Krueger and Ungar 2010 Krueger 2011) and to-gether these data can help put the Moula-Guercy ante-rior teeth and molars into some context Figures 5 and 6compare average values for the Moula-Guercy incisorsand molars (each represented by one tooth per individ-ual) with those reported by several completed Neander-thal and bioarcheological studies (for the incisorsKrueger 2011 Krueger and Ungar 2010 2012 for themolars El Zaatari 2010 El Zaatari et al 2011) Textureattribute averages are presented for Point Hope Ipiutakincisors specifically because Ryan (1980) suggested ante-rior dental microwear similarities between this sampleand Neanderthals Indeed researchers have proposedthat Neanderthal front tooth use closely resembled that

of recent Alaskan Eskimos and Canadian and GreenlandInuit for many decades (eg Brace 1975)

Incisors Both incisors have large deep microwearpits and gouges on their labial surfaces though thereare pits of varying sizes and depths on M-D1-259 Bothalso have striations but these do not dominate eithersurface and they show little directionality Microweartexture data for these individuals not only stand apartfrom the penecontemporaneous Krapina Neanderthalsbut also from all bioarcheological groups presented hereexcept the Point Hope Ipiutak The Moula-Guercy inci-sors share with this Point Hope sample extremely highAsfc Tfv and HAsfc values and low epLsar values (Fig5 note that this shows the average of the Moula-Guercyincisor data presented in Table 2 which includes arange of variation that while seemingly large at firstglance is not remarkable relative to other samples)They separate from all other groups by their low Smcvalues

Canines The maxillary canines are more striatedwith most scratches running apicocervically especiallyfor M-S-TNN1 M-G4-144 has more pits and gougesmostly small to moderate in size and shows less homo-geneity of feature orientation The overall pattern is con-sistent with lower complexity and higher anisotropy

Fig 5 Microwear texture attribute averages for the Moula-Guercy incisors (black) compared with averages for various bioarch-eological groups from Krueger and Ungar (2010) (white) Average values for an Ipiutak sample from Point Hope Alaska and theKrapina Neanderthals (Krueger 2011 Krueger and Ungar 2012) are also presented for comparison (grey and stripe respectively)

486 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

values compared with the incisors The Smc values arealso relatively high

Premolar The M-S-27 surface is deeply pitted withmicrowear features of varying sizes There are also afew deep striations Its Asfc value is high and epLsarand Smc values are comparable to those of the M-D1-259 RI2 and its HAsfc values are in the range of thosefor the canines and permanent molars

Permanent molars The permanent molar ldquophase IIrdquofacets are dominated by small to moderate sized andfairly shallow pits These surfaces also have a few largerstriations but these tend not to show tightly constrainedorientations Microwear texture values for the fourspecimens vary but averages for all of the attributes aremost comparable to those reported for Neanderthalsfrom wooded environments (El Zaatari et al 2011) TheMoula-Guercy microwear texture attributes are unre-markable compared with those for nonhuman primatemolars (Scott et al 2006 Ungar et al 2007) The TfvepLsar and Smc averages are also well within theranges of those reported by El Zaatari (2010) for bioarch-eological samples though the Moula-Guercy molar Asfcaverage is near the low end (Fig 6) El Zaatari did notreport HAsfc9 or HAsfc81 values

Deciduous molars The deciduous molar of M-14-55has microwear features similar to those on facet 9 of itsM1 These include large deep microwear pits and a fewstriations The Asfc epLsar Tfv and HAsfc values are inline with those for the permanent molars and the Smcvalue is the same as that of the M1 of this specimen

DISCUSSION

Although Neanderthal teeth have been recognized todiffer from modern human teeth for well over a century

(eg Gorjanovic-Kramberger 1906 Keith 1913) andfrom those of Homo erectus for almost as long (eg Wei-denreich 1937) recent work by Bailey (2002 20042006aa b) Bailey and Lynch (2005) Crummett (1994)Irish (1998) Kupczik and Hublin (2010) Martinon-Torres et al (2006) and others have refined andincreased our understanding of the diagnostic elementsTheir work has established that maxillary and mandibu-lar incisors M1 P4 and M1-3 of Neanderthals have suchunique combinations of traits that these teeth are oftenidentifiable even if found in isolation (Bailey 2006cS43)

The Moula-Guercy dental assemblage has representa-tives for all of these more diagnostic elements save forthe P4 and all of these specimens demonstrate traitscharacteristic of Neanderthals For example the M1

from M-I4-55 has the typically Neanderthal skewed andinternally compressed cusp configuration the M1-3 of M-G2-419 have the Neanderthal configuration of stronglyexpressed mid-trigonid crests and large anterior foveaand the two incisors are characteristically Neanderthalin their labial convexity shoveling and tuberculum den-tale None of the dental material recovered from Moula-Guercy provide evidence of a hominid taxon other thanNeanderthals

The dental remains from Moula-Guercy add to thecontinually growing sample of Neanderthals fromEurope and Eurasia (eg Bailey and Hublin 2006Arsuaga et al 2007 Trinkaus et al 2007) While all ofthese specimens increase our understanding of the geo-graphic and temporal variation of this hominid taxonconsiderable controversy about the evolutionary historyof Neanderthals remains (as succinctly summarized inEndicott et al 2010)

Turning to a different data set from the fossilized mor-phology recent reassessment of the ancient mtDNA datafrom Neanderthals (Endicott et al 2010) finds thatNeanderthals and H sapiens shared a last mtDNAcommon ancestor 410ndash440 kya Endicott et al (2010)interpret these genetic data to support only the paleon-tological hypothesis that Neanderthals and the lineage

Fig 6 Microwear texture attribute averages for the Moula-Guercy permanent molars (black) compared with averages for vari-ous bioarcheological groups from El Zaatari (2010) (white) and wooded-environment Neanderthals (El Zaatari et al 2011)

MOULA-GUERCY DENTITION 487

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

leading to H sapiens diverged in the Middle Pleistocenefrom Homo heidelbergensis Interestingly they also findthat Neanderthals and H sapiens have within speciespopulation coalescent dates of about 115 kya and 137kya respectivelymdasha relatively recent date that may indi-cate substantial genetic drift during the MIS 6 glaciation(130ndash191 kya) (Endicott et al 201093) With this pur-ported demographic history it is perhaps not surprisingthat the specimens from Moula-Guercy have some simi-larities in size and morphology to the relatively penecon-temporaneous site of Krapina Croatia at approximately100 kya although more work needs to be done (and inconjunction with the rest of the skeletal material) to testthis hypothesis Denoting further affinities based onthese incomplete and isolated dental remains would beimprudent at this time

In terms of the paleobiology of the Neanderthals theMoula-Guercy dental remains yield an interesting com-bination of expected and unexpected results For exam-ple we find from the enamel surface microstructureresults that the Moula-Guercy specimens are fairly char-acteristic of Neanderthals Perikymata in Neanderthalteeth tend to be distributed more evenly along theenamel surface than they are in the teeth of modernhumans such that the percentage of total perikymata inthe cervical halves of Neanderthal teeth is smaller thanthat of modern humans (Guatelli-Steinberg et al 2007)In Neanderthals average percentages of total periky-mata present in the cervical halves of teeth range from584 (I1) to 624 (I2) whereas in various modernhuman samples averages range from 641 (southernAfrican I1 and Northern European C1) to 685 (InupiaqI2) (Guatelli-Steinberg et al 2007) The Moula-Guercyenamel surface microstructure data yield evidence of aNeanderthal pattern of development although at thelower end of the range of variation

However in the Moula-Guercy sample the presence ofLEH defects in the lower first molars of presumablytwo different individuals suggests an early occurrence ofphysiological stress that is not seen in the Krapina sam-ple or other studied Neanderthals LEH is less prevalenton molars than it is on other permanent teeth in bothmodern humans and Neanderthals (Molnar and Molnar1985 Goodman and Rose 1990 Hutchinson et al1997) presumably because of the way molars grow (Hill-son and Bond 1997) In contrast to the presence of LEHon the first molars reported here for Moula-Guercy noLEH defects were reported on any of the M1s of the Kra-pina Neanderthals (Molnar and Molnar 1985 Hutchin-son et al 1997) Ogilvie et al (1989) whose dataincluded enamel hypoplasia of all types (not only LEHbut also enamel pits) did however find some enamel hy-poplasia on first molars in an expanded sample of Nean-derthals from the Near East and Europe

The ontogenetic timing of this stress is somewhat com-plicated to pinpoint The first molar initiates before birthin modern humans and completes formation early in thethird year of life (Reid and Dean 2006) First molarenamel formation may have even been completedslightly earlier in Neanderthals (Smith et al 20072009 2010) Using modern human standards to ageLEH defects Skinner (1996) found that LEH in his Mid-dle Paleolithic samples clustered between 35 and 55years of age while in his upper Paleolithic sample LEHdefects were more evenly distributed between 2 and 5years of age In their study of the 40 kya Le Moustier1 Neanderthal Bilsborough and Thompson (2005)

estimated that the majority of hypoplastic insultsoccurred between 3 and 4 years of age They suggestthat this could be the result of weaning (Thompson1998 Bilsborough and Thompson 2005) although giventhe developmental timing of tooth mineralization andthe nature of the weaning process the ability to linkLEHs directly with weaning is dubious (Humphrey2008) While the early stress indicated by the Moula-Guercy first molar LEHs is atypical of Middle Paleolithicindividuals the implications of what the perikymatadata imply in terms of life history differences betweenhumans and Neanderthals remain unclear (as discussedin detail in Guatelli-Steinberg and Reid 2008)

Antemortem molar microwear data suggest that theNeanderthals from Moula-Guercy did not differ signifi-cantly from some modern humans in terms of the frac-ture properties of the food they were consuming (seeUngar et al 2007 for non-human primate comparativemolar data) Moreover the texture attributes of theseindividuals are most congruent with other Neanderthalsfrom wooded environments consistent with the recon-structed environmental context of the Moula-Guercyhominins (El Zaatari et al 2011) These data suggestthat the Moula-Guercy individuals most likely relied onmeat for subsistence but ate other foods perhapsincluding a richer plant resource base (El Zaatari et al2011)

The anterior dental microwear data indicate thatthese Neanderthals may have used their teeth as toolssimilar to the practices of some modern human popula-tions from the arctic (eg Brace 1975) Indeed the inci-sor and canine microwear texture signatures of theMoula-Guercy specimens examined here are most simi-lar to those of the Ipiutak from Point Hope Alaska Thisbioarcheological sample is inferred to have participatedin intense clamping and grasping activities in relation tothe production of clothing (Krueger 2011) This suggeststhat these Neanderthal individuals may have been par-ticipating in similar behavioral strategies or at leastbehaviors that also required substantial anterior toothloading

On the other hand the Moula-Guercy Neanderthalsare different in their anterior dental microwear texturescompared to those from the penecontemporaneous site ofKrapina While the incisor textures of Moula-Guercy areon the extreme ends of the spectrum overall the Kra-pina sample is moderate in its values (Fig 4) The Kra-pina sample shows moderate complexity textural fillvolume and heterogeneity and moderately low anisot-ropy (Krueger 2011 Krueger and Ungar 2012) Whilethese values fall within the range of using the teeth astools they are not congruent with intense clamping orgrasping activities The Krapina Neanderthals are mostsimilar in their values to the Coast Tsimshian fromPrince Rupert Harbour a sample inferred to have usedtheir anterior dentition in vegetation softening for weav-ing tasks (Cybulski 1974 Krueger 2011 Krueger andUngar 2012) This not only indicates a lower anteriorloading regime in these Neanderthals but is also con-sistent with the inferred importance of plant resources(Henry et al 2011) Consequently the data from Moula-Guercy coupled with those from Krapina suggest vary-ing Neanderthal behavioral strategies

The larger-scale macro-striations noted on the labialsurface of one of the maxillary incisors from Moula-Guercy also suggest that these Neanderthals partici-pated in several behavioral practices affecting their

488 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

anterior teeth These macro-striations distinct fromsmaller microwear textures presented above are similarto those reported for Neanderthals from Krapina(Lalueza Fox and Frayer 1997) and the much older (per-haps as old as 600000 years ago) hominids from Simade los Huesos (Lozano et al 2008)

In conclusion in the morphological descriptions pre-sented here we firmly establish that the Moula-Guercyhominids were Neanderthals with no evidence of therebeing another hominid taxon represented Until excava-tions are completed at the site we will not know the fullextent of this population ie the number of individualsor the demographic composition However from theremains recovered to date it is evident that Moula-Guercy already provides important sets of morphologi-cal developmental and behavioral data bearing on ourunderstanding of the evolutionary history of thishominid

ACKNOWLEDGMENTS

We want to extend our thanks to the numerous peoplewithin the Human Evolution Research Center at the Uni-versity of California Berkeley who assisted with thisresearch especially Tim D White Kyle Brudvik andRebecca Jabbour Thanks also to David Degusta WhitneyReiner and five anonymous reviewers who provided criti-cal comments on a previous version of this manuscriptMany thanks are also due to Rebecca Ferrell who collabo-rated with us on the perikymata and LEH data and tookSEM images of the Moula-Guercy teeth AD specificallythanks la Municipalite de Soyons (Ardeche) la DirectionGenerale des Affaires Culturelles de la Region Rhone-Alpes le Conseil General de lrsquoArdeche et Fanny Derym forits support and assistance Funding for this research wasprovided in part by National Science Foundation DoctoralDissertation Improvement Grant 0925818 to KLK andPSU the measuring microscope used in the analysis ofenamel surface microstructure was funded by NSF grantBCS-0607520 to DGS

LITERATURE CITED

Arsuaga JL Villaverde V Quam R Martınez I Carretero JMLorenzo C Gracia A 2007 New Neandertal remains fromCova Negra (Valencia Spain) J Hum Evol 5231ndash58

Bailey SE 2002 A closer look at Neanderthal postcanine dentalmorphology the mandibular dentition Anat Rec 269148ndash156

Bailey SE 2004 A morphometric analysis of maxillary molarcrowns of Middle-Late Pleistocene hominins J Hum Evol47183ndash198

Bailey SE 2006a The evolution of non-metric dental variationin Europe Mitteilungen der Gesellshaft feurour Urgeschichte159ndash30

Bailey SE 2006b Beyond shove-shaped incisors Neandertaldental morphology in a comparative context Periodicum Biol-ogorum 108253ndash267

Bailey SE 2006c Who made the early Aurignacian Evidencefrom isolated teeth Am J Phys Anthropol 129(S43)60

Bailey SE Hublin J-J 2006 Dental remains from the Grotte deRenne at Arcy-sur-Cure (Yonne) J Hum Evol 50485ndash508

Bailey SE Lynch JM 2005 Diagnostic differences in mandibu-lar P4 shape between Neandertals and anatomically modernhumans Am J Phys Anthropol 126268ndash277

Benazzi S Viola B Kullmer O Fiorenza L Harvati K Paul TGruppioni G Weber GW Mallegni F 2011 A reassessment ofthe Neanderthal teeth from Taddeo Cave (southern Italy) JHum Evol 61377ndash87

Bilsborough A Thompson JL 2005 The dentition of the LeMoustier 1 Neandertal In Ullrich H editor The Neandertaladolescent Le Moustier 1 new aspects new results BerlinStaatliche Museen u Berline ndash Preubischer Kulturbesitz p157ndash186

Boule M 1921 Les homes fossils Paris MassonBrace CL 1975 Comment on did La Ferrassie 1 use his teeth

as a tool Curr Anthropol 16396ndash397Brace CL Rosenberg KR Hunt KD 1987 Gradual change in

human tooth size in the Late Pleistocene and Post-Pleisto-cene Evolution 41705ndash720

Carbonell VM 1965 The teeth of the Neanderthal child fromGibraltar a re-evaluation Am J Phys Anthropol 2341ndash49

Condemi S 2001 Les Neandertaliens de la Chaise (abri Bour-geois-Delaunay) Paris Editions du Comite des travaux his-toriques et scientifiques Societe prehistorique francaise

Crevecoeur I Bayle P Rougier H Maureille B Higham T vander Plicht J De Clerck N Semal P 2010 The Spy VI child anewly discovered Neandertal infant J Hum Evol 59641ndash656

Crummett T 1994 The evolution of shovel shaping regionaland temporal variation in human incisor morphology [PhDDissertation] University of Michigan Ann Arbor

Cybulski JS 1974 Tooth wear and material culture pre-contactpatterns in the Tsimshian area British Columbia Syesis731ndash35

Dean MC Reid DJ 2001 Perikymata spacing and distributionon hominid anterior teeth Am J Phys Anthropol 116209ndash215

Dean MC Stringer CB Bromage TG 1986 Age at death of theNeanderthal child from Devilrsquos Tower Gibraltar and theimplications for studies of general growth and development inNeanderthals Am J Phys Anthropol 70301ndash309

Defleur A Cregut-Bonnoure E Desclaux E 1998 First observa-tion of an Eemian sequence with human remains in theBaume Moula-Guercy filling (Soyons Ardeche) C R Acad SciII 326453ndash458

Defleur A Cregut-Bonnoure E Desclaux E and Thinon M2001 Paleoenvironmental presentation of the filling fromBaume Moula-Guercy Soyons (Ardeche) palaeoclimatic andchronological implications LrsquoAnthropologie 105369ndash408

Defleur A Dutour O Valladas H Combier J Vandermeersch B1993a Discovery of Mousterian human remains in AbriMoula (Soyons Ardeche) C R Acad Sci II 3161005ndash1010

Defleur A Dutour O Valladas H and Vandermeersch B 1993bCannibals among the Neanderthals Nature 362214

Defleur A White T Valensi P Slimak L Cregut-Bonnoure E1999 Neanderthal cannibalism at Moula-Guercy ArdecheFrance Science 286128ndash131

Demirjian A Goldstein H Tanner JM 1973 A new system ofdental age assessment Hum Biol 45211ndash227

Desclaux E and Defleur A 1997 Etude preliminaire des micro-mammiferes de la Baume Moula-Guercy a Soyons (ArdecheFrance) Systematique biostratigraphie et paleoecologie Qua-ternaire 8213ndash223

Endicott P Ho SYW Stringer C 2010 Using genetic evidenceto evaluate four palaeoanthropological hypotheses for the tim-ing of Neanderthal and modern human origins J Hum Evol5987ndash95

El Zaatari S 2010 Occlusal microwear texture analysis and thediets of historicalprehistoric hunter-gatherers Int J Osteoar-chaeol 2067ndash87

El Zaatari S Grine FE Ungar PS Hublin J-J 2011 Ecogeo-graphic variation in Neandertal dietary habits evidence fromocclusal microwear texture analysis J Hum Evol 61411ndash424

Fitzgerald CM 1998 Do enamel microstructures have regulartime dependency J Hum Evol 35371ndash386

Garralda MD Maureille B Pautrat Y Vandermeersch B 2008La molaire drsquoenfant Neandertalien de Genay (Cote-drsquoOrFrance) Reflexions sur la variabilite dentaire des Neander-taliens Paleo 2089ndash100

Goodman AH Rose JC 1990 Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasias and associ-ated histological structures Yearb Phys Anthropol 3359ndash110

MOULA-GUERCY DENTITION 489

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Gorjanovic-Kramberger K 1906 Der Diluviale Mensch vonKrapina in Kroatien Wiesbaden Kreidel

Grine FE 1987 Quantitative analysis of occlusal microwear inAustralopithecus and Paranthropus Scanning Microsc 1647ndash656

Guatelli-Steinberg D Ferrell RJ Spence J Talabere T HubbardA Schmidt S 2009 Sex differences in anthropoid mandibularcanine lateral enamel formation Am J Phys Anthropol140216ndash233

Guatelli-Steinberg D Reid DJ 2008 What molars contribute toan emerging understanding of lateral enamel formation inNeandertals vs modern humans J Hum Evol 54236ndash250

Guatelli-Steinberg D Reid DJ Bishop TA 2007 Did the lateralenamel of Neandertal anterior teeth grow differently fromthat of modern humans J Hum Evol 5272ndash84

Heim J-L 1982 Les Enfants Neandertaliens de la FerrassieParis Masson

Henry AG Brooks AS Piperno DR 2011 Microfossils in calcu-lus demonstrate consumption of plants and cooked foods inNeanderthal diets (Shanidar III Iraq Spy I and II Belgium)PNAS 108486ndash491

Hillson S 1996 Dental anthropology Cambridge CambridgeUniversity Press

Hillson S Bond S 1997 The relationship of enamel hypoplasiato the pattern of tooth crown growth a discussion Am JPhys Anthropol 10489ndash103

Humphrey L 2008 Enamel traces of early lifetime events InSchutkowski H editor Between biology and culture NewYork Cambridge University Press p 186ndash286

Hutchinson DL Larsen CS Choi I 1997 Stressed to the maxPhysiological perturbation in the Krapina Neandertals CurrAnthropol 38904ndash914

Irish JD 1998 Ancestral dental traits in recent Sub-SaharanAfricans and the origins of modern humans J Hum Evol3481ndash98

Kallay J 1951 Healed tooth fractures in a Krapina Neander-thal Am J Phys Anthropol 9369ndash371

Keith A 1913 Problems relating to the teeth of the earlierforms of prehistoric man Proc R Soc Med VI OdontolSect111

Krueger KL 2011 Dietary and behavioral strategies of Nean-dertals and anatomically modern humans evidence from an-terior dental microwear texture analysis [PhD dissertation]Fayetteville University of Arkansas

Krueger KL Scott JR Kay RF Ungar PS 2008 Technical notedental microwear textures of ldquoPhase Irdquo and ldquoPhase IIrdquo facetsAm J Phys Anthropol 137485ndash490

Krueger KL Ungar PS 2010 Incisor microwear textures of fivebioarcheological groups Int J Osteoarchaeol 20549ndash560

Krueger KL Ungar PS 2012 Anterior dental microwear tex-ture analysis of the Krapina Neandertals Cent Eur J Geosci4651ndash662

Kupczik K Hublin J-J 2010 Mandibular molar root morphol-ogy in Neandertals and Late Pleistocene and recent Homosapiens J Hum Evol 59525ndash541

Lalueza Fox C Frayer DW 1997 Non-dietary marks in the an-terior dentition of the Krapina Neanderthals Int J Osteoar-chaeol 7133ndash149

Liversidge HM Molleson T 2004 Variation in crown and rootformation and eruption of human deciduous teeth Am J PhysAnthropol 123172ndash180

Lozano M Bermudez de Castro JM Carbonell E Arsuaga JL2008 Non-masticatory uses of anterior teeth of Sima de losHuesos individuals (Sierra de Atapuerca Spain) J Hum Evol55713ndash728

Macchiarelli R Bondioli L Debehath A Mazurier A Tourne-piche J-F Birch W Dean C 2006 How Neandertal molarteeth grew Nature 444748ndash751

Madre-Dupouy M 1992 LrsquoEnfant de Roc de Marsal Cahiers dePaleoanthropologie Paris Editions du Centre National de laRecherche Scientifique

Martin H 1923 LrsquoHomme Fossile de la Quina Paris GastonDoin Editeur

Martin H 1926 Recherches sur lrsquoEvolution du Mousterien dansle Gisement de La Quina (Charente) Quatrieme VolumeLrsquoEnfant fossile de La Quina Angouleme ImprimerieOuvriere

Martinon-Torres M Bastir M Bermudez de Castro JM GomezA Sarmiento S Muela A Arsuaga JL 2006 Hominin lowersecond premolar morphology evolutionary inferences throughgeometric morphometric analysis J Hum Evol 50523ndash533

Maureille B Rougier H Houeuroet F Vandermeersch B 2001 Lesdents inferieures de Neandertalien Regourdou 1 (site deRegourdou commune de Montignac Dordogne) analysesmetriques et comparatives Paleo [En ligne] 13 URL httppaleorevuesorg1043

Molnar S Molnar IM 1985 The prevalence of enamel hypopla-sia among the Krapina Neandertals Am Anthropol 87536ndash549

Ogilvie MD Curran BK Trinkaus E 1989 Prevalence and pat-terning of dental enamel hypoplasia among the NeandertalsAm J Phys Anthropol 7925ndash41

Patte E 1957 LrsquoEnfant Neanderthalien du Pech de LrsquoAzeParis Masson et Cie

Radovcic J Smith FH Trinkaus F Wolpoff MH 1988 The Kra-pina hominids an illustrated catalog of skeletal collectionMladost Croatian Natural History Museum

Ramirez-Rozzi FV Bermudez de Castro JM 2004 Surprisinglyrapid growth in Neanderthals Nature 428936ndash939

Reid DJ Dean MC 2006 Variation in modern human enamelformation times J Hum Evol 50329ndash346

Reid DJ Ferrell RJ 2006 The relationship between number ofstriae of Retzius and their periodicity in imbricational enamelformation J Hum Evol 50195ndash202

Reid DJ Guatelli-Steinberg D Walton P 2008 Variation inmodern human premolar enamel formation times implica-tions for Neandertals J Hum Evol 54225ndash235

Ryan AS 1980 Anterior dental microwear in hominid evolu-tion comparisons with human and nonhuman primates[PhD Dissertation] University of Michigan Ann Arbor

Sakura H 1970 Dentition of the Amud man In Suzuki HTakai F editors The Amud man and his cave site TokyoThe University of Tokyo p 207ndash229

Sanzelle S Pilleyre T Montret M Faeuroın J Miallier D Camus Gde Goeuroer de Herve A Defleur A 2000 Datation par thermolu-minescence etude drsquoune correlation chronologique possibleentre le maar de La Vestide-du-Pal et un niveau de tephra deLa Baume-Moula-Guercy (Ardeche France) C R Acad Sci IIA330541ndash546

Scott GR Turner CG II 1997 The anthropology of modernhuman teeth New York Cambridge University Press

Scott RS Ungar PS Bergstrom TS Brown CA Childs BE Tea-ford MF Walker A 2006 Dental microwear texture analysistechnical considerations J Hum Evol 51339ndash349

Skinner M 1996 Developmental stress in immature homininesfrom Late Pleistocene Eurasia evidence from enamel hypo-plasia J Archaeol Sci 23833ndash852

Smith TM Harvati K Olejniczak AJ Reid DJ Hublin J-J Pan-agopoulou E 2009 Brief communication dental developmentand enamel thickness in the Lakonis Neanderthal molar AmJ Phys Anthropol 138112ndash118

Smith TM Tafforeau P Reid DJ Pouech J Lazzari V ZermenoJP Guatelli-Steinberg D Olejniczak AJ Hoffman A RadovcicJ Makaremi M Toussaint M Stringer C Hublin J-J 2010Dental evidence for ontogenetic differences between modernhumans and Neanderthals Proc Natl Acad Sci USA10720923ndash20928

Smith TM Toussaint M Reid DJ Olejniczak AJ Hublin J-J2007 Rapid dental development in a Middle Paleolithic Bel-gian Neanderthal Proc Natl Acad Sci USA 10420220ndash20225

Stringer CB Humphrey LT Compton T 1997 Cladistic analysisof dental traits in recent humans using a fossil outgroup JHum Evol 32389ndash402

Suwa G Kono RT Simpson SW Asfaw B Lovejoy CO WhiteTD 2009 Paleobiological implications of the Ardipithecusramidus dentition Science 32694ndash99

490 LJ HLUSKO ET AL

American Journal of Physical Anthropology

Ten Cate AR 1994 Oral histology development structure andfunction 4th edition St Louis CV Mosby

Thompson JL 1998 Neanderthal growth and development InUlijaszek SJ Johnston FE Preece MA editors The Cam-bridge encyclopedia of human growth and development Cam-bridge Cambridge University Press p 106ndash107

Tillier AM Genet-Varcin E 1980 La plus ancienne mandibuledrsquoenfant decouverte en France dans le gisement de La Chaisede Vouthon (Abri Suard) en Charente Z Morph Anthropol71196ndash214

Trinkaus E 2006 Modern human versus Neandertal evolution-ary distinctiveness Curr Anthropol 47597ndash620

Trinkaus E Maki J Zilhao J 2007 Middle Paleolithic humanremains from the Gruta da Oliveira (Torres Novas) PortugalAm J Phys Anthropol 134263ndash273

Turner CG II Nichol CR Scott GR 1991 Scoring proceduresfor key morphological traits of the permanent dentition TheArizona State University dental anthropology system InKelley MA Larsen CS editors Advances in dental anthropol-ogy New York John Wiley p 13ndash31

Ungar PS 2011 Dental evidence for the diets of Plio-Pleisto-cene hominins Am J Phys Anthropol 146 Suppl 5347ndash62

Ungar PS Scott RS Scott JR Teaford MF 2007 Dental micro-wear analysis historical perspectives and new approachesIn Irish JD Nelson GC editors Technique and applicationin dental anthropology Cambridge Cambridge UniversityPress p 389ndash425

Walker MJ Gibert J Lopez MV Lombardi AV Perez- Perez ASchwenninger J-L Zilhao J Trinkaus E 2008 Late Neander-tals in Southeastern Iberia Sima de las Palomas del CabezoGordo Murcia Spain Proc Natl Acad Sci USA 10520631ndash20636

Walker MJ Ortega J Parmova K Lopez MV Trinkaus E 2011Morphology body proportions and postcranial hypertrophy ofa female Neandertal from the Sima de las Palomas south-eastern Spain Proc Natl Acad Sci USA 10810087ndash10091

Weidenreich F 1937 The dentition of Sinanthropus pekinensisa comparative odontography of the hominids PalaeontologiaSinica New Series D No 1 Whole Series No 101

White TD Suwa G Simpson S Asfaw B 2000 Jaws and teethof Australopithecus afarensis from Maka Middle AwashEthiopia Am J Phys Anthropol 11145ndash68

MOULA-GUERCY DENTITION 491

American Journal of Physical Anthropology