The bony labyrinth of Neanderthalscontent.csbs.utah.edu/~rogers/ant6299/readings/Spoor-JHE-44... · Neanderthals and modern humans can be used to assess the phylogenetic aﬃnities

The bony labyrinth of Neanderthals

Fred Spoora*, Jean-Jacques Hublinb, Marc Braunc, Frans Zonneveldd

aEvolutionary Anatomy Unit, Dept. of Anatomy and Developmental Biology, University College London, Rockefeller Building,University Street, London WC1E 6JJ, UK

bLaboratoire d’Anthropologie, Universite de Bordeaux 1, Avenue des facultes, 33405 Talence, FrancecDept. of Anatomy, University of Nancy I, France

dDepartment of Radiology, Utrecht University Hospital, The Netherlands

Received 3 July 2002; accepted 7 October 2002

Abstract

This paper presents a comprehensive comparative analysis of the Neanderthal bony labyrinth, a structure locatedinside the petrous temporal bone. Fifteen Neanderthal specimens are compared with a Holocene human sample, as wellas with a small number of European Middle Pleistocene hominins, and early anatomically modern and EuropeanUpper Palaeolithic humans. Compared with Holocene humans the bony labyrinth of Neanderthals can be characterizedby an anterior semicircular canal arc which is smaller in absolute and relative size, is relatively narrow, and shows moretorsion. The posterior semicircular canal arc is smaller in absolute and relative size as well, it is more circular in shape,and is positioned more inferiorly relative to the lateral canal plane. The lateral semicircular canal arc is absolutely andrelatively larger. Finally, the Neanderthal ampullar line is more vertically inclined relative to the planar orientation ofthe lateral canal. The European Upper Palaeolithic and early modern humans are most similar, although not fullyidentical to Holocene humans in labyrinthine morphology. The European Middle Pleistocene hominins show thetypical semicircular canal morphology of Neanderthals, with the exception of the arc shape and inferiorly position ofthe posterior canal and the strongly inclined ampullar line. The marked difference between the labyrinths ofNeanderthals and modern humans can be used to assess the phylogenetic affinities of fragmentary temporal bonefossils. However, this application is limited by a degree of overlap between the morphologies. The typical shape of theNeanderthal labyrinth appears to mirror aspects of the surrounding petrous pyramid, and both may follow fromthe phylogenetic impact of Neanderthal brain morphology moulding the shape of the posterior cranial fossa. Thefunctionally important arc sizes of the Neanderthal semicircular canals may reflect a pattern of head movementsdifferent from that of modern humans, possibly related to aspects of locomotor behaviour and the kinematic propertiesof their head and neck.� 2003 Elsevier Science Ltd. All rights reserved.

Keywords: bony labyrinth; temporal bone; Neanderthals; Pleistocene hominins

Introduction

The temporal bone of Neanderthals shows asuite of derived morphological features (e.g.,

* Corresponding authorE-mail address: [email protected] (F. Spoor).

Journal of Human Evolution 44 (2003) 141–165

0047-2484/03/$ - see front matter � 2003 Elsevier Science Ltd. All rights reserved.doi:10.1016/S0047-2484(02)00166-5

Vallois, 1969; Hublin, 1978; Santa Luca, 1978;Condemi, 1988), and it is, therefore, among themost diagnostic parts of the Neanderthal skull.Efforts to explore the inside of the Neanderthaltemporal bone have employed radiological tech-niques to visualize mastoid pneumatization(Kindler, 1960; Kindler and Kiefer, 1963) and,inside the petrous part, the bony labyrinth(Delattre et al., 1967; Fenart and Empereur-Buisson, 1970; Wind and Zonneveld 1985;Zonneveld and Wind 1985; Silipo et al., 1991;Zollikofer et al., 1995). The latter structurehouses the inner ear, which includes the senseorgans for the perception of sound in the cochlea,and of movement and spatial orientation in thevestibule and semicircular canals. Using computedtomography, Hublin et al. (1996) provided a firstcomparative analysis of the bony labyrinth ofNeanderthals. The study identified a numberof characters which appear to distinguishNeanderthals from both modern humans andHomo erectus, and used these to establish thephylogenetic affinities of the infant Chatel-perronian temporal bone from Arcy-sur-Cure(France). These findings confirmed previous obser-vations that the mammalian bony labyrinth tendsto show a consistent, species-specific morphology(Hyrtl, 1845; Gray, 1907, 1908; Spoor, 1993), andcan help identify a fossil’s affiliation (Spoor, 1993;Spoor et al., 1994).

Hublin et al. (1996) found that in Neanderthalsthe arc sizes of the vertical (anterior and posterior)semicircular canals are smaller than in modernhumans and H. erectus, whereas its lateral canalis larger-arced. Moreover, the position of theposterior canal was described as markedly inferiorrelative to the plane of the lateral canal. It wasobserved that among great apes and a numberof hominin species the position and size of theposterior canal are correlated: the larger the canalthe more inferiorly it is positioned. However,Neanderthals do not follow this general trendbecause their posterior canal is inferiorly posi-tioned, but relatively small. Given that H. erectusis similar to modern humans in any of the traitsthat characterize the Neanderthal labyrinth(Spoor, 1993; Spoor and Zonneveld, 1994; Spooret al., 1994), Hublin et al. (1996) concluded that

the Neanderthal morphology is likely derived rela-tive to both H. erectus and modern humans.Subsequent studies of Neanderthal specimens haveestablished that Dederiyeh 93002 from Syria showsthe typical Neanderthal labyrinthine morphology(Spoor et al., 2003), whereas Le Moustier 1appears to have a morphology closer to that ofmodern humans (Thompson and Illerhaus, 1998;Ponce de Leon and Zollikofer, 1999).

Spoor and Zonneveld (1998) describe two keyinfluences on the morphology of the labyrinth thatlikely underlie differences between primate species.The arc size and planar orientation of the semi-circular canals are directly linked to their sensoryfunction of perceiving angular head motion,whereas other aspects of labyrinthine shape arecorrelated with cranial base morphology, such asthe degree of sagittal flexion. Apparently charac-terized by different canal arc sizes and an inferiorlypositioned posterior canal, the Neanderthal laby-rinth appears to show features related to bothfunction and cranial base morphology.

Expanding upon the initial findings of Hublinet al. (1996) this paper presents a more comprehen-sive comparative analysis of the Neanderthal bonylabyrinth. The full morphology of the structure isconsidered, the Neanderthal sample is increased,and preliminary comparisons are made withsmall samples of European Middle Pleistocenehominins, as well as early modern and EuropeanUpper Palaeolithic humans.

Materials and Methods

The sample investigated comprises 15Neanderthals, four European Upper Palaeolithicmodern humans, two early anatomically modernhumans, and three European Middle Pleistocenehominins (Table 1), as well as 54 Holocene humanswith a worldwide, geographically diverse origin(see Appendix 5.1 of Spoor, 1993). All specimensin the comparative sample are adult, but someNeanderthal specimens are immature. The lattercan be compared directly with the adult specimensbecause the bony labyrinth reaches adult size andshape well before birth (Bast, 1930; Spoor, 1993).The Neanderthals correlate with oxygen isotope

F. Spoor et al. / Journal of Human Evolution 44 (2003) 141–165142

stages 3 and 4, with the exception of Tabun C1which likely correlates with oxygen isotope stage 5or 6 (Grun and Stringer, 2000, but see Schwarczet al., 1998). The term “modern human”, whenused without any further qualification, refers to thecombined Holocene, Upper Palaeolithic and earlyanatomically modern human samples, or thepopulations they represent.

The bony labyrinths were visualized by com-puted tomography (CT), following the proceduresdescribed in Spoor and Zonneveld (1995). Thefollowing medical CT scanners were used: PhilipsTomoscan 310/350 (Holocene humans, Gibraltar2, Reilingen, Steinheim, Tabun C1), SiemensSomatom plus 4 (Gibraltar 1, Skhul 5, Spy 1 & 2),Toshiba Xvigor (Dederiyeh 93002), GeneralElectric Highspeed (all other specimens). The scanswere made in the sagittal plane, and in a transverseplane parallel with the arc of the lateral semi-circular canal. The slice thickness is 1.0 or 1.5 mmand the slice increment ranges from 0.5 to 1.5 mm.Images were reconstructed with a pixel size ofbetween 0.1 and 0.3 mm. One specimen, LeMoustier 1, was scanned with a nonmedical CTscanner, and its image dataset has an isotropicvoxel size of 0.1 mm (Thompson and Illerhaus,1998). One labyrinth of each specimen wasinvestigated, with the exception of three fossils of

which both sides were assessed (Table 1). In thelatter case measurements of the left and right sidewere averaged, noting that bilateral differences aresmall compared with inter-individual ones (Spoor,1993).

Measurements, taken from the digital images,are those used in Spoor and Zonneveld (1998), acomprehensive review of extant primate labyrin-thine morphology. They are shown in Figure 1,summarized in Table 2, and detailed definitions aregiven in Spoor and Zonneveld (1995). After reduc-tion of the pixel size through weighted inter-polation, linear measurements were taken to thenearest tenth of a millimeter, and angles to thenearest degree. For the CT images with the lowestresolution used in this study (Philips Tomoscan310/350), the maximum error of these measure-ments was established experimentally as �0.1 mmand �4 degrees, respectively (Spoor andZonneveld, 1995). The images with higher resolu-tions will have at least this accuracy and precision.

The linear measurements of the labyrinthinclude the height and width of the arc of eachsemicircular canal and of the basal turn of thecochlea [Figure 1(a),(b)]. The height of each canalarc is measured to the point furthest away from thevestibule (the vertex), and the width perpendicularto the height. The radius of curvature (R) of each

Table 1The fossil sample analyzed in this study

Neanderthals European UpperPalaeolithic

Early anatomicallymodern

European MiddlePleistocene

Dederiyeh 93002 (r; im) Abri Pataud 1 (r; ad) Qafzeh 6 (l; ad) Abri Suard (l; ad)Gibraltar 1 (r; ad) Abri Pataud 3 (l; im) Skhul 5 (r; ad) Reilingen (r; ad)Gibraltar 2 (l; im) Cro-Magnon 1 (r; ad) Steinheim (l,r; ad)La Chapelle-aux-Saints (l; ad) Laugerie Basse 1 (l; ad)La Ferrassie 1 (r; ad)La Ferrassie 2 (r, ad)La Ferrassie 3 (l,r; im)La Quina 5 (l; ad)La Quina H27 (r; ad)Le Moustier 1 (l,r; im)Pech de l’Aze 1 (l; im)Petit-Puymoyen 5 (r; ad)Spy 1 (r; ad)Spy 2 (r; ad)Tabun C1 (l; ad)

Abbreviations: l. left side; r. right side; ad. adult; im. immature.

F. Spoor et al. / Journal of Human Evolution 44 (2003) 141–165 143

canal arc and of the cochlear basal turn wascalculated by taking half the average of the heightand width measurements (0.5[h + w]/2).

Interspecifically, the size of the semicircularcanals and the cochlea correlates with body mass(Watts, 1924; Jones and Spells, 1963; Spoor andZonneveld, 1998). Ideally, this phenomenonshould be taken into account when comparing the

hominin groups, even though the increase of laby-rinth size with body mass is small (e.g., a Gorillalabyrinth is about 2.8 times larger than a Micro-cebus labyrinth), and body mass estimates for thefossil groups assessed here do not vary widely(Ruff et al., 1997). Cochlea size scales uniformlyamong extant primate species (Spoor andZonneveld, 1998), and the reduced major axis

Fig. 1. Superior (a), (c) and lateral (b), (d) aspects of a left human labyrinth, as reconstructed from transverse and sagittal CT scansrespectively, showing the measurements used in this study. Measurement abbreviations are listed in Table 2.


Table 2The abbreviations in alphabetical order of the measurements of the labyrinth and the petrous pyramid

Linear dimensions and their derivativesASCh Height of the anterior semicircular canal [Figure 1(b)].ASCw Width of the anterior semicircular canal [Figure 1(a)].COh Height of the basal turn of the cochlea [Figure 1(b)].COw Width of the basal turn of the cochlea [Figure 1(a)].h/w Shape index of the arc of a semicircular canal or of the basal turn of the cochlea (height/width �100)LSCh Height of the lateral semicircular canal [Figure 1(a)].LSCw Width of the lateral semicircular canal [Figure 1(a)].PSCh Height of the posterior semicircular canal [Figure 1(a)].PSCw Width of the posterior semicircular canal [Figure 1(b)].R Radius of curvature of a semicircular canal or the cochlear basal turn, measured to the centre of the lumen (R = 0.5�[height + width]/2)SLI The sagittal labyrinthine index, calculated from the dimensions SLIs and SLIi as SLIi/(SLIs + SLIi)�100 [Figure 1(b)]. Quantifies how the arc of the

posterior canal is positioned relative to the plane of the lateral canal (LSCm)

OrientationsAPA The ampullar line, connecting the centres of the anterior and posterior ampullae, and projected onto the sagittal plane [Figures 1(d), 7]. Reflects how the

vertical canals are set onto the vestibule in lateromedial view.ASCi The inferior most part of the anterior semicircular canal, defined by the line in the transverse plane connecting the apertures of the anterior ampulla and

the common crus into the vestibule [Figure 1(c)]. Labelled as “V” in Spoor and Zonneveld (1995)ASCm The arc of the anterior semicircular canal at its greatest width in the transverse plane [Figure 1(c)].ASCs The superior most part of the anterior semicircular canal in the transverse plane [Figure 1(c)].CCR The common crus in the sagittal plane [Figure 1(d)].COs The basal turn of the cochlea in the sagittal plane [Figure 1(d)].COt The basal turn of the cochlea in the transverse plane [Figure 1(c)].FC3 The third part of the facial canal in the sagittal plane [Figure 7].LSCI The lateral most part of the lateral semicircular canal in the sagittal plane [Figure 1(d)].LSCm The arc of the lateral semicircular canal at its greatest width in the sagittal plane [Figure 1(d), 7].LSCt The axis of symmetry of the lateral semicircular canal in transverse plane [Figure 1(c)].PPp The posterior petrosal surface in the sagittal plane at the level of the common crus [Figure 7].PSCi The inferior limb of the posterior semicircular canal in the transverse plane [Figure 1(c)].PSCm The arc of the posterior semicircular canal at its greatest width in the transverse plane [Figure 1(c)].PSCs The superior limb of the posterior semicircular canal in the transverse plane [Figure 1(c)].SG Intersection of the (mid)sagittal plane of the cranium in the transverse plane.VC The vestibulocochlear line, connecting the centre of the arc of the lateral semicircular canal and the lateral most point of the second cochlear turn,

projected onto the sagittal plane [Figure 1(d)]. Reflects the infero-superior position of the cochlea relative to the vestibule.VSC Reference line in the transverse plane based on the vertical semicircular canals. It bisects the angle between the arc orientations of these two canals that

opens anteriorly or posteriorly [ASCm, PSCm; Figure 1(c)].

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(RMA) regression is used here to correct for bodymass. Semicircular canal size, on the other hand,does not scale uniformly among primates (Spoorand Zonneveld, 1998). The regressions most ap-propriate to correct for body mass in the currentstudy are those for the extant great apes, as theseappear to represent the primitive condition forhominins (Spoor, 1996). However, based on justfour extant species the correlations of canal sizewith body mass do not reach statistical signifi-cance, and the possible impact of scaling on thecomparisons of the three canals is only consideredvisually on the basis of bivariate plots. Estimatedbody masses used follow Smith and Jungers (1997)for all extant primates, including Holocenehumans, and Ruff et al. (1997) for the UpperPalaeolithic and early modern humans andNeanderthals. For the European Middle Pleisto-cene a rough minimum estimate of 80 Kg was used(C. Ruff, personal communication).

In addition to the height and width measure-ments of the canals and the cochlea two furtherlinear measurements were taken to calculate thesagittal labyrinthine index (SLI). This indexexpresses the percentage of the posterior semi-circular canal that is located inferiorly to the levelof the lateral semicircular canal [Figure 1(b): SLIs,SLIi].

Angles were taken to quantify the spatialorientation of labyrinthine structures in relation toeach other and in relation to aspects of thecranium. All orientations are defined in the trans-verse or sagittal plane [Figure 1(c),(d)], and anglescalculated between two such orientations aretherefore projected onto either of these planes.Angles are indicated by the abbreviations ofthe two orientations on which they are based,separated by the “<” symbol. For example,“CCR<LSCm” is the angle between the commoncrus and the lateral canal in the sagittal plane[Figure 1(d): Table 2].

Two aspects of each of the three semicircularcanals are quantified using angles, the degree oftorsion, and the planar orientation. The arc of asemicircular canal is rarely entirely planar; rather itis nearly always somewhat twisted, showing adegree of torsion. Here the torsion of the anteriorand posterior canals is quantified as the difference

between the orientations of their superior-mostand inferior-most parts [Figure 1(c): ASCs<ASCi;PSCs<PSCi], and that of the lateral canal as thedifference between orientations of the lateral-mostpart and at the greatest arc width [Figure 1(d):LSCl<LSCm]. The planar orientation of eachcanal is approximated by measuring the arc at itswidest part, for the vertical semicircular canals inthe transverse plane [Figure 1(c): ASCm, PSCm],and for the lateral canal in the sagittal plane[Figure 1(d): LSCm]. These three canal orienta-tions constitute the most stable, i.e., least variable,feature of the labyrinth among extant primatespecies, most likely because they reflect the func-tionally important physiological plane of optimumperceptive sensitivity (Spoor and Zonneveld,1998). They are, therefore, used as reference orien-tations in the comparison of more diverse aspectsof labyrinthine shape. The measurements of theanterior and posterior canals in the transverseplane are combined into a single reference orienta-tion by taking the line that bisects the anglebetween the two canal orientations [Figure 1(c):VSC, the bisector of the angle ASCm<PSCmopening anteriorly and posteriorly]. Other aspectsof the labyrinth of which the orientation ismeasured are the axis of symmetry of the lateralcanal, the common crus, the ampullar line, and thecochlea [Figure 1, Table 2: LSCt, CCR, APA,COt, COs and VC, respectively].

The labyrinth is well preserved in all fossilsincluded in this study. The only postmortemdamage concerns the inferoposterior part of theposterior semicircular canal of Tabun Cl. Theplanar orientation (PSCm) and height (PSCh)of this canal can nevertheless be estimated onthe basis of the preserved bone. However, theorientation of the inferior limb of this canal (PSCi)cannot be measured and the torsion (PSCtor) cantherefore not be calculated.

Angles involving structures other than thelabyrinth itself were considered for adult speci-mens only. The planar orientations of the anteriorand posterior semicircular canals to the cranialmidsagittal plane (ASCm<SG; PSCm<SG) areobviously not available for isolated temporalbones, and neither could they be measured for Spy1, Spy 2 and Cro-Magnon 1 because the required


transverse overview images were not available.Spoor and Zonneveld (1998) assess the planarorientation of the lateral semicircular canal relativeto aspects of the midline cranial base. However,these basicranial parts are not preserved in theexamined Neanderthal specimens other thanGibraltar 1, and such angles are thus not con-sidered here. The lateral canal is, however, com-pared relative to the orientations of the posteriorsurface of the petrous pyramid (PPp) and the thirdpart of the facial canal (FC3). Both are defined inSpoor and Zonneveld (1995), and schematicallyshown in Figure 7.

Differences between the means of the fivehominin groups were compared using ANOVAand t-tests. Bonferroni adjustments for multi-plicity were made using the sequential proceduredescribed in Rice (1989). Both the protected (i.e.,Bonferroni adjusted) and unprotected probabilitiesare given. In reporting the quantitative analysesthe emphasis is on the comparisons between

Neanderthals and Holocene humans. For the pre-liminary comparisons involving the other threehominin groups only significant differences ofmeans will be highlighted, as nonsignificance caneasily reflect the small sample sizes rather thansimilarity.

Descriptions and comparisons

CT-based three-dimensional reconstructions ofthe bony labyrinths of two Neanderthal specimensand a representative Holocene human are shownin Figure 2. Furthermore, CT slices throughthe arcs of the three semicircular canals of aHolocene human and a Neanderthal are shown inFigure 3.

The absolute and relative radii of curvature ofthe semicircular canals are given in Table 3 (R and%R). The statistical significance of the differencebetween sample means is indicated. Neanderthals

Fig. 2. Lateral (a)–(c) and superior (d)–(f) aspects of the right bony labyrinths of a Holocene human (a), (d), and the Neanderthalspecimens Gibraltar 1 (b), (e) and Petit Puymoyen 5 (c), (f), reconstructed from sagittal CT scans. The lateral views are alignedaccording to the plane of the lateral semicircular canal. S. superior, A, anterior, and L, lateral. Scale bar is 5 mm.


have absolutely and relatively smaller vertical(anterior and posterior) canal arcs, and a largerlateral canal arc than Holocene humans. In thesefeatures they are closest to the Middle Pleistocenehominins. The Upper Palaeolithic and earlymodern humans have larger anterior, and theformer relatively smaller lateral canals thanNeanderthals. Compared with Holocene humansboth have an absolutely and relatively largerlateral canal, and a relatively smaller posteriorcanal.

Figure 4 plots the mean canal arc radii againstestimated body mass for the hominin groups anda sample of extant primates. The plots of theanterior and posterior canals show the grouping ofNeanderthals and Middle Pleistocene hominins onthe one hand, and Holocene, Upper Palaeo-lithic and early modern humans on the other[Figure 4(a),(b)]. The former are larger-bodied, buthave smaller canals than the latter. Thus, correct-ing for body mass will increase the differencesbetween the two groupings observed for absoluteanterior and posterior canal radii. The Neander-thals and Middle Pleistocene hominins fall close tothe assumed great ape regression, whereas the

Holocene, Upper Palaeolithic and early modernhumans fall well above it, and thus have largervertical canals for their body mass. In the plot forthe lateral canal the hominins form a cluster justbelow and mostly parallel with the assumed greatape regression. This pattern suggests that differ-ences in lateral canal radius between the hominingroups largely follow from differences in bodymass, but the exact extent cannot be establishedowing to the uncertain slope of the great aperegression. Particularly the size difference betweenthe lateral canals of early modern and Holocenehumans could be more than the effect of size alone.

The indices expressing the arc shape of the threesemicircular canals are given in Table 4 (h/w). Theshape of the anterior canal of both Neanderthalsand the Middle Pleistocene hominins is relativelynarrow in width compared with Holocene andearly modern humans. The relatively greater widthof the anterior canal arc in Holocene humanscorresponds with a morphology where the ampullabulges out laterally, whereas it points more superi-orly in Neanderthals [Figure 3(a),(d)]. The UpperPalaeolithic sample mean for the shape index ofthe anterior canal is close to that of the Holocenehumans, but statistically not significantly differentfrom that of the Neanderthals. The average arcshape of the posterior canal of Neanderthals isclose to circular (i.e., shape index = 100), whereasit is taller than it is wide in Holocene and UpperPalaeolithic humans [Figure 3(b),(e)]. Given theorientations of the heights and widths of theanterior and posterior canals (Figure 1) theseresults imply that in Neanderthals the arc shape ofboth anterior and posterior canals is foreshortenedanteroposteriorly when compared with Holocenehumans. The arc shapes of the lateral canal are notsignificantly different (Table 4).

The anterior semicircular canal of Neanderthalsand the Middle Pleistocene hominins shows moretorsion, and the Upper Palaeolithic humans lesstorsion than Holocene humans (Table 4: ASCtor).The torsion of the posterior canal is similar inNeanderthals and Holocene humans, but the Up-per Palaeolithic sample shows more torsion thanHolocene humans (Table 4: PSCtor). The degreesof torsion of the lateral canal are not significantlydifferent (Table 4: LSCtor).

Fig. 3. CT slices through the arcs of the posterior (a), (d),anterior (b), (e) and lateral (c), (f) semicircular canals of aHolocene human (a)–(c) and the Neanderthal specimen PetitPuymoyen 5 (d)–(f). Scale bar is 5 mm. Notice that the moreirregular appearance of the Petit Puymoyen canals is theconsequence of the presence of matrix in parts of their lumen.


Table 3The radii of curvature to the centre of the lumen (R) of the semicircular canals (ASC, PSC, LSC) given in millimeters, and therelative radii of the semicircular canals in percent (%R: sum of the three radii is 100%)

ASC-R PSC-R LSC-R ASC %R PSC %R LSC %R

Dederiyeh 3.2 3.0 2.7 36 33 30Gibraltar 1 2.7 2.8 2.5 34 35 31Gibraltar 2 3.2 3.0 2.6 36 34 30La Chapelle aux Saints 3.0 2.9 2.5 36 34 30La Ferrassie 1 3.3 2.6 2.6 39 30 31La Ferrassie 2 2.9 2.7 2.7 35 33 32La Ferrassie 3 2.9 2.5 2.3 38 32 30La Quina 5 3.2 3.1 2.9 35 34 31La Quina H27 3.0 3.0 2.7 35 35 31Le Moustier 1 3.4 3.4 2.7 36 36 28Pech de l’Aze 3.0 2.9 2.8 35 33 32Petit Puymoyen 5 2.9 2.8 2.7 35 33 32Spy 1 3.3 3.2 2.8 35 34 30Spy 2 2.9 3.0 2.5 34 36 30Tabun C1 2.7 2.5 2.4 35 33 31

Abri Pataud 1 3.2 2.8 2.4 39 33 28Abri Pataud 3 3.4 3.1 2.7 37 34 29Cro Magnon 1 3.1 3.0 2.5 36 35 29Laugerie Basse 1 3.4 3.3 2.5 37 36 27

Qafzeh 6 3.6 3.1 2.8 38 33 29Skhul 5 3.2 3.1 2.6 36 35 29

Abri Suard 2.9 2.7 2.3 37 34 29Reilingen 3.1 2.7 2.6 37 32 31Steinheim 2.8 2.7 2.4 35 35 31

Holocene (54)Mean 3.22 3.15 2.26 37.3 36.5 26.2Range 2.6/4.0 2.3/3.9 1.9/2.8 34/41 32/40 23/31S.D. 0.25 0.30 0.21 1.29 1.82 1.85

Upper Palaeolithic (4)Mean 3.27 3.05 2.51 37.1 34.5 28.4S.D. 0.13 0.23 0.12 1.1 1.2 1.0

Early modern (2)Mean 3.43 3.12 2.70 37.1 33.7 29.2S.D. 0.27 0.01 0.14 1.2 1.4 0.2

Neanderthals (15)Mean 3.02 2.88 2.61 35.5 33.8 30.7S.D. 0.22 0.25 0.16 1.3 1.4 1.1

Middle Pleistocene (3)Mean 2.93 2.72 2.45 36.2 33.6 30.2S.D. 0.19 0.02 0.16 1.1 1.3 1.0

ANOVA x xx xxx xxx xxx xxxt-test:Neanderthal—Holocene xx xx xxx xxx xxx xxxNeanderthal—Upper Palaeolithic x ns ns ns ns xxNeanderthal—early modern x ns ns ns ns nsNeanderthal—Middle Pleistocene ns x ns ns ns nsUpper Palaeolithic—Holocene ns ns x ns x xEarly modern—Holocene ns ns xx ns x xMiddle Pleistocene—Holocene ns xxx ns ns xx xxx

The statistical significance of the difference between the means is indicated by x: P<0.05, xx: P<0.01 and xxx: P<0.001.Bonferroni adjusted (’protected’) probabilities are underlined.


The planar orientations of the anterior andposterior semicircular canals in the cranium, i.e.,relative to the midsagittal plane, are not differentin Neanderthals and the other hominins for whichthese angles could be measured (Table 5:ASCm<SG, PSCm<SG). This could be the resultof the small sample sizes of the fossil groups forwhich these measurements are available. However,similarity is supported by the observation that theangle between the planar orientations of the twocanals, which could be measured for all specimensconsidered, shows no significant differences either(Table 6: ASCm<PSCm). The angle between theplanar orientation of the lateral canal and theposterior petrosal surface is larger in Neanderthalsthan in Holocene humans (Table 5: LSCm<PPp).Likewise, the angle between this canal’s orienta-tion and the third portion of the facial canal islarger in Neanderthals than in Holocene andUpper Palaeolithic humans (Table 5: LSCm<FC3). This means that in Neanderthals theposterior petrosal surface and the facial canalportion are oriented more upright relative to theplane of the lateral canal.

Neither the angle between the axis of symmetryof the lateral canal arc and the vertical canalorientations, nor that between the common crusand the lateral canal orientation are significantlydifferent between the groups (Table 6: LSCt<VSC,CCR<LSCm, respectively). On the other hand, theampullar line is more vertically inclined relative tothe lateral canal orientation in Neanderthals thanin any of the other groups, whereas it is lessvertically inclined in early modern humans than inHolocene humans (Table 6: APA<LSCm). More-over, the arc of the posterior canal is positionedmore inferiorly, relative to the lateral canal inNeanderthals than in all other groups, whereas it ispositioned more superiorly in Upper Palaeolithichumans than in Holocene humans (Table 6: SLI).As a consequence of this morphology the commoncrus of Neanderthals tends to be unusuallyshort compared with Holocene humans, and anyother extant primate species investigated thus far[Figure 2(a)–(c)].

Figure 5(a) demonstrates the interspecific corre-lation among hominid species between the position(SLI) and size (R) of the posterior canal; the

Fig. 4. Bivariate double logarithmic plots between estimatedbody mass and the radii of curvature to the centre of the lumenof (a) the anterior semicircular canal (ASC-R), (b). the pos-terior canal (PSC-R) and (c) the lateral canal (LSC-R). N.Neanderthals, H. Holocene modern humans, U. EuropeanUpper Palaeolithic humans, M, European Middle Pleistocenehominins, o. great apes, +. other extant primate species. Dataof extant species after Spoor and Zonneveld (1998). The bodymass of fossil hominins follows Ruff et al. (1997), and that ofother species Smith and Jungers (1997). The reduced major axisregressions for the great ape species are indicated, but thecorrelations are not statistically significant (rrank = 0.800,P > 0.05, for all three canals).


Table 4The shape indices (h/w�100) and torsions (tor) of the semicircular canals (ASC, PSC, LSC)

ASCh/w PSCh/w LSCh/w ASCtor* PSCtor† LSCtor‡

Dederiyeh 103 107 93 15 �4 1Gibraltar 1 95 93 85 25 �11 10Gibraltar 2 85 100 84 19 �7 �1La Chapelle aux Saints 88 99 85 32 �6 8La Ferrassie 1 93 92 91 25 �23 1La Ferrassie 2 97 98 91 22 �15 �3La Ferrassie 3 101 87 94 21 �9 12La Quina 5 87 108 93 29 �12 11La Quina H27 94 111 100 27 �8 8Le Moustier 1 84 98 83 26 �16 11Pech de l’Aze 89 93 88 15 �21 2Petit Puymoyen 5 93 93 89 25 �10 �6Spy 1 97 108 104 23 �10 3Spy 2 100 109 94 15 �12 5Tabun C1 102 98 84 17 � 4

Abri Pataud 1 84 106 92 12 �17 5Abri Pataud 3 96 118 93 12 �13 8Cro Magnon 1 80 118 91 13 �17 7Laugerie Basse 1 93 102 96 12 �21 1

Qafzeh 6 91 105 87 23 �14 2Skhul 5 72 88 82 10 �4 0

Abri Suard 98 96 84 24 �12 �2Reilingen 95 132 91 24 �13 2Steinheim 90 109 87 24 �8 1

Holocene (54)Mean 87.3 107.2 88.5 16.1 �9.1 3.8Range 74/97 94/128 67/100 5/28 �22/0 �7/14S.D. 4.69 7.57 6.57 5.3 4.5 4.3

Upper Palaeolithic (4)Mean 88.1 110.7 92.8 12.3 �17.0 5.2S.D. 7.4 8.4 2.4 0.5 3.3 3.3

Early modern (2)Mean 81.3 96.5 84.6 16.5 �9.0 0.8S.D. 13.5 11.9 3.0 9.2 7.1 1.1

Neanderthals (15§)Mean 93.8 99.6 90.6 22.4 �11.8 4.3S.D. 6.2 7.3 6.0 5.4 5.4 5.6

Middle Pleistocene (3)Mean 94.4 112.3 87.1 24.0 �11.0 0.1S.D. 4.4 18.1 3.5 0.5 2.4 1.9

ANOVA xxx xx ns xx x nst-test:Neanderthal—Holocene xxx xxx ns xxx ns nsNeanderthal—Upper Palaeolithic ns x ns xxx ns nsNeanderthal—early modern x ns ns ns ns nsNeanderthal—Middle Pleistocene ns ns ns ns ns nsUpper Palaeolithic— Holocene ns ns ns xxx xx nsEarly modern—Holocene ns ns ns ns ns nsMiddle Pleistocene—Holocene x ns ns xxx ns ns

Statistical significance as indicated in the caption of Table 3.*ASCs<ASCi; positive when ASCs is more coronally oriented than ASCi.†PSCs<PSCi; positive when PSCs is more sagitally oriented than PSCi.‡LSCl<LSCm; positive when LSCl is more inclined than LSCm.§PSCtor based on 14 specimens.


Table 5Angles in degrees describing the planar orientation of the semicircular canals in the cranium

ASCm<SG PSCm<SG LSCm<PPp LSCm<FC3

Gibraltar 1 38 144 70 96La Chapelle aux Saints 37 150 73 102La Ferrassie 1 30 144 82 86La Ferrassie 2 — — 71 82La Quina 5 28 136 66 91La Quina H27 — — 74 104Petit Puymoyen 5 — — 61 93Spy 1 — — 61 85Spy 2 — — 70 81Tabun C1 — — 62 —

Abri Pataud 1 39 150 80 77Cro Magnon 1 — — 55 79Laugerie Basse 1 — — 54 72

Qafzeh 6 33 142 64 85Skhul 5 37 144 65 86

Abri Suard — — 67 85Reilingen 34 146 64 92Steinheim 29 145 54 74

Holocene (50,50,53,52)Mean 35.8 139.1 61.0 77.2Range 26/47 129/150 42/80 58/90S.D. 4.9 5.4 8.0 6.8

Upper Palaeolithic (3)Mean — — 62.9 75.9S.D. — — 14.9 3.8

Early modern (2)Mean 35.0 143.0 64.3 85.3S.D. 2.8 1.4 1.1 1.1

Neanderthals (4,4,10,9)Mean 33.2 143.4 68.9 91.0S.D. 5.0 5.7 6.7 8.2

Middle Pleistocene (3)Mean 31.1 145.7 61.6 83.5S.D. 3.4 0.9 7.0 9.1

ANOVA ns ns x xxxt-test:Neanderthal—Holocene ns ns xx xxxNeanderthal—Upper Palaeolithic — — ns xNeanderthal—early modern ns ns ns nsNeanderthal—Middle Pleistocene ns ns ns nsUpper Palaeolithic—Holocene — — ns nsEarly modern—Holocene ns ns ns nsMiddle Pleistocene—Holocene ns ns ns ns

Explanation of the measurement codes and symbols in Figure 1 and Table 2.The first two angles open anteriorly, the other two antero-superiorly. Statistical significance as indicated in Table 3.


Table 6Angles in degrees and index (SLI) in per cent of the semicircular canals

ASCm<PSCm LSCt<VSC CCR<LSCm APA<LSCm SLI

Dederiyeh 115 108 127 45 65Gibraltar 1 106 102 117 53 76Gibraltar 2 114 113 120 50 74La Chapelle aux Saints 113 108 118 42 60La Ferrassie 1 114 108 124 40 65La Ferrassie 2 103 119 111 46 65La Ferrassie 3 101 100 118 53 61La Quina 5 108 114 124 45 63La Quina H27 105 106 117 52 68Le Moustier 1 107 108 112 40 55Pech de l’Aze 98 120 124 50 68Petit Puymoyen 5 91 119 127 41 65Spy 1 103 110 122 42 53Spy 2 110 119 120 49 61Tabun C1 101 120 121 51 69

Abri Pataud 1 111 125 129 42 54Abri Pataud 3 98 104 120 36 39Cro Magnon 1 112 103 122 35 41Laugerie Basse 1 92 109 120 33 33

Qafzeh 6 109 103 120 36 47Skhul 5 107 114 113 29 40

Abri Suard 99 102 109 40 51Reilingen 113 103 133 39 60Steinheim 113 114 117 33 40

Holocene (54)Mean 103.6 112.3 121.0 40.6 51.0Range 90/112 101/125 113/133 32/57 34/69S.D. 5.2 5.1 3.9 4.7 7.0

Upper Palaeolithic (4)Mean 103.2 110.2 122.5 36.6 41.6S.D. 9.9 9.9 4.1 3.6 8.9

Early modern (2)Mean 108.0 108.0 116.3 32.2 43.6S.D. 1.4 7.8 4.6 4.9 4.8

Neanderthals (15)Mean 105.9 111.5 120.0 46.7 64.7S.D. 6.8 6.7 4.8 4.7 6.0

Middle Pleistocene (3)Mean 108.1 106.1 119.6 37.1 50.4S.D. 7.9 6.7 12.0 3.9 9.9

ANOVA ns ns ns xxx xxxt-test:Neanderthal—Holocene ns ns ns xxx xxxNeanderthal—Upper Palaeolithic ns ns ns xxx xxxNeanderthal—early modern ns ns ns xxx xxxNeanderthal—Middle Pleistocene ns ns ns xx xxUpper Palaeolithic—Holocene ns ns ns ns xEarly modern—Holocene ns ns ns x nsMiddle Pleistocene—Holocene ns x ns ns ns

Explanation of the measurement codes and symbols in Figure 1 and Table 2. The first two angles open laterally; the other twoantero-superiorly. Statistical significance as indicated in Table 3.


larger the canal the more inferior its position. Theposterior canal in Neanderthals has a moreinferior position (higher SLI) for its size thanpredicted by the regression (Table 7). Likewise, thecanal of Middle Pleistocene hominins has a some-what more inferior position than predicted. Incontrast, that of the Upper Palaeolithic andearly modern humans is positioned slightly moresuperiorly (lower SLI) than predicted. However,the deviations from the general hominid regressionshown by the latter three groups are small com-pared to the degree of inter-individual variationamong Holocene humans and Neanderthals[Figure 5(b)]. Among individuals of each of thesetwo groups posterior canal size and position arenot correlated (P > 0.05; rrank 0.025 and �0.470,respectively). The bivariate plot of Figure 5(b)shows a good separation of Neanderthals andHolocene humans, but there is a degree of overlap,with Le Moustier 1 and Spy 1 falling well within

Fig. 5. The relationship between the radius of curvature of the posterior semicircular canal (PSC-R, in millimeters) and theSagittal Labyrinthine Index (SLI, in percentages). (a) Mean values of N, Neanderthals; H, Holocene modern humans; U, UpperPalaeolithic modern humans; E, early modern humans; M, Middle Pleistocene hominins; �, H. erectus (OH 9, Sangiran 2, Sangiran4); Australopithecus africanus (Taung, Sts 5, Sts 19, MLD 37/38); Paranthropus robustus (SK 46, SK 47, SK 879); Dryopithecusbrancoi (RUD 77); Pan troglodytes (n = 7); Pan paniscus (n = 6); Gorilla gorilla (n = 6) and Pongo pygmaeus (n = 7). The RMAregression (y = 23.59��22.91) is given for the sample excluding Neanderthals, Upper Palaeolithic and early modern humans,and Middle Pleistocene hominins (rrank = 0.917, P<0.001). (b) Mean values N and H as in (a) and specimen values ofo, Neanderthals; +, Holocene modern humans; x, Upper Palaeolithic modern humans; #, early modern humans and , MiddlePleistocene hominins.

Table 7Values of the sagittal labyrinthine index (SLI) and thecochlear basal turn size (CO-R) as predicted by posteriorcanal size (PSC-R) and body mass, respectively, using theRMA regressions shown in Figures 5 and 7

Xi Ypred SE L1 L2 Yobs

SLI (%) predicted from PSC-R (mm)Holocene 3.15 51.4 1.3 48.3 54.5 51.0Upper Palaeolithic 3.05 49.0 1.5 45.5 52.5 41.6Early Modern 3.12 50.6 1.9 46.1 55.1 43.6Neanderthals 2.88 44.9 0.9 42.7 47.2 64.7Middle Pleistocene 2.72 41.3 1.4 38.0 44.6 50.4

CO-R (mm) predicted from body mass (g)Holocene 58313 2.12 1.03 1.99 2.26 2.26Upper Palaeolithic 66400 2.16 1.05 1.94 2.41 2.41Early Modern 66600 2.16 1.07 1.87 2.50 2.61Neanderthals 76000 2.20 1.04 2.04 2.38 2.27Middle Pleistocene 80000 2.22 1.06 1.96 2.51 2.24

The standard error (SE) and 95% confidence interval(L1, L2) of the predicted value (Ypred) are given. Observedvalues (Yobs) outside the confidence interval are given inbold.


the Holocene human range. The two Holocenehuman specimens that fall within the coreNeanderthal range (i.e., excluding Le Moustier 1and Spy 1) originate from Central Asia (Kalmuck)and Mozambique.

The size of the cochlear basal turn ofNeanderthals is not different from that inHolocene humans, whereas that of early modernhumans, and to a lesser extent that of UpperPalaeolithic humans is larger (Table 8: CO-R).When taking body mass into account, by calculat-ing the residuals from the extant primate regres-sion, Holocene and Upper Palaeolithic humansare not significantly different in cochlea size,whereas the latter do have a larger cochlea thanNeanderthals (Figure 6; Table 8). Only the cochleaof the early modern humans is larger than pre-dicted by body mass on the basis of the extantprimate regression (Table 7).

No significant differences are observed for theshape index and orientation in the transverse planeof the cochlear basal turn (Table 8: COh/w,COt<VSC, respectively). The position and orien-tation of the cochlea, relative to the plane of thelateral canal, is not different in Neanderthals andHolocene humans (Table 8: VC<LSCm, COs<LSCm, respectively). On the other hand, bothearly modern and Upper Palaeolithic humans havea more superiorly positioned cochlea thanHolocene humans (Table 8: VC<LSCm), and theapex of the cochlea faces more inferiorly in MiddlePleistocene hominins than in Neanderthals andHolocene humans (Table 8: COs<LSCm).

In summary, compared with Holocene humansthe bony labyrinth of Neanderthals can becharacterized as follows.

• The anterior semicircular canal arc is smallerin absolute and relative size, is narrow inwidth compared to its height, and shows moretorsion.

• The posterior semicircular canal arc is smallerin absolute and relative size, is less high relativeto its width, and is positioned more inferiorlyrelative to the lateral canal plane.

• The lateral semicircular canal arc is absolutelyand relatively larger.

• The ampullar line is more vertically inclined.

The European Upper Palaeolithic and earlymodern humans are most similar, although notfully identical to Holocene humans in labyrinthinemorphology. The European Middle Pleistocenehominins show the typical semicircular canal mor-phology of Neanderthals, with the exception of thearc shape and inferiorly position of the posteriorcanal and the strongly inclined ampullar line.

Whereas sample means of individual traitsdiffer significantly between modern humans andNeanderthals, their ranges largely overlap. In fact,among the discriminating traits all Neanderthalspecimens fall within the Holocene human rangefor ASC-R, PSC-R, ASC-%R, LSC<PPp andAPA<LSCm. La Chapelle aux Saints, and LaQuina H27 are only outside the Holocene rangefor the angle describing the facial canal orientation(FC3<LSCm), which is not a character of thelabyrinth itself. Spy 1 is only outside the range forthe shape index of the lateral canal (LSCh/w),a character that does not discriminate betweenNeanderthals and Holocene humans. Of allNeanderthals examined the labyrinth of LeMoustier 1 is the closest in morphology to that ofHolocene humans, falling within the latter’s rangefor all traits. Among Neanderthals it has therelatively smallest lateral canal (LSC-%R), thelowest anterior canal arc (ASCh/w), the leastvertically inclined ampullar line (APA<LSCm),and almost the lowest sagittal labyrinthine index(SLI). In contrast, the La Ferrassie 1 labyrinthshows three traits outside the Holocene range, thatare all related to its posterior canal (PSC-%R,PSCh/w, PSCtor). The labyrinths of La Quina 5,Pech de 1’Aze and Petit Puymoyen each show twotraits outside Holocene range.

Discussion

The results of the present study confirm theinitial findings of Hublin et al. (1996) that the bonylabyrinth of Neanderthals is distinct in morphol-ogy from that of Holocene and Late Pleistocenemodern humans. The increase of the Neanderthalsample, from nine in Hublin et al. (1996) to 15here, has not led to changes in the mean values ofthe canal radii, other than an increase from 2.5 to


Table 8Linear dimensions and angles of the cochlea

CO-R residual COh/w COt<VSC VC<LSCm COs<LSCm

Dederiyeh 2.3 131 110 146 54Gibraltar 1 2.5 123 121 154 68Gibraltar 2 2.1 150 111 140 70La Chapelle aux Saints 2.3 133 107 156 52La Ferrassie 1 2.4 138 107 152 53La Ferrassie 2 2.4 141 114 143 64La Ferrassie 3 2.2 154 122 155 46La Quina 5 2.2 154 121 166 60La Quina H27 2.2 134 116 148 60Le Moustier 1 2.5 127 121 144 54Pech de l’Aze 2.3 140 111 148 59Petit Puymoyen 5 2.5 123 107 167 64Spy 1 2.2 128 113 150 58Spy 2 2.2 123 119 145 61Tabun C1 2.0 122 124 149 59

Abri Pataud 1 2.3 131 125 158 59Abri Pataud 3 2.4 155 109 161 60Cro Magnon 1 2.6 140 109 166 52Laugerie Basse 1 2.4 144 111 158 54

Qafzeh 6 2.5 120 112 156 57Skhul 5 2.7 139 116 165 58

Abri Suard 2.3 145 119 144 47Reilingen 2.3 122 125 142 54Steinheim 2.1 145 120 147 43

Holocene (54)Mean 2.26 0.13 136.6 116.3 150.9 59.4Range 2.0/2.6 118/156 106/127 140/170 46/69S.D. 0.13 8.6 5.0 6.1 5.2

Upper Palaeolithic (4)Mean 2.41 0.24 142.3 113.4 160.8 56.2S.D. 0.13 10.2 7.4 3.6 3.7

Early modern (2)Mean 2.61 0.45 129.1 113.5 160.4 57.3S.D. 0.12 13.5 2.8 5.9 1.1

Neanderthals (15)Mean 2.27 0.07 134.8 114.7 150.8 58.7S.D. 0.14 11.3 6.1 7.8 6.3

Middle Pleistocene (3)Mean 2.24 0.02 137.2 121.3 144.2 48.2S.D. 0.11 13.2 3.4 2.7 5.6

ANOVA xx — ns ns xx xt-test:Neanderthal—Holocene ns ns ns ns ns nsNeanderthal—Upper Palaeolithic ns x ns ns x nsNeanderthal—early modern xx xx ns ns ns nsNeanderthal—Middle Pleistocene ns ns ns ns ns xUpper Palaeolithic—Holocene x ns ns ns xx nsEarly modern—Holocene xxx xx ns ns x nsMiddle Pleistocene—Holocene ns ns ns ns ns xxx

Explanation of the measurement codes and symbols in Figure 1 and Table 2. The first angle opens antero-laterally; the othertwo antero-superiorly. Statistical significance as indicated in Table 3.


2.6 mm for the lateral canal. Furthermore, themean value of the sagittal labyrinthine index (SLI)has changed from 68 to 65. Importantly, thepresent, more comprehensive comparative analysishas identified a number of additional traits thatdistinguish the labyrinths of the two hominingroups.

The labyrinth of only one Neanderthal, LeMoustier 1, has been examined quantitatively instudies other than Hublin et al. (1996). Thompsonand Illerhaus (1998) report anterior, posterior andlateral canal radii of 3.2, 3.3 and 2.6 mm, and anSLI of 64 for its right labyrinth. These values differfrom those obtained for the right labyrinth in thisstudy (3.4, 3.4, 2.7 mm and 55, respectively), eventhough they are based on the same CT images. Thediscrepancies appear to follow from the differentways in which the measurements were taken.Thompson and Illerhaus (1998) used 3D recon-structions derived from the CT images, similar tothose shown in Figure 2, rather than the cross-sectional images themselves [J. Thompson per-sonal communication; assistance was given by oneof us (FS)]. Most landmarks involved are locatedin the centre of the lumen of the canals (Figure 1;

Spoor and Zonneveld, 1995), and these have to beestimated from the surface contours when takingmeasurements from 3D images. In practice, it isparticularly difficult to estimate the planar orien-tation of the lateral canal, as defined in Spoor andZonneveld (1995: LSCm), whereas this is essentialto obtain compatible SLI values. Ponce de Leonand Zollikofer (1999) also measured 3D recon-structions of the labyrinths of Le Moustier 1, butbased on CT images different from the ones usedhere. The values of 3.4 mm for the posterior canalradius and 54 for the SLI, plotted in their Figure7B, are very close to those obtained here (3.4 mmand 55). Unlike Thompson and Illerhaus (1998),however, Ponce de Leon and Zollikofer displayedthe 3D reconstructions on a stereo screen (C.Zollikofer personal communication), and theadded perception of depth undoubtedly improvedtheir ability to accurately locate the internallandmarks.

The identification of an expanded suite of laby-rinthine traits characterizing Neanderthals under-lines the potential of using this structure to assessthe phylogenetic affinities of fragmentary LatePleistocene hominin fossils. That the labyrinth

Fig. 6. Bivariate double logarithmic plots between estimated body mass and the radii of curvature to the basal turn of the cochlea(CO-R). Symbols as in Figure 4. Sample of 25 extant primate species as in Spoor and Zonneveld, 1998, plus Galago moholi. Solid lineis the reduced major axis regression for the extant primates (rrank 0.878, P<0.001), RMA slope 0.139, intercept. �0.335).


reaches adult morphology well before birth notonly has the practical advantage that adult andimmature specimens can be compared directly.Given its unusual ontogeny the bony labyrinth

may also reflect the genotypic make-up of anindividual to a greater degree than do most otherskeletal parts because postnatal influences on themorphology by environmental or behavioralfactors are minimal or absent. On the other hand,the present study highlights that each of theidentified traits shows considerable overlapbetween modern humans and Neanderthals.Consequently, statistically conclusive attributionswill almost always require multivariate analyses, asexemplified by studies of the Arcy sur Cure andDederiyeh labyrinths (Hublin et al., 1996; Spooret al., 2003). Moreover, conclusive attribution willbe impossible when dealing with labyrinths similarto that of Le Moustier 1, which entirely fall in themorphological overlap zone of Neanderthals andmodern humans.

Shape of the labyrinth

The most striking aspect of the Neanderthallabyrinth, as yet not found in any other homi-noid species (Spoor, 1993; Spoor and Zonneveld,1998), is the particularly inferior position of itsposterior semicircular canal. Individual traits thatare associated with this morphology are not onlythe high SLI value, but also the more verticallyinclined ampullar line (APA<LSCm), which fol-lows from the inferiorly positioned posteriorampulla, and the unusually shortened commoncrus (Figure 2). Moreover, a particularly inferiorposition of the ampullar limb of the posteriorcanal is spatially consistent with a relatively largearc width, and thus the lower shape index seen inNeanderthals (PSCh/w). Among extant primatespecies the SLI and the ampullar line angle arecorrelated, and both are also correlated with theorientation of the posterior petrosal surface andthe third part of the facial canal (Spoor, 1993;Spoor and Zonneveld, 1998). These correlationsimply that a more inferiorly positioned posteriorcanal arc corresponds with a more verticallyinclined ampullar line, posterior petrosal surfaceand facial canal. When viewing the lateral aspectof the left temporal bone and labyrinth thismorphology can be seen as a joint clockwiserotation, relative to both the plane of the lateralsemicircular canal (LSCm) and the midlineanterior cranial base (Spoor and Zonneveld,

Fig. 7. Lateral view of the left bony labyrinths of (a) Panpaniscus, (b) a Holocene modern human and (c) the La Ferassie1 Neanderthal. The labyrinths are aligned according to theplanes of their lateral semicircular canal (LSCm; dashed line),and the course of the second and third parts of the facial nervecanal (thick line) and the endocranial petrosal contour at thelevel of the common crus are indicated. Single headed arrowsindicate morphological differences comparing (b) to (a), and (c)to (b). The ampullar line (APA, thick dotted line), the third partof the facial nerve canal (FC3) and the posterior petrosalsurface (PPp) are increasingly vertically inclined from (a) to (c),and the inferior component of the sagittal labyrinthine indexincreases (SLIi, double headed arrows). Neanderthals andHolocene humans are similar in having a common crus that istilted posteriorly (CCR), and a cochlea that is positioned moresuperiorly (COs and VC) than in nonhominin primates.


1998). Modern humans follow the interspecificprimate trend, and are characterized by a particu-larly rotated morphology [Figure 7(a),(b)]. TheNeanderthal posterior canal, petrosal surface andfacial canal also follow this trend, and show whatcan best be described as a hyper-rotated mor-phology [Figure 7(c)]. The anterior canal mor-phology of Neanderthals, marked by strongertorsion and a higher arc shape than that ofmodern humans, is not correlated with thiscomplex of characters.

The inferior position of the posterior canal inNeanderthals is unlikely to affect the function ofsensing head rotations because it is the orientationof a canal, not its position, that determines thephysiological plane of optimum perceptive sensi-tivity. In Neanderthals the planar orientation ofboth the posterior and the anterior canal, either inthe cranium, or relative to each other, does notdiffer from that in the other hominins (Table 5:PSCm<SG, Table 6: ASCm<PSCm). This findingis consistent with the observation that amongextant primates the planar orientation of all threecanals is functionally constrained, and shows littleinterspecific variation (Spoor and Zonneveld,1998). The degree of torsion and the arc shape doinfluence a canal’s response behaviour to someextent (Blanks et al., 1985; McVean, 1999), but itis unclear whether the differences between theanterior canals of Neanderthals and modernhumans has any significant functional impact.

The rotated morphology of the labyrinth andsurrounding petrous pyramid in modern humanshas been linked with the phylogenetic impact ofthe enlarged brain on the human basicranium, inparticular through mechanisms involving thetentorium cerebelli attachment to the superiorpetrosal margin and spatial demands of thecerebellum in the posterior cranial fossa (Spoor,1997; Spoor and Zonneveld, 1998). In thislight, factors underlying the uniquely rotatedNeanderthal morphology may well be found inaspects of its platycephalic brain shape. However,comparisons of Neanderthal and modern humanendocast morphology largely focus on overall vol-ume and cerebral features (Holloway, 1981, 1985;Trinkaus and LeMay, 1982), whereas a detailedcomparative assessment of the posterior cranial

fossa and cerebellar morphologies would berequired in the present context.

Semicircular canals and locomotion

The second important character complex thatdistinguishes the Neanderthal and modern humanlabyrinths is the arc size of the semicircular canals.The larger lateral canal arc in Neanderthals appearto be mainly the consequence of their greater bodymass [Figure 4(c)], and it is particularly theirsmaller vertical, i.e., anterior and posterior canalsthat will be considered further. Previous studies ofhominin semicircular canal size have arguedthat enlargement of the vertical canals in modernhumans and H. erectus, relative to the great apesand South African australopiths should be seen asa functional adaptation to a locomotor repertoirethat includes habitual bipedal running andjumping (Spoor et al., 1994, 1996; Spoor andZonneveld, 1998). The underlying reasoning is thatarc enlargement of these canals, and thus of theenclosed, functionally important membranousducts, results in increased mechanical sensitivityand the improved ability to resolve the smallchanges in fast vertical head rotations that charac-terize modern human bipedal running on a natural(i.e., irregular) substrate. This provides a moreaccurate input into the vestibular reflexes, which,together with visual and proprioceptive input, playan important role in maintaining body coordina-tion (see Spoor and Zonneveld, 1998; Spoor, 2003for a more detailed review). It should be empha-sized that the functional interpretation of homininsemicircular canal morphology does not relate toissues of body posture or bipedalism as generallocomotor mode. What canal arc sizes appear torelate to in extant primates, and in mammals andbirds in general, is the overall agility of locomo-tion, and the requirement for fast and accuratecoordination of locomotor movements (Spoor,2003).

If the proposed link between enlarged verticalcanals and agile bipedal running in hominins iscorrect, this would suggest that Neanderthals andMiddle Pleistocene hominins, both with canal sizesmore similar to the primitive hominin condition,had locomotor repertoires marked by significantly


less running and general agility than modernhumans or H. erectus. This controversial sugges-tion raises the question whether the functionalmorphology of the Neanderthal postcranialskeleton provides any evidence that these homininsdid indeed have a different locomotor behaviourthan modern humans. Neanderthals are character-ized by a large body mass and overall robusticity,as well as relatively short limbs, in particular thedistal segments (Trinkaus, 1981, 1983; Ruff, 1994;Ruff et al., 1997). Considered within the context ofhow modern human body build tends to correlatewith different athletic capabilities, these propertiesappear generally less compatible with locomotoragility and speed. This could thus be seen as anindication that, on the whole, Neanderthals wereendurance “walkers” rather than “runners”.

More specifically, significant differences havebeen demonstrated between the anatomy of thecoxal bone and lower limb of Neanderthalsand modern humans. Both Neanderthals andMiddle Pleistocene hominins display a particularlywide pelvis with a typically long upper pubicramus (Trinkaus, 1983; Rak, 1990; Ruff, 1991;Rosenberg, 1998; Arsuaga et al., 1999). Thismorphology has been associated with wide, coldadapted bodies (Ruff, 1991; 1994), whereas othershave interpreted it as the plesiomorphic conditionfor the genus Homo (Rak, 1993; Rosenberg, 1998;Arsuaga et al., 1999; Marchal, 2000). Importantly,it has been recognized that this pelvic morphologycould point at certain locomotor differencesbetween Neanderthals and modern humans (Rak,1991, 1993; Rosenberg, 1998). However, it seemsunlikely that such differences would be reflected inthe size of the vertical semicircular canals, giventhat later H. erectus appears to be most similar toNeanderthal and Middle Pleistocene hominins incoxal morphology (Arsuaga et al., 1999; Marchal,2000), but shares large canals with modernhumans.

Neanderthal femora have long been recognizedas morphologically distinct from those of modernhumans (e.g., Boule, 1911–13; Trinkaus, 1983).Using, among others, analyses of diaphyseal cross-sectional geometry, these differences have beeninterpreted in terms of general robusticity, habitualloading regimes and locomotor mobility levels

(Trinkaus, 1983, 1997). A problem with interpret-ing such analyses in relation to types of locomotorbehaviour is that the results can reflect differentcombinations of rates and duration of locomotionand burden carrying (Trinkaus, 1997; Trinkausand Ruff, 1999). Perhaps some indication ofdifferences in gait preference and the degree ofmaneuverability follows from the observationthat the Neanderthal femoral diaphysis appearsenlarged mediolaterally, in contrast with antero-posterior reinforcement observed in modernhumans (Trinkaus et al., 1998; Trinkaus and Ruff,1999). The somewhat distinct directional patternsin biomechanical loading levels, suggested by thesemorphologies, could reflect different use of thelower limb, but may also result from the dissimilarpelvic proportions, affecting bending momentson the femur shaft (Trinkaus and Ruff, 1999).In sum, current skeletal evidence suggests thatNeanderthals could have displayed differences intheir gait when compared to modern humans, butneither the degree nor the nature of such differ-ences is clear beyond a plausible link betweenoverall robustness and reduced locomotor agility.

Two less well-studied aspects of Neanderthalbody build that may be important to understandtheir semicircular canal system are the kinematiccharacteristics of the neck and head (Spoor andWood, 1999). The neck passively converts loco-motor movements of the body into involuntaryhead motions, and its elastic properties can thusinfluence the input signal of the canal system.On the other hand, the canals supply the neckmusculature through the vestibulo-collic reflex,stabilizing the head by compensatory neck move-ments. As a feedback system this keeps the inputsignal of the canals within limits, and contributesto the stabilization of gaze during locomotion (thelatter particularly aided by the vestibulo-ocularreflex working on the extra-ocular muscles). Theshape of the head, including the position of itscentre of gravity, is another important factor thataffects head stabilization during running (Bramble,2000), and thus interacts with semicircular canalfunction. The complex interplay between the mor-phology of the head and neck and the semicircularcanal system is poorly understood. Further inves-tigation is warranted, given that Neanderthals may


have had bulkier neck proportions than modernhumans, which could well have affected passivehead-on-trunk motion. For example, the cervicalsegment forms a relatively short 16% of the totalspine length of the Kebara 2 skeleton, whereas amean value of 22% was obtained for modernhumans (Arensburg, 1991). Likewise, the cervicallength of the Shanidar Neanderthals has beendescribed as short, although within the rangeof modern human variation (Trinkaus, 1983).Contrasting with this shortish neck length,Neanderthals had relatively long and horizontalspinous processes of the lower cervical vertebrae(Trinkaus, 1983), broad shoulders, as indicated bytheir long clavicles (Trinkaus, 1981, 1983), and awell-developed nuchal surface area associated withtheir typical occipital morphology (Trinkaus andLeMay, 1982). Moreover, Neanderthals havelonger neurocrania and more projecting faces thanmodern humans, which could affect head stabiliz-ation during running, although the same holds truefor H. erectus, a species with modern human-likecanal sizes.

In the end, the key question is whether differ-ences in locomotion and kinematic propertiesof the head and neck, as envisaged betweenrobustly built Neanderthals and Middle Pleisto-cene hominins on the one hand, and more gracileH. erectus and modern humans on the other, are ofa nature that has the potential to affect the semi-circular canal system. Any answer will require abetter idea of how locomotor diversity and canalmorphology are associated, and will have to come

from detailed comparative morphological andkinematic studies of living primates and othermammals.

Given that Neanderthals are considered cold-adapted, showing the closest similarity in bodyshape to Holocene populations living in coldclimates (Trinkaus, 1981; Ruff, 1994; Holliday,1997; Holliday, 2000), it is worth consideringwhether climate is a factor that affects semicircularcanal size, and the bony labyrinth in general. TheHolocene human sample of this study includesfive specimens from regions with a cold climate(indigenous people of Lapland, Greenland,Siberia, and Labrador). These specimens are notsignificantly different from the subsample of 21specimens that originates in tropical regions forany of the labyrinthine characters that distinguishbetween Neanderthals and modern humans(Table 9). Hence, the evidence suggests that cli-mate does not constitute a major factor affectingthe morphology of the labyrinth. However, larger,more specific Holocene samples would have to beassessed to detect more subtle climatic influences,either directly or, more likely, via differencesin body proportions that affect locomotion andhead-trunk motion.

Phylogenetic considerations

Phylogenetic interpretation of the morphologyof the Neanderthal labyrinth requires an under-standing of the polarity of the characters involved.When using the extant great apes and South

Table 9Comparison of subgroups of the Holocene sample, originating from cold and warm climate region (5 and 21 specimens,respectively). Labyrinthine characters are those that distinguish Neanderthals and modern humans

ASC-R PSC-R LSC-R ASC %R PSC %R LSC %R ASC h/w PSCh/w ASCtor APA<LSCm SLI

Cold*

Mean 3.15 3.14 2.32 36.6 36.4 27.0 86.3 108.0 18.7 39.3 49.1S.D. 0.18 0.35 0.12 0.8 2.7 2.2 5.1 7.4 1.6 4.7 4.2

Warm†

Mean 3.25 3.12 2.27 37.6 36.1 26.3 87.4 106.0 16.5 40.7 51.9S.D. 0.27 0.28 0.20 1.3 1.6 1.8 4.8 6.4 6.0 5.8 8.2

Differences between the means are not significant (P > 0.05).*Indigenous people of Lapland, Greenland, Siberia and two of Labrador.†Indigenous people of African, Asian and American regions between the tropics of Cancer and Capricorn.


African australopiths as outgroups (Spoor, 1993;Spoor et al., 1994; Spoor and Zonneveld, 1998), asmall arc size of the anterior and posterior semi-circular canals appears to represent the primitivehominin condition, whereas both a high-arcedanterior canal with strong torsion and the charac-ter complex associated with the inferiorly posi-tioned posterior canal are derived. However, acloser related, more appropriate outgroup for thehominins investigated in the present study is H.erectus. The labyrinth of this species, as repre-sented by Sangiran 2 and 4 and Olduvai Hominid9, is not significantly different from that ofHolocene humans (Spoor, 1993; Spoor andZonneveld, 1994; Spoor et al., 1994; Hublin et al.,1996). Based on the assumption that H. erectus isancestral to all later forms of the genus Homo,Hublin et al. (1996) concluded that all character-istic features of the Neanderthal labyrinth arederived. This would not necessarily be the casewhen using a phylogenetic model in which someor all later representatives of Homo descendedexclusively from early African forms of H. erectus(H. ergaster to some), of which the labyrinthinemorphology is as yet unknown. Nevertheless, thatthe Neanderthal character complex associated withthe inferior position of the posterior semicircularcanal is indeed derived is strongly supported byits absence in the European Middle Pleistocenehominins that are widely seen as exclusivelyancestral to Neanderthals. Confirmation thatthe other Neanderthal characters, shared bythe European Middle Pleistocene hominins, arederived as well awaits the examination of earlyAfrican H. erectus fossils. The European MiddlePleistocene hominins show a more inferiorly facingcochlea (Table 8: COs<LSCm) than Neanderthals,as well as modern humans and H. erectus (Spoor,1993; sample as above). Using the extant greatapes and South African australopiths as outgroups(Spoor, 1993; Spoor and Zonneveld, 1998) thisappears to be a primitive feature, but here too,further evidence on early African H. erectus formsis needed to confirm the polarity within the genusHomo.

The Neanderthal sample investigated hereshows no indication of major temporal or geo-graphic variation in the morphology of the laby-

rinth. For example, Tabun C1, an early westernAsian representative (Grun and Stringer, 2000),has a labyrinth expressing the typical Neanderthalcharacteristics as strongly as younger specimensfrom western and southern Europe (but seeSchwarcz et al., 1998 for an alternative date, whichwould make Tabun C1 contemporary with the restof the Neanderthal sample). Younger than42,000 BP (Mellars and Grun, 1991) and possiblythan 37,000 BP (Valladas et al., 1986) Le Moustier1 is perhaps the youngest Mousterian Neanderthalin the sample, living at the time when thefirst modern humans migrated into Europe. Itsatypical, and more modern human labyrinthinemorphology could thus be viewed as a sign of geneflow between Neanderthals and modern migrants.However, neither the overall cranial morphology(Thompson and Bilsborough, 1996; Ponce de Leonand Zollikofer, 1999) nor the Mousterian archaeo-logical context of the specimen (Bourgon, 1957;Mellars, 1996; Thompson and Bilsborough, 1996)suggests cultural or biological interaction. Rather,the Le Moustier 1 labyrinth is consistent with therest of the Neanderthal sample as a more extremeform of their normal range of variation. In thisrespect it is worth noting that even where there ispossible evidence for cultural interaction, in theChatelperronian layers of Arcy sur Cure, the laby-rinth of the associated fossil hominin temporalbone shows typical Neanderthal morphology(Hublin et al., 1996).

With respect to geographical variation theNeanderthal pattern of stasis is similar to thatobserved for the Holocene sample, which showsfew differences between different regions (Spoor,1993), none of which concern the traits consideredhere. In contrast, comparisons of the Holocenehumans with the small European Upper Palaeo-lithic and early modern samples suggest that thereis temporal variation in modern human labyrin-thine morphology. One interesting observationthat warrants further investigation is that in bothearly modern and Upper Palaeolithic humans thecochlea is positioned more superiorly than inHolocene humans (Table 8: VC<LSCm), a featurewith uncertain polarity within the genus Homo(Spoor, 1993). More important here is that earlymodern or Upper Palaeolithic humans do not


take an intermediate position between Holocenehumans and Neanderthals for the features thatdiffer among the three groups of modern humans,and characterize Neanderthals (Table 4: ASCtor;Table 6: APA<LSCm, SLI; Table 7, Figure 5:relationship PSC-R and SLI). In fact, in labyrin-thine morphology the early modern and EuropeanUpper Palaeolithic humans are more differentfrom the Neanderthals than the Holocene humansare. Hence, like analyses of body shape (Holliday,2000), the present study does not provide evidencefor admixture between the early modern Skhul/Qafzeh populations and Neanderthals in theLevant (Kramer et al., 2001). The Upper Palaeo-lithic sample studied here is less appropriate forconsidering the possibility of admixture inEurope, because of its temporal distance to the lastNeanderthal populations. Instead, assessment ofthe bony labyrinths of the Mladec and StettenVogelherd specimens would be of interest in thisrespect. It should, however, be remembered thatsmall Neanderthal contributions to modernhuman genetic variation, and vice versa, may wellnot be reflected in the labyrinthine morphology.

In sum, the derived bony labyrinth ofNeanderthals has its best ancestor in the morphol-ogy of European Middle Pleistocene hominins,and further insights into its origin will requirestudy of Pleistocene hominins from Europe andAfrica. The Holocene modern human morphol-ogy, on the other hand, can be traced back to bothAsian and African representatives of H. erectus viathe Upper Palaeolithic and early modern Skhul-Qafzeh populations, as well as the Singa specimenfrom Sudan (Spoor et al., 1998). Examination ofearly African H. erectus is of particular importanceto further clarify its origins. Moreover, the smallbut significant temporal variation of the modernhuman labyrinth indicates that a more comprehen-sive study of this phenomenon may well contributeto a better understanding of the relationshipsbetween Holocene and Late Pleistocene humanpopulations worldwide.

Acknowledgements

We are grateful to A. Langaney (Musee del’Homme Paris), H. de Lumley (Institut de

Paleontologie Humaine), R. Orban (InstitutRoyal des Sciences naturelles de Belgique), C. B.Stringer (Natural History Museum London), B.Vandermeersch (Universite Bordeaux 1) and R.Ziegler (Staatliches Museum fur Naturkunde inStuttgart) for permission to CT scan homininfossils in their care, and to B. Illerhaus, O. Kondoand J. Thompson for sharing CT images. Wethank S. Condemi, C. Dean, J. DePonte, T.Harrison, K. H. Hohne, N. Jeffery, R. Kruszynski,K. Kupczik, D. Lieberman, J. Moore, D.Plummer, A. Pommert, J. Thompson, C.Zollikofer and an anonymous referee for help.This research was supported by the Royal Society(London), the UCL Graduate School, the Chairede Paleoanthropologie du College de France,GDR 2152 of CNRS and Philips Medical Systems.

References

Arensburg, B., 1991. The vertebral column, thoracic cageand hyoid bone, in: Bar Yosef, O., Vandermeersch, B.(Eds.), Le squelette Mousterien de Kebara 2. Ed. CNRS,Paris, pp. 125–146.

Arsuaga, J.L., Lorenzo, C., Carretero, J.M., Gracia, A.,Martınez, I., Garcıa, N., Bermudez de Castro, J.M.,Carbonell, E., 1999. A complete human pelvis from theMiddle Pleistocene of Spain. Nature 399, 255–258.

Bast, T.H., 1930. Ossification of the otic capsule in humanfetuses. Contr. Embryol. 21, 55–82.

Blanks, R.H.I., Curthoys, I.S., Bennett, M.L., Markham, C.H.,1985. Planar relationship of the semicircular canals inrhesus and squirrel monkeys. Brain Research 340, 315–324.

Boule, M., 1913. L’homme fossile de La Chapelle-aux-Saints.Ann. Paleont. 6, 111–172. 7, 21–56, 85–192, 8, 1–70.

Bourgon, M., 1957. Les industries mousteriennes etpremousteriennes du Perigord. Arch. Inst. Paleontol.Humaine 27, 1–141.

Bramble, D.M., 2000. Head stabilization in human running:implications for hominid evolution. Am. J. Phys. Anthrop.30(Suppl), 111.

Condemi, S., 1988. Caracteres plesiomorphes et apomorphesde l’os temporal des neanderthaliens EuropeensWurmiens, in: Otte, M. (Ed.), l’Homme de Neandertal 3,l’anatomie, pp. 49–52.

Delattre, A., Fenart, R., Empereur-Buisson, R., 1967.Orientation vestibulaire de cranes de neanderthaliens parmethode radiographique. J. Sc. Med. Lille 85, 219–222.

Fenart, R., Empereur-Buisson, R., 1970. Application de lamethode “vestibulaire” d’orientation au crane de l’enfantdu Pech-de-l’Aze et comparaison avec d’autres cranesneandertaliens. Arch. Inst. Paleont. Hum. 33, 89–104.


Grun, R., Stringer, C., 2000. Tabun revisited: revised ESRchronology and new ESR and U-series analyses of dentalmaterial from Tabun C1. J. Hum. Evol. 39, 601–612.

Holliday, T., 1997. Postcranial evidence of cold adaptation inEuropean Neandertals. Am. J. Phys. Anthrop. 104,245–258.

Holliday, T., 2000. Evolution at the crossroads: modernhuman emergence in western Asia. Am. Anthrop. 102,54–68.

Holloway, R.L., 1981. Volumetric and asymmetry determina-tions on recent hominid endocasts: Spy I and II, DjebelIhroud I, and the Sale Homo erectus specimens, with somenotes on Neandertal brain size. Am. J. Phys. Anthrop. 55,385–393.

Holloway, R.L., 1985. The poor brain of Homo sapiens nean-derthalensis: see what you please, in: Delson, E. (Ed.),Ancestors: The Hard Evidence. Alan Liss, New York, pp.319–324.

Hublin, J.J., 1978. Quelques caracteres apomorphes du craneneandertalien et leur interpretation phylogenetique. C. R.Acad. Sci., Paris. D287, 923–926.

Hublin, J.J., Spoor, F., Braun, M., Zonneveld, F., Condemi, S.,1996. A late Neanderthal from Arcy-sur-Cure associatedwith Upper Palaeolithic artefacts. Nature 381, 224–226.

Hyrtl, J., 1845. Vergleichend-anatomische UntersuchungenUber das innere Gehororgan des Menschen und derSaugethiere. F. Ehrlich, Prague.

Jones, G.M., Spells, K.E., 1963. A theoretical and comparativestudy of the functional dependence of the semicircular canalupon its physical dimensions. Proc. Roy. Soc., Lond. B157,403–419.

Kindler, W., 1960. Roentgenologische Studien ueberStirnhoehlen und Warzenfortsaetze beim klassischenNeandertaler im mitteleuropaeischen Raum. Z. Laryng.Rhin. Otol. 39, 411–424.

Kindler, W., Kiefer, R., 1963. Roentgenologische Studien ueberStirnhoehlen und Warzenfortsaetze beim Neandertaler immitteleuropaeischen Raum (II. Teil). Z. Laryng. Rhin. Otol.42, 752–767.

Kramer, A., Crummett, T.L., Wolpoff, M.H., 2001. Out ofAfrica and into the Levant: replacement or admixture inWestern Asia? Quatern. Int. 75, 51–63.

Marchal, F., 2000. A new morphometric analysis of thehominid pelvic bone. J. Hum. Evol. 38, 347–365.

McVean, A., 1999. Are the semicircular canals of the Europeanmole, Talpa europaea, adapted to a subterranean habitat?Comp. Biochem. Physiol. A123, 173–178.

Mellars, P., 1996. The Neanderthal Legacy. PrincetonUniversity Press, Princeton.

Mellars, P., Grun, R., 1991. A comparison of the electron spinresonance and thermoluminescense dating methods: theresults of ESR dating at Le Moustier (France). CambridgeArchaeol. J. 1, 269–276.

Ponce de Leon, M.S., Zollikofer, C.P.E., 1999. New evidencefrom Le Moustier 1: computer-assisted reconstruction andmorphometry of the skull. Anat. Rec. 254, 474–489.

Rak, Y., 1990. On the differences between two pelvises ofMousterian context from the Qafzeh and Kebara caves,Israel. Am. J. Phys. Anthrop. 81, 323–332.

Rak, Y., 1993. Morphological variation in Homo neandertha-lensis and Homo sapiens in the Levant. A biogeographicmodel, in: Kimbel, W.H., Martin, L.B. (Eds.), Species,Species Concepts, and Primate Evolution. Plenum Press,New York, pp. 523–536.

Rice, W.R., 1989. Analyzing tables of statistical tests.Evolution 43, 223–225.

Rosenberg, K.R., 1998. Morphological variation in West Asianpostcrania. Implications for obstetric and locomotorbehavior, in: Akazawa, T., Aoki, K., Bar-Yosef, O. (Eds.),Neandertals and Modern Humans in Western Asia. PlenumPress, New York, pp. 367–379.

Ruff, C.B., 1991. Climate and body shape in hominid evolution.J. Hum. Evol. 21, 81–105.

Ruff, C.B., 1994. Morphological adaptation to climate inmodern and fossil hominids. Yearb. Phys. Anthrop. 37,65–107.

Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body massand encephalization in Pleistocene Homo. Supplementaryinformation to. Nature 387, 173–176.

Santa Luca, A.P., 1978. A re-examination of presumedNeanderthal-like fossils. J. Hum. Evol. 7, 619–636.

Schwarcz, H.P., Simpson, J.J., Stringer, C.B., 1998. Neander-thal skeleton from Tabun: U-series data by gamma-rayspectrometry. J. Hum. Evol. 35, 635–645.

Silipo, P., Dazzi, M., Feliciani, M., Guglielmi, G., Guidetti, G.,Martini, S., Massani, D., Mori, S., Tanfani, G., 1991.Computerized tomographic analysis of the Neandertalcranium of the Guattari Cave, in: Piperno, M., Sachilone,G. (Eds.), The Circeo 1 Neandertal Skull, Studies andDocumentation. Libreria dello Stato, Italia, Rome, pp.513–538.

Smith, R.L., Jungers, W.L., 1997. Body mass in comparativeprimatology. J. Hum. Evol. 32, 532–559.

Spoor, C.F., 1993. The comparative morphology and phylo-geny of the human bony labyrinth. Ph.D. dissertation,Utrecht University.

Spoor, C.F., Zonneveld, F.W., 1994. The bony labyrinth inHomo erectus, a preliminary report. Cour. Forschungsinst.Senckenberg 171, 251–256.

Spoor, F., 1996. The ancestral morphology of the hominidbony labyrinth; the evidence from Dryopithecus. Am. J.Phys. Anthrop. 22(Suppl), 219.

Spoor, F., 2003. The semicircular canal system and locomotorbehaviour, with special reference to hominin evolution.Cour. Forschungsinst. Senckenberg. (in press).

Spoor, F., Hublin, J.J., Kondo, O., 2003. The bony labyrinth ofthe Dederiyeh child, in: Akazawa, T., Muhesen, S. (Eds.),Neanderthal Burials. Excavations of the DederiyehCave, Afrin, Syria. The Tokyo University Press, Tokyo (inpress).

Spoor, F., Stringer, C., Zonneveld, F., 1998. Rare temporalbone pathology of the Singa calvaria from Sudan. Am. J.Phys. Anthrop. 107, 41–50.


Spoor, F., Wood, B., Zonneveld, F., 1994. Implications of earlyhominid labyrinthine morphology for the evolution ofhuman bipedal locomotion. Nature 369, 645–648.

Spoor, F., Wood, B., Zonneveld, F., 1996. Evidence for a linkbetween human semicircular canal size and bipedalbehaviour. J. Hum. Evol. 30, 183–187.

Spoor, F., Wood, W., 1999. Neck proportions in modernhumans and Neanderthals. Am. J. Phys. Anthrop.28(Suppl), 256.

Spoor, F., Zonneveld, F., 1995. Morphometry of the primatebony labyrinth: a new method based on high resolutioncomputed tomography. J. Anat. 186, 271–286.

Spoor, F., Zonneveld, F., 1998. A comparative review of thehuman bony labyrinth. Yearb. Phys. Anthrop. 41, 211–251.

Thompson, J.L., Bilsborough, A., 1996. Time for one of the lastNeanderthals. Proc. of the XIII UISPP Congress (Forli,Italy) 2, 289–298.

Thompson, J.L., Illerhaus, B., 1998. A new reconstructionof the Le Moustier 1 skull and investigation of internalstructures using CT data. J. Hum. Evol. 35, 647–665.

Trinkaus, E., 1981. Neanderthal limb proportions and coldadaptation, in: Stringer, C.B. (Ed.), Symposia of the Societyfor the Study of Human Biology vol 21, Aspects of HumanEvolution. Taylor & Francis, London, pp. 187–224.

Trinkaus, E., 1983. The Shanidar Neandertals. Academic Press,New York.

Trinkaus, E., 1997. Appendicular robusticity and the paleo-biology of modern human emergence. Proc. Nat. Acad. Sci.94, 13367–13373.

Trinkaus, E., LeMay, M., 1982. Occipital bunning among laterPleistocene hominids. Am. J. Phys. Anthrop. 57, 27–35.

Trinkaus, E., Ruff, C.B., 1999. Diaphyseal cross-sectionalgeometry of Near Eastern Middle Paleolithic humans: thefemur. J. Archaeol. Sci. 26, 409–424.

Trinkaus, E., Ruff, C.B., Churchill, S.E., Vandermeersch, B.,1998. Locomotion and body proportions of the Saint-Cesaire 1 Chatelperronian Neandertal. Proc. Nat. Acad. SciUSA 95, 5836–5840.

Valladas, H., Geneste, J.-M., Joron, J.-L., Chadelle, J.-P., 1986.Thermoluminescense dating of Le Moustier (Dordogne,France). Nature 322, 452–454.

Vallois, H.V., 1969. L’os temporal des Neandertaliens. C. R.Ass. Anat. 144, 1710–1716.

Watts, H.J., 1924. Dimensions of the labyrinth correlated.Proc. Roy. Soc. Lond. B96, 334–338.

Wind, J., Zonneveld, F.W., 1985. Radiology of fossil hominidskulls, in: Tobias, P.V. (Ed.), Hominid Evolution, Past,Present and Future. Alan Liss, New York, pp. 437–442.

Zollikofer, C.P.E., Ponce de Leon, M.S., Martin, R.D., Stucki,P., 1995. Neanderthal computer skulls. Nature 375,283–285.

Zonneveld, F.W., Wind, J., 1985. High-resolution computedtomography of fossil hominid skulls: a new method andsome results, in: Tobias, P.V. (Ed.), Hominid Evolution,Past, Present and Future. Alan Liss, New York, pp.427–436.


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