Journal of Human Evolution xxx (2014) 1e8

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Journal of Human Evolution

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Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy
Stefano Benazzi a, b, *, Shara E. Bailey b, c, Marco Peresani d, Marcello A. Mannino b, Matteo Romandini d, Michael P. Richards b, e, Jean-Jacques Hublin b
a

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121 Ravenna, Italy Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany Center for the Study of Human Origins, Department of Anthropology, New York University, 25 Waverly Place, New York, NY 10003, USA d Sezione di Scienze Preistoriche e Antropologiche, Dipartimento di Studi Umanistici, Universit di Ferrara, Corso Ercole I dEste 32, I-44100 Ferrara, Italy e Department of Anthropology, University of British Columbia, Vancouver, British Columbia, V6T 1Z1 Canada
b c

a r t i c l e i n f o
Article history: Received 16 December 2013 Accepted 3 March 2014 Available online xxx Keywords: Deciduous teeth Homo neanderthalensis Homo sapiens Late Pleistocene Southern Europe

a b s t r a c t
The site of Fumane Cave (western Lessini Mountains, Italy) contains a stratigraphic sequence spanning the Middle to early Upper Paleolithic. During excavations from 1989 to 2011, four human teeth were unearthed from the Mousterian (Fumane 1, 4, 5) and Uluzzian (Fumane 6) levels of the cave. In this contribution, we provide the rst morphological description and morphometric analysis of the dental remains. All of the human remains, except for Fumane 6, are deciduous teeth. Based on metric data (crown and cervical outline analysis, and lateral enamel thickness) and non-metric dental traits (e.g., mid-trigonid crest), Fumane 1 (lower left second deciduous molar) clearly belongs to a Neandertal. For Fumane 4 (upper right central deciduous incisor), the taxonomic attribution is difcult due to heavy incisal wear. Some morphological features observed in Fumane 5 (lower right lateral deciduous incisor), coupled with the large size of the tooth, support Neandertal afnity. Fumane 6, a fragment of a permanent molar, does not show any morphological features useful for taxonomic discrimination. The human teeth from Fumane Cave increase the sample of Italian fossil remains, and emphasize the need to develop new methods to extract meaningful taxonomic information from deciduous and worn teeth. 2014 Elsevier Ltd. All rights reserved.

Introduction Fumane Cave is located at the foot of the Venetian Pre-Alps in the western Lessini Mountains (Fig. 1). The cave is part of a fossil karst system and comprises a large entrance in which three tunnels, A, B and C, converge (Supplementary Online Material [SOM] Figs. S1, S2). Excavations over the last two decades yielded a stratigraphic sequence spanning the late Middle to early Upper Paleolithic (sealed by thick slope waste and rockfall deposits), from which ve human dental remains were discovered. In this contribution, we present the rst detailed morphological description and morphometric comparison of the four human teeth (Fumane 1, 4, 5 (all deciduous) and Fumane 6) unearthed from the Mousterian and Uluzzian levels of the cave (Table 1). Since human remains dating to the late Middle Paleolithic are extremely scarce in Italy, these ndings have the potential to further clarify the evolutionary history of Neandertals. The fth human deciduous tooth (Fumane 2),
* Corresponding author. E-mail address: stefano_benazzi@eva.mpg.de (S. Benazzi). http://dx.doi.org/10.1016/j.jhevol.2014.03.001 0047-2484/ 2014 Elsevier Ltd. All rights reserved.

discovered in the Proto-Aurignacian deposit, is currently under investigation and its description will be part of a forthcoming contribution. Archaeological context The uppermost Mousterian deposits of Fumane Cave consist of numerous thin to very thin parallel levels and lenses grouped into nine stratigraphic units, labeled from bottom to top as A13 to A5 (Peresani et al., 2008) (SOM Fig. S1). Except A13 and A12, which are composed of at angular stones embedded in yellow sands and silts, the other units consist of frost-shattered slabs with variable sand content and aeolian dust. Units A13, A12 and A7 are archaeologically sterile. Nevertheless, A12 contains portions of the overlying anthropogenic unit A11, displaced by post-depositional deformations. Unit A11 is, in fact, composed of loamy dark-brown sediment with stones associated with abundant lithic artifacts and faunal remains. Above, unit A10 yielded anthropogenic lenses embedded in various levels of stones resulting from frostshattering.

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

S. Benazzi et al. / Journal of Human Evolution xxx (2014) 1e8

Figure 1. Geographical position of Fumane Cave (western Lessini Mountains, Italy).

Unit A9 comprises several layers showing a succession of dark, anthropogenic thin levels alternating with loose, stone-supported layers or thin sandy levels. Unit A7 separates A9 from A6, which consists of dark sediment with a high content of anthropogenic remains. Unit A5 is composed of loose stones with a loamy ne fraction and fewer archaeological remains than A6. Lithic artifacts from the Middle Paleolithic sequence (Peresani, 2012) belong to the Levallois Mousterian in the lowermost unit (A11). Lithics in units A6eA5 belong to the Levallois Mousterian but also include sporadic artifacts attributed to other aking methods (Peresani et al., 2013a). Sandwiched between layers A11 and A6, the set of levels of unit A10 has been attributed to the Levallois and discoid reduction sequences, either alternating or coexisting in the

same level, while the discoid technology becomes exclusive in A9 (Peresani, 2012). Analysis of the faunal remains shows that red deer, roe deer, ibex, chamois and giant deer were the most frequently hunted species (Fiore et al., 2004; Peresani et al., 2011a; Romandini et al., in press). In addition, remains of brown bear (Ursus) and fox (Vulpes) showing traces of exploitation are found in A6 and A5. The large and varied avifauna from these same units reveals unusual human modications on species that are not clearly related to consumption or utilitarian purposes (Peresani et al., 2011b). The Upper Paleolithic sequence includes six stratigraphic units labeled from bottom to top as A4 to A1, D6 and D3, where A4 and A3 are Uluzzian, and A2, A1 up to D3 are Proto-Aurignacian (Broglio et al., 2005). The bottom units A4 and A3 consist of frost-

Table 1 Inventory of human dental remains from Fumane Cave. Inventory no. Fumane Fumane Fumane Fumane
a b c d e

Tooth class Lower left second deciduous molar (Ldm2) Upper right central deciduous incisor (Rdi1) Lower right lateral deciduous incisor (Rdi2) Molar fragment

MD 9.9 6.1 5.5

BL 9.4 5.4 5.1

Wear stagea 5/6 5 5 5

Estimated ageb-e 10/11 years 6 years 6 years

Stratigraphic unit A11 A9 I A9 A3 I

Deposit Mousterian Mousterian Mousterian Uluzzian/Proto-Aurignacian

1 4 5 6

Molnar (1971). Moorrees et al. (1963). Ubelaker (1978). AlQahtani et al. (2010). Shackelford et al. (2012).

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

S. Benazzi et al. / Journal of Human Evolution xxx (2014) 1e8

shattered slabs with variable sand content and aeolian dust that becomes more prevalent toward the outermost part of the cave. In addition to numerous lithic artifacts and bones, dwelling structures with hearths and a refuse area were identied during the 2005e 2006 eldwork season (Peresani, 2008). Faunal remains from units A4 and A3 reveal exploitation of red deer, ibex and carnivores (Tagliacozzo et al., 2013). The radiocarbon dataset from the whole sequence suggests that the Uluzzian units accumulated between 43.9 and 41.9 ka (thousands of years ago) cal BP, the nal Mousterian units A5 and A6 between 44.8 and 43.9 ka cal BP and underlying Mousterian units A8eA9 to A11 between 47.6 ka cal BP (considered as the minimum age) and 44.8 ka cal BP (Peresani et al., 2008; Higham et al., 2009). The discovery context of the teeth The late Mousterian layers from A11 to A5 and the Uluzzian layers A4 and A3 have been excavated at different times since 1989 outside the present-day drip-line and inside the cave. All of the teeth (Table 1, SOM Figs. S1, S2) were found during sediment sieving. Fumane 1 was discovered at the base of unit A11, in square 63, during the 1989 excavation that explored the stratigraphy in the easternmost zone in proximity to the present-day cave entrance (SOM Figs. S1, S2). In the same square and during the same eld season in which Fumane 1 was found, the labial half of an incisor was discovered. This tooth, labeled Fumane 3 and initially considered human, proved to be a lower incisor of Ursus sp. Fumane 4 and 5 were discovered during the 2010e2011 excavations in unit A9 (level A9I-square 98f, and level A9- square 97 g, respectively), in the westernmost zone at the entrance of the present-day cavity (SOM Fig. S2). Extensively excavated over a total surface of 68 m2, the stratigraphic complex identied under the unit A9 has variable thickness, reaching about 20 cm in squares 98 and 97, where it also includes the anthropogenic levels A9 and A9I, separated by thin sheets of sand. Layering is regular, boundaries are clear and no traces of bioturbation, cryoturbation or injections of allocthonous sediment were recorded during the excavation in this zone. Moreover, no artifacts diagnostic of the overlying and underlying Levallois Mousterian units A6 and A10 were identied in A9. Unfortunately, the exact position of Fumane 6 (a small tooth fragment) cannot be dened. It was found in layer A3I, which extends for over 10 m2 in the easternmost part of the cave entrance. Field observations in this zone carried out during the 1993, 1995 and 1996 excavations have revealed post-depositional disturbances due to frost action and other mechanisms which have affected the sequence between layers A4 to D3, thus producing signicant dispersion of Proto-Aurignacian stone implements in the layers below. Based on the spatial scattering of the diagnostic int artifacts, the attribution of the fragmented tooth to the Uluzzian or Proto-Aurignacian complexes remains uncertain. Nevertheless, Fumane 6 has been included in the present contribution because, following the recent reassessment of the teeth from Grotta del Cavallo (Benazzi et al., 2011a), it has become paramount to establish whether the last Neandertals may have had anything to do with the Uluzzian across the geographical spread of this culture. Materials and methods Micro-CT scan High-resolution micro-CT images of the Fumane teeth (Table 1, Fig. 2) were obtained with a Skyscan 1172 microtomographic system (Max Planck Institute for Evolutionary Anthropology, Leipzig,

Germany) using the following scan parameters: 100 kV, 100 mA, with an aluminum/copper lter (0.50 mm/0.04 mm thickness). Volume data were reconstructed using isometric voxels ranging between 11.98 mm and 13.35 mm. The micro-CT images of the original sample were virtually segmented using a semiautomatic threshold-based approach in Avizo 7 (Visualization Sciences Group Inc.) to reconstruct 3D digital models of the teeth, which were then used to support the morphological description and to collect morphometric data on the teeth. Morphological description Terminology for the morphological description of the teeth follows Scott and Turner (1997). Owing to the lack of guidelines to assess non-metric dental traits in the deciduous dentition, nonmetric characters were recorded using the Arizona State University Dental Anthropology System (ASUDAS) (Turner et al., 1991), which was developed for permanent teeth. Occlusal wear stage was assessed based on Molnar (1971). Ages at death for the deciduous teeth were estimated using the tooth formation, dental eruption and root resorption sequences provided by Moorrees et al. (1963), Ubelaker (1978) and AlQahtani et al. (2010) for recent Homo sapiens. Moorrees and colleagues approach (which for the deciduous dentition is limited to canines, rst and second molars), was recently improved by Shackelford et al. (2012) by translating the graphical information from Moorrees et al. (1963) to numerical parameters. We used these parameters for a more accurate estimation of age at death. Metric comparison For metric traits, we measured the mesio-distal (MD) and bucco-lingual (BL) crown and cervical diameters in the digital models of the teeth (Table 1). The BL diameters were then compared with a sample of Neandertals (N), Upper Paleolithic H. sapiens (UPHS) and recent H. sapiens (RHS) collected from the scientic literature (Henry-Gambier, 2001; Henry-Gambier et al., 2004; Crevecoeur et al., 2010; Hershkovitz et al., 2011). Moreover, further morphometric analyses for the specimen Fumane 1 (lower second deciduous molar) were carried out, as for this tooth class digital methods for taxonomic discrimination have been recently developed (Benazzi et al., 2011b, 2012). We used crown and cervical outline analysis (Benazzi et al., 2012), and we measured various parameters (such as enamel and dentine volume) gathered from the lateral aspects of the crown (Benazzi et al., 2011b). Since the adoption of a common orientation system is required for outline analysis, the best-t plane of the cervical line was computed in Rapidform XOR2 (INUS Technology, Inc., Seoul, Korea). The tooth was aligned with the cervical plane parallel to the xy-plane of the Cartesian coordinate system and rotated around the z-axis, so that the tangent to the geometrical minimum of the two lobes of the lingual side is parallel to the x-axis (Benazzi et al., 2012). For outline analysis, the crown outline was projected onto the cervical plane, while the cervical outline was represented by the contour of the section identied by the cervical plane itself (SOM Fig. S3). Since Fumane 1 shows interproximal wear (see morphological description below), the mesial and distal borders of the crown outline were corrected following the crown margins in occlusal view (e.g., Wood et al., 1983; Bailey, 2004; Benazzi et al., 2011c). The outlines were imported in Rhino 4.0 Beta CAD environment (Robert McNeel and Associates, Seattle, WA), centered superimposing the centroids of their area according to the sample created in a previous contribution (Benazzi et al., 2012), represented by 16 pseudolandmarks obtained by equiangularly spaced radial vectors out of the centroid, and scaled to unit centroid size

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

S. Benazzi et al. / Journal of Human Evolution xxx (2014) 1e8

Figure 2. Three-dimensional digital models of Fumane 1 (lower left second deciduous molar, Ldm2), Fumane 4 (upper right central deciduous incisor, Rdi1), Fumane 5 (lower right lateral deciduous incisor, Rdi2), and Fumane 6 (molar fragment). The black bar is equivalent to 1 cm. B, buccal; D, distal; L, lingual; M, mesial; O, occlusal.

(Benazzi et al., 2011a,c; 2012). The shape variables of the Fumane 1 crown and cervical outlines were projected into the shape-space obtained from a principal component analysis (PCA) of the comparative sample used by Benazzi et al. (2012). Leave-one-out cross-validation quadratic discriminant analysis (QDA) was then used to classify Fumane 1. Three measurements (the enamel volume in mm3, the lateral dentine plus pulp volume [LDPV] in mm3, and the EDJ lateral surface in mm2) were collected from a region between the cervical plane and a plane parallel to the cervical plane and passing through the lowest point of the enamel-dentine junction (EDJ) in the midocclusal basin (SOM Fig. S3) (Toussaint et al., 2010; Benazzi et al., 2011b). These measurements were used for the computation of both the lateral average enamel thickness index (AET volume of lateral enamel divided by the EDJ lateral surface, measured in millimeters) and the lateral relative enamel thickness index (RET AET divided by the cubic root of LDPV, a scale-free index) (Toussaint et al., 2010). Finally, the distance between the two planes (lateral crown height LCH) was measured. Parameters gathered from the lateral aspect of the Fumane 1 crown were compared with those obtained by Benazzi et al. (2011b). Standardized scores (Z-scores) were computed to establish to which group means the values of the Fumane teeth were closest. The data were processed and analyzed using R v. 2.15.1 (R Development Core Team, 2012). Results Morphological description Fumane 1 Lower left second deciduous molar (Ldm2), represented by a complete crown and the cervical quarter of the root (Fig. 2). The tooth, split in two halves by a MD fracture and with

several smaller fractures, is heavily worn, equal to an advanced wear stage 5 (Molnar, 1971). On the occlusal surface, which is worn obliquely mesio-buccally to disto-lingually, only a small area of enamel is preserved. When the enamel is digitally removed, the remnants of ve principal cusps, as well as a complex pattern of grooves and crests are still visible on the dentine surface (EDJ). The metaconid is in contact with the hypoconid, conrming the classic Y-5 pattern. The two deep grooves that separate respectively the protoconid/hypoconid and hypoconid/hypoconulid are interrupted by two crests that connect these cusps. Two additional grooves can be distinguished on the buccal face of the EDJ, one on the mesiobuccal aspect of the protoconid and another on the disto-buccal aspect of the hypoconulid. Moreover, an anterior fovea is bordered distally by a continuous mid-trigonid crest (MTC) of grade 2 or 3 (Bailey et al., 2011) (Fig. 3a), a trait that appears with high frequency in Neandertals (Bailey, 2002). The buccal wall of the crown bulges and is evenly convex mesiodistally. This morphology is typically observed in Neandertal dm2s (Benazzi et al., 2012). Both mesial and distal aspects bear large interproximal wear facets. The mesial facet is more invasive than the distal (where subvertical grooves can be noted; see Villa and Giacobini, 1995), having reached the underlying dentine. Root resorption suggests that the tooth had been lost ante-mortem due to the emergence of the permanent fourth premolar. The degree of resorption (stage Res3/4 of Moorrees et al., 1963) corresponds to an age ranging from about nine to 12 years based on the work by Shackelford et al. (2012). This age is also supported by the wear stage. Traces of calculus are present in the buccal and mesio-lingual cervical third of the crown. There is no evidence of either caries or enamel hypoplasia. The tooth crown has a MD diameter of 9.9 mm (minimum estimation due to wear) and a BL diameter of 9.4 mm (Table 1). At the cervix, the MD diameter is 8.2 mm and BL diameter is 7.9 mm.

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

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Figure 3. 3D digital model of the enameledentine junction (EDJ) of (a) Fumane 1, and (b) Fumane 6. MTC mid-trigonid crest. B, buccal; D, distal; L, lingual; M, mesial.

Fumane 4 Upper right central deciduous incisor (Rdi1), represented by a well-preserved crown and the cervical quarter of the root (Fig. 2). There is a large and deep crack (extending past the cervix) that runs the MD length of the tooth, from which a shallower disto-labially directed crack emanates. This smaller crack does not reach the cervix. The worn incisal surface corresponds to a wear stage 6 (Molnar, 1971) and is notable for its sharply oblique orientation. On the mesio-labial border of the incisal edge, small fragments of enamel are chipped off. From the incisal view, the crown has moderate labial convexity (ASUDAS grade 3) with a cervical swelling (but no tubercle-like structure). Due to the heavy wear, shovel-shaped morphology cannot be ascertained. A small interproximal wear facet is visible on the distal side of the crown, but not on the mesial side, and was probably removed by wear. The preserved root is longer labially (2.5 mm) than lingually (1.6 mm). The stage of resorption of the tooth is close to grade Res3/4 of Moorrees et al. (1963), suggesting that the tooth had been lost ante-mortem through dental development, a stage that corresponds to an age of approximately six years in recent modern children (Ubelaker, 1978; AlQahtani et al., 2010). Traces of calculus are present in the mesio-labial wall of the crown, but there is no evidence of either caries or enamel hypoplasia. The tooth crown has a MD diameter of 6.1 mm (minimum estimation due to wear) and a BL diameter of 5.4 mm (Table 1). At the cervix, the MD diameter is 4.6 mm and BL diameter is 4.9 mm. Fumane 5 Lower right lateral deciduous incisor (Rdi2) with wellpreserved crown and about two-thirds of the root preserved (Fig. 2). The dentine shows several fractures, and one of them crosses the enamel on the mesial side. The incisal surface is worn obliquely mesially to distally, exposing a large area of dentine equivalent to wear stage 4 (Molnar, 1971). From the incisal view the crown appears asymmetrical, mainly due to the distal projection of

a moderate lingual cervical eminence (but no tubercle-like structure). The labial surface exhibits pronounced mesio-distal convexity (ASUDAS grade 4). The lingual surface is concave, and shows remnants of faint mesial and distal marginal ridges, as well as a median ridge, which disappears as it reaches the cervical eminence. Interproximal wear facets are visible on the mesial and distal sides; the latter, which is more extensive, has impacted and reduced the expression of the distal marginal ridge. The preserved root stump, more elongated labially (6.05 mm) than lingually (1.45 mm), appears to be resorptive, conrming an age of approximately six years on the basis of recent human standards (Ubelaker, 1978; AlQahtani et al., 2010). There is no evidence of either caries or enamel hypoplasia. The tooth crown has a MD diameter of 5.5 mm (minimum estimation due to wear) and a BL diameter of 5.1 mm (Table 1). At the cervix, the MD diameter is 4.6 mm and BL diameter is 4.9 mm. Fumane 6 Small molar fragment with a short segment of root preserved (Fig. 2). The occlusal surface is heavily worn (at least wear stage 5), and a large interproximal wear facet marks one side of the fragment. On the portion of the crown where the enamel is preserved, the cervical line is nearly straight, and the enamel rises almost vertically after a hint of aring. When the enamel is virtually removed, a fovea is visible on the EDJ (Fig. 3b). Based on these features, it is likely that this fragment represents the mesio-lingual portion of a lower molar. Metric comparison Comparative data for BL crown diameters are reported in Table 2. For Fumane 5 (Rdi2), the computed Z-score is closer to the Neandertal mean than to Upper Paleolithic and recent H. sapiens. More ambiguous are the results obtained for Fumane 1 (Ldm2),

Table 2 Dental dimensions (in mm) of the Fumane teeth standardized to Z-scores of the hominin samplesaed used in this study (m mean; s standard deviation; n number of individuals). di1 BL m s (n) Fumane N UPHS RHS 5.44 6.13 0.35 (23)a 5.42 0.35 (18)a 4.87 0.35 (47)a 1.97 0.06 1.63 Z score BL m s (n) 5.08 4.85 0.25 (15)a 4.58 0.30 (18)a 4.14 0.37 (62)a 0.92 1.67 2.54 di2 Z score BL m s ( n) 9.36 9.4 0.5 (34)b 9.44 0.35 (8)c,d 8.3 0.6 (57)b 0.08 0.23 1.77 dm2 Z score

N Neandertals; UPHS Upper Paleolithic Homo sapiens; RHS recent Homo sapiens. a Crevecoeur et al. (2010). b Hershkovitz et al. (2011). c Henry-Gambier et al. (2004). d Henry-Gambier (2001).

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

S. Benazzi et al. / Journal of Human Evolution xxx (2014) 1e8

Figure 4. Shape-space PCA plots of Neandertal and H. sapiens (RHS UPHS) dm2 crown outlines (a), and cervical outlines (b). The deformed mean outlines in the four directions of the PCs are drawn at the extremity of each axis. N, Neandertal; UPHS, Upper Paleolithic H. sapiens; RHS, recent H. sapiens.

with low Z-scores for both Neandertals and UPHS, while the BL diameter of Fumane 4 (Rdi1) is closer to the UPHS mean. Fumane 1 crown and cervical outlines were projected in the shape-space previously computed by Benazzi et al. (2012) for Neandertal and H. sapiens dm2s (Fig. 4). For the crown outline, the rst two PCs account for about 73% of the total variance (PC1 41.5%; PC2 31.3%). Neandertals separate from UPHS and RHS along PC2 due to a disto-buccal outline expansion and a convex lingual outline shape (Fig. 4a). Fumane 1 plots within the range of variability of the Neandertal sample identied by the convex hull. For the cervical outline, the rst two PCs account for about 60% of the total variance (PC1 35.5%; PC2 24.7%). Neandertals and H. sapiens separate mainly along PC1 and, to a lower extent, along PC2, the former having a subcircular (positive PC1) or subsquare (positive PC2) cervical outline, with a disto-buccal expansion and convex lingual outline (Benazzi et al., 2012). Fumane 1 falls close to the Neandertal sample, but far from the range of variability of H. sapiens dm2s (Fig. 4b). The cross-validation QDA of the rst three PCs shows that 92% (for crown outline) and 96% (for cervical outline) of the Neandertal and H. sapiens samples are correctly classied (Benazzi et al., 2012). For both crown and cervical outline, Fumane 1 is attributed to Neandertals with a Ppost > 0.97. Similar results were obtained considering the parameters gathered from the lateral aspects of the dm2 crown. As shown in Table 3, in almost all cases the computed Z-score for Fumane 1 (except for LCH) is closer to Neandertals than H. sapiens due to the relative large volume of the dentine and the low RET index. However, as mentioned in a previous contribution (Benazzi et al., 2011b), results obtained from the lateral enamel thickness should be considered with caution, as the method is strongly affected by the magnitude of the interproximal (and sometime occlusal) wear. Discussion and conclusions All of the human remains from Fumane Cave are represented by deciduous teeth, except for the small dental fragment unearthed from the Uluzzian deposit. This poses serious limits for taxonomic discrimination, because most studies of dental morphological

variation, as well as the development of advanced (digital) morphometric protocols (for both the external and internal dental topography) useful in distinguishing between Neandertals and H. sapiens teeth, have mainly focused on the permanent dentition, with an unavoidable bias towards unworn/slightly worn teeth (e.g., Bailey, 2002, 2004, 2006; Olejniczak et al., 2008; Benazzi et al., 2011c, 2013; Gomez-Robles et al., 2012; Smith et al., 2012). More recently, few studies have explored deciduous dental variation, but these contributions either have been limited to specic tooth classes (i.e., deciduous molars; e.g., Benazzi et al., 2011a,b; 2012; Benazzi, 2012; Bailey et al., 2014, in press) or, for dental tissue proportion, have required unworn teeth (Bayle et al., 2009, 2010). It is then not surprising that here we emphasize the analysis of Fumane 1, since morphometric methods have been developed recently to specically address the issue of heavily worn dm2s (Benazzi et al., 2011b, 2012). While traditional morphometric analysis based on BL crown diameter fails to discriminate between Neandertal and H. sapiens dm2s, outline analyses (both crown and cervical outline) and the parameters gathered from the lateral aspect of the dm2 crown support the Neandertal afliation of Fumane 1. This is supported by some morphological features recognized on the EDJ (e.g., anterior fovea distally bordered by a MTC). The taxonomic attribution of the other dental remains is much more difcult. While there are no morphological features useful to
Table 3 Lateral crown height (LCH, mm), lateral dentine plus pulp volume (LDPV; mm3) and lateral enamel thickness of Fumane 1, standardized to Z-scores of the hominin dm2 samplea used in this study. Homo sapiens Fumane 1 LCH LDPV AETb RETc
a b c

Neandertal Mean (SD/n) 3.03 183.70 0.37 6.54 (0.23/8) (28.22/10) (0.07/10) (1.17/10) Z-score 1.00 0.82 0.14 0.01

Mean (SD/n) 2.58 138.20 0.41 7.91 (0.22/18) (19.49/18) (0.05/18) (0.85/18)

Z-score 1.00 1.15 1.00 1.60

2.80 160.60 0.36 6.55

Comparative data from Benazzi et al. (2011b). Average enamel thickness index (in mm). Relative enamel thickness index (scale-free).

Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001

S. Benazzi et al. / Journal of Human Evolution xxx (2014) 1e8

classify Fumane 4, the Z-score computed for its BL diameter is closer to those of H. sapiens than it is to Neandertals. The asymmetrical crown of Fumane 5, with faint mesial and distal ridges on the lingual aspect, coupled with the large BL diameter suggests that the tooth belongs to a Neandertal (Bailey, unpublished data). As the teeth were found in the same unit (A9) and appear to be in a nal stage of resorption, it is possible that they both belong to a second individual (approximately six years old based on recent H. sapiens standards), younger than the one to which Fumane 1 belongs (w10/ 11 years old based on recent H. sapiens standards). Even less can be said for Fumane 6, for which the archaeological integrity of the context in which the fossil was discovered is uncertain (Uluzzian levels but with dispersion of Proto-Aurignacian stone implements due to post-depositional disturbance). The crown fragment is unambiguously part of a permanent molar, most probably a lower molar, and the advanced stage of wear does not support its association with either Fumane 1 or Fumane 4/5, thus raising up to three the minimum number of individuals represented in the Middle Paleolithic and Uluzzian levels of Fumane Cave. However, there are no morphological features useful for a taxonomic discrimination of the tooth. The human remains unearthed from the Mousterian deposit of Fumane Cave are among the last Neandertals in Italy. This lends further support to inferences based on the cultural record that Neandertals were the bearers of the Aspa marginata ochered shell (a Miocene-Pliocene fossil marine shell smeared with pigment, discovered in Unit A9, and supposed to be a component of Neandertal symbolic culture; Peresani et al., 2013b) and the makers of the cut-marked bird bone assemblages recovered from several layers across the late Mousterian sequence (Peresani et al., 2011b). Based on the recent reassessment of the dental remains from the Uluzzian levels of Cavallo Cave (South Italy; Benazzi et al., 2011a; Ronchitelli et al., 2014; Bailey et al., in press), the Uluzzian of Fumane might be provisionally assigned to H. sapiens, even though the uncertainty about both the position in which Fumane 6 was found and its taxonomic attribution do not allow us to conclude this with certainty. In the nearby site of Riparo Mezzena, Neandertal remains associated with Levallois Mousterian lithic industries were retrieved from a deposit claimed to date to 40,380e 38,840 cal years BP (Longo et al., 2012; Condemi et al., 2013). If this chronological attribution is correct, Neandertals occupied Mezzena when Proto-Aurignacian modern humans were already at Fumane (Higham et al., 2009), which would suggest that they co-existed for about 5000 years and that replacement of the former by the latter was discontinuous in biological and cultural terms. It should be pointed out, however, that there is a strong disparity in the quality of the archaeological data from these two sites and that the limited data from Riparo Mezzena requires the support of an adequate dating programme to be taken fully into account (as previously suggested by Douka et al., 2014). Further research is needed to better understand the timing of the disappearance of Neandertals from the Italian Peninsula and the role played by incoming modern humans in this process during the Middle to Upper Paleolithic transition. Besides an increase in well documented and chronologically-dated sites, it is essential to acquire diagnostic human remains to study with state-of-the-art methods. Due to methodological limitations, there is a real risk that the taxonomic discrimination of Late Pleistocene human remains might be inuenced by the archaeological context in which the fossils were discovered (Benazzi et al., 2014), assuming that, at least in Europe, Neandertals were the makers of Mousterian technocomplexes. Therefore, while the human teeth from Fumane Cave increase the sample of Italian fossil remains, they emphasize the need to develop new methods to extract meaningful taxonomic information from deciduous and worn teeth.

Acknowledgments The authors are grateful to H. Temming for technical support. We wish to thank the Editor (Dr. S. Elton), the Associate Editor and the anonymous reviewers for their important comments, which improved tremendously the manuscript. Research at Fumane is coordinated by the Ferrara University in the framework of a project supported by the Ministry of Culture e Veneto Archaeological Superintendency, public institutions (Lessinia Mountain Community e Regional Natural Park, Fumane Municipality, Veneto Region e Department for Cultural Heritage), and private associations and companies (Cariverona Foundation, Banca CC Valpolicella-Benaco, Roberto Gardina & C., Albino Armani Vinegrowers, Dental Clinic Rea Sibilla).

Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.jhevol.2014.03.001

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Please cite this article in press as: Benazzi, S., et al., Middle Paleolithic and Uluzzian human remains from Fumane Cave, Italy, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.03.001