Journal of Human Evolution

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1 Journal of Human Evolution xxx (2010) 1e5 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: News and Views Multivariate analysis and classification of the Apidima 2 cranium from Mani, Southern Greece Katerina Harvati a, *, Chris Stringer b, Panagiotis Karkanas c a Department of Early Prehistory and Quaternary Ecology, Senckenberg Center for Human Evolution and Paleoecology, Eberhard Karls Universität Tübingen, Rümelinstrasse 23, Tübingen 72070, Germany b Natural History Museum, Cromwell Road, London SW7 5BD, UK c Ephoreia of Paleoanthropology and Speleology of Southern Greece, Ardittou 34b, Athens, Greece article info Article history: Received 16 May 2010 Accepted 30 September 2010 Keywords: Homo neanderthalensis Homo heidelbergensis Greece In 1978, two well-preserved fossil human crania were discovered at the Apidima site, a karstic cave complex in the Mani peninsula (southern Peloponnese; Fig. 1), during excavations by the University of Athens Medical School (Pitsios, 1995; Harvati and Delson, 1999; Harvati et al., 2009). Together with the Petralona cranium, the Apidima specimens represent the most important paleoanthropological finds in Greece, and some of the most significant human fossil discoveries in south-eastern Europe, a region whose paleoanthropological record remains relatively unexplored. However, despite their importance, these specimens remain obscure; little has been published about them in the international literature, and detailed description and documentation are still pending. Of the two specimens, Apidima 2 is the better preserved, though somewhat distorted and showing multiple cracks (Fig. 2A). The occipital bone, parts of the temporals, as well as all of the teeth and part of the palate, are all absent. A fragment of the right mandibular ramus is preserved, attached to the encasing matrix and cranium in roughly anatomical position. Apidima 2 has been described as showing an elongated, low vault with a pronounced supra-orbital torus, a wide interorbital breadth, large rounded orbits, no canine fossa, a large nasal aperture, and a prognathic face (Harvati and Delson, 1999; Geanacos, 2001; Pitsios, 2002; Harvati et al., 2009). It is relatively gracile, and has been considered a female (Harvati and Delson, 1999; Pitsios, 2002; Harvati et al., 2009). Neanderthal affinities have been noted and the specimen has been proposed to * Corresponding author. address: (K. Harvati). represent a pre-neanderthal. Of particular interest is its possible relationship with the Petralona cranium from Northern Greece (Fig. 2B), and the suggestion that Apidima 2 may represent a female Homo heidelbergensis comparable to Petralona in geological age. Apidima 1 is less complete and preserves only the posterior part of the neuro- and basicranium. Attempts at identifying Apidima 2 to taxon have been stymied by the lack of both detailed description and extensive metric data. On the basis of its general morphology, Pitsios (1999) suggested that Apidima 2 lies on the Neanderthal lineage and proposed the name Homo (sapiens) teanarius (Pitsios, 1995). Harvati and Delson (1999) suggested affinities with H. heidelbergensis (s.l.). Nine osteometric measurements published in a forensic report by Koutselinis et al. (1995) have been used as variables in previous metric analyses by Manolis (1996) and, more recently, by Harvati et al. (2009). Both studies were inconclusive in their results, placing Apidima 2 either in an area of overlap between H. heidelbergensis (s.l.) and early anatomically modern humans (Manolis, 1996), or between Homo neanderthalensis and H. heidelbergensis (s.l.) (Harvati et al., 2009). Given the importance of the Apidima specimens and the small amount of information on them that currently exists, we reexamine the metric data published for Apidima 2. We 1) test the original nine reported measurements for possible error associated with distortion; 2) correct the measurements for size, so that we can examine shape differences; and 3) take into account as many measurements and Middle-Late Pleistocene specimens as possible, in order to achieve the best resolution for classifying Apidima 2. We review the geology and chronology of the site in light of recent reevaluation of regional geomorphology and discuss the implications of our findings for the interpretation of the Apidima remains. Materials and methods Our comparative sample comprises nineteen fossil human crania (Table 1) on which all of the variables known for Apidima 2 can be measured (Table 2). Most data were collected by one of us (CS), although some were taken from the literature (Trinkaus, pers. comm., for Shanidar 1; Arsuaga et al., 1997). For the purposes of our analyses, we grouped the European Middle Pleistocene specimens /$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi: /j.jhevol

2 2 K. Harvati et al. / Journal of Human Evolution xxx (2010) 1e5 Figure 1. Left panel: map of the most important Paleolithic sites in Greece. Stars represent sites where human remains have been recovered. Image adapted from Harvati et al. (2009). Right panel: the Apidima locality. Caves AeE are labelled, as is the approximate position of the 5 masl highstand. Petralona and Sima 5, together with the African specimen from Broken Hill, into H. heidelbergensis (s.l.), due to their well-documented overall morphological similarities (e.g., Stringer, 1974; Stringer et al., 1979; Rightmire, 2001; Harvati et al., 2007, 2010; Harvati, 2009). We recognize that the latter two specimens may or may not belong to this taxon (e.g., Hublin,1998, 2009; Endicott et al., 2010; Harvati et al., 2010). Following previous views on its classification, Apidima 2 was also a priori assigned to H. heidelbergensis (s.l.). We conducted row standardization in order to control for outlier values (and possible measurement errors due to breakage and/or distortion) in the reported measurements for Apidima 2 in comparison with the mean Neanderthal, H. heidelbergensis, and H. sapiens values for the same measurements. This was achieved by dividing each value by the mean of all measurements for Apidima 2 and for each of the three samples used. Two measurements that were found to be outliers were removed from the analysis. The remaining seven raw variables were adjusted for size by subtracting the log geometric mean of each variable for each individual from each log-transformed measurement. We then conducted a canonical variates analysis (CVA) on the seven size-corrected variables and classified the specimen using discriminant analysis. Finally, we used three of the apparently undistorted reported measurements (glabella-opisthocranion length, maximum cranial breadth, and basion-bregma height) to estimate cranial capacity for Apidima 2 using the modified formula for Pleistocene humans provided by Olivier and Tissier (1975): Cranialcapacity: 0:304ðlengthbreadthbasion bregmaheightþþ346cc Figure 2. A: The Apidima 2 cranium. Photograph of a cast of the original specimen before complete separation from the block of breccia. The arrow points to the mandibular fragment adhering to the matrix. B: the Petralona cranium. Photographs provided by and copyright Eric Delson.

3 K. Harvati et al. / Journal of Human Evolution xxx (2010) 1e5 3 Table 1 Specimens included in this study, the taxon to which they were assigned for the purposes of the canonical variates analysis (CVA), and the source of measurements used. Abbreviations used in Fig. 3 are shown in parentheses. Specimen Taxon Measurements source Apidima 2 (Ap2) H. heidelbergensis (s.l.) Koutselinis et al. (1995) Atapuerca Cranium 5 (Si) H. heidelbergensis (s.l.) Arsuaga et al. (1997) Petralona (Pe) H. heidelbergensis (s.l.) CS Broken Hill (Kb) H. heidelbergensis (s.l.) CS Guattari (Gt) H. neanderthalensis CS Forbes Quarry 1 (Gb) H. neanderthalensis CS La Chapelle (Ch) H. neanderthalensis CS La Ferrassie 1 (Fr1) H. neanderthalensis CS Shanidar 1 (Sh1) H. neanderthalensis E. Trinkaus (pers. comm.) Qafzeh 6 (Qz6) H. sapiens CS Qafzeh 9 (Qz9) H. sapiens CS Skhul 5 (Sk5) H. sapiens CS Abri Pataud (AP) H. sapiens CS Cro Magnon 1 (CM1) H. sapiens CS Chancelade (Cn) H. sapiens CS Grimaldi 6 (Gr) H. sapiens CS Mladec1 (Ml1) H. sapiens CS Predmostí 3 (Pd3) H. sapiens CS Predmostí 4 (Pd4) H. sapiens CS Upper Cave 101 (UC1) H. sapiens CS Results Row standardization When the row-standardized measurements for Apidima 2 were compared to the equivalent mean values for the other samples, bizygomatic breadth (ZYB) and orbital height (OBH) stood out as outliers (Table 2). These variables are likely affected by distortion or breakage: distortion is apparent in the area of the left orbit, and breakage can be seen in the region of the right zygomatic bone (Fig. 2B). ZYB and OBH were removed from further analysis. Canonical variates analysis Canonical Axis 1 (85.4% of the total variance; Fig. 3) separates H. sapiens from H. heidelbergensis (s.l.) and H. neanderthalensis, and is influenced mostly by BBH, NPH, and GOL. Canonical Axis 2 (14.6% of the total variance) separates Neanderthals from H. heidelbergensis (s.l.) and is mostly influenced by XCB, NPH, and NLH. Apidima 2 was a priori assigned to H. heidelbergensis (s.l.) following previous views on its status as a pre-neanderthal. Despite this assignment, Apidima 2 is pulled out of the range of the other three H. heidelbergensis (s.l.) specimens, and falls within the Neanderthal range on the first two canonical axes. Discriminant analysis Apidima 2 was classified as H. neanderthalensis (posterior probability 1.00). This analysis classified most specimens correctly to species with the exception of Skhul 5, which was misclassified as H. heidelbergensis (s.l.) (posterior probability 0.85). Cranial capacity The estimated cranial capacity for the Apidima 2 individual is 1454 cc. Geomorphological implications for the chronology of the Apidima site The Apidima site comprises five caves (Caves AeE; Fig. 1) formed in the Upper CretaceouseLate Eocene limestone on the coastal cliffs of the inner Mani. Key in understanding the chronology of the specimens is the relationship of the skull breccia encasing the human specimens to other deposits within Cave A. Since the human remains were recovered at least 2.5 m above all other finds from Cave A (including Middle Paleolithic lithic artifacts [Kourstesi-Philipaki, reported in Harvati and Delson, 1999], as well as Middle-Late Pleistocene faunal remains [Tsoukala, 1999]), they are most likely not contemporary with them (Lax, 1995). Attempts at radiometric dating have not been fruitful. Koutselinis et al. (1995) suggested an age between ka, a chronology considered broadly in accordance with the specimens perceived archaic morphology. In the absence of radiometric dating and clearly associated archaeological and faunal evidence, understanding of the site s chronology relies on evidence for Pleistocene sea level highstands present in the Mani region. The main formation of the caves is attributed to sea level highstands (Pitsios, 1985; Basiakos, 1993), which also produced notches and wave-cut platforms found at similar heights in the area (Fig. 1). Cave B and the upper part of Cave E formed at a 12 masl highstand (Pitsios, 1985), and were later filled by red Pleistocene breccia, forming a talus cone that fanned out along the cliff below Caves C and D, and sealed the entrances of Caves B and E. The talus cone was eroded and partially collapsed during a subsequent highstand, resulting in a reopening of Caves E and B. The main opening of Cave A seems to have occurred during a later and lower Table 2 Top: raw measurements (in mm) reported for Apidima 2 (in bold) and mean values for H. heidelbergensis (s.l.), H. neanderthalensis, early anatomically modern humans, and Upper Paleolithic samples. Bottom: row-standardized values of the same variables. The values reported for ZYB and OBH for Apidima 2 clearly stand out in comparison to the other row-standardized values for those measurements. Glabella- Opisthoc. length (GOL) Maximum Cranial breadth (XCB) Basion- Bregma height (BBH) Bizygom. breadth (ZYB) Nasion- Prosth. height (NPH) Nasal height (NLH) Nasal breadth (NLB) Orbital breadth (OBB) Raw measurements Apidima Mean H. heidelbergensis (s.l.) Mean H. neanderthalensis Mean early anatomically modern Mean Upper Paleolithic Row standardized Apidima Mean H. heidelbergensis (s.l.) Mean H. neanderthalensis Mean early anatomically modern Mean Upper Paleolithic Orbital height (OBH)

4 4 K. Harvati et al. / Journal of Human Evolution xxx (2010) 1e5 MIS 6 (190e130 ka). Given the tectonic instability of the area, however, the possibility that the 5 m and 12 m paleocoastlines correlate with the Neo-tyrrhenian (MIS 5c) and Eutyrrhenian (MIS 5e) highstands cannot be excluded. This would constrain the age of the crania to be between 115 ka and 105 ka. Discussion Figure 3. Canonical variates analysis, canonical axes 1 and 2. Abbreviated specimen labels as in Table 1. Although early modern humans from Skhul and Qafzeh are labelled separately from Upper Paleolithic specimens, the two samples were pooled in the analysis as H. sapiens. 5 m highstand, which dissolved and eroded the red breccia as well as the underlying limestone (Basiakos, 1993). Cave A is tunnelled for several meters inside the red breccias (Fig. 3), and therefore could not have been filled with the cone sediments after its formation (contra Lax, 1995). The skull breccia was found almost 7 m from the entrance of Cave A. Although no physical connection was observed, the excavators proposed that it was part of the talus cone breccia found in front of the cave, and through which the entrance of Cave A is tunnelled, because of sediment similarities (Pitsios, 1985). If so, the human crania must have been deposited before the main opening phase of Cave A (Pitsios, 1985). At a later time, Middle Palaeolithic cultural remains were deposited on the floor of the Cave A (see above). It therefore seems that the opening of Cave A, as well as the exposure of the skull breccia, is related to the 5 m highstand. Geomorphological evidence of this highstand, and of the higher coastline at ca.12 m related to Caves B and E, is reported from several locations around the Mani (Kelletat and Gassert, 1975; Tsartsidou et al., 2002). These two highstands were believed in the past to represent the Neo-tyrrhenian and Eutyrrhenian sea levels, respectively (Kelletat and Gassert, 1975; Eutyrrhenian is correlated with MIS 5e, i.e., the last interglacial. Neo-tyrrhenian could represent MIS 5c [e.g., Keraudren et al., 2000] or MIS 5a). However, recent radiometric dates and stratigraphic correlations assign two outcrops representing the 5 m highstand to the last interglacial, i.e., the Eutyrrhenian rather than the Neo-tyrrhenian highstand (at the Kalamakia Cave, close to Apidima, and at Lakonis Cave on the eastern coast of Mani; Darlas, 2007; Elefanti et al., 2008). This new assessment agrees with the general consensus that the global sea level peaked at least 6 m higher than today, during the last interglacial (Kopp et al., 2009). Therefore, there is a strong possibility that Cave A was formed during the last interglacial. If this is correct, Caves B and E were formed by an earlier and even higher sea level occurrence, possibly during MIS 11 (w430e400 ka), the longest and one of the warmest interglacials (Augustin et al., 2004), whose highstand is thought to range from close to the present sea level up to 20 masl (Waelbroeck et al., 2002; Olson and Hearty, 2009). A correlation of the 12 m paleocoastline with MIS 11 puts the age of the Apidima crania between ka. Rondoyanni et al. (1995), on the basis of field observations and tentative correlations with other studied areas, constrained the formation of the talus cone to the Riss, and probably late Riss, which is broadly correlated with Previous assessments of the phylogenetic position of Apidima 2, and the less complete Apidima 1, have relied on a few short published descriptions (e.g., Koutselinis et al., 1995; Pitsios and Liebhaber, 1995; Pitsios, 1999, 2002), brief visual inspections (e.g., Harvati and Delson, 1999), and morphometric analyses of a few published measurements (Manolis, 1996; Harvati et al., 2009). Apidima 2 has been described as showing some Neanderthal-like facial features, and possibly representing an early member of the Neanderthal lineage closely related to Petralona and likely dating to the Middle Pleistocene (Harvati and Delson, 1999; Pitsios, 1999, 2002; Harvati et al., 2009). Our reassessment of the taxonomic status of Apidima 2 also relied on published measurements. However, by identifying and excluding variables affected by distortion or breakage, we were able to remove a possible source of error, which might have confounded previous results (Manolis, 1996; Harvati et al., 2009). We also adjusted the measurements for size and maximized both the comparative sample and the variables used. Contrary to our expectations, Apidima 2 did not show affinities with H. heidelbergensis (s.l.) or with the Petralona cranium in particular, but aligned more closely with our Neanderthal sample despite having been grouped a priori with H. heidelbergensis (s.l.). A brief comparison of the Apidima 2 frontal view to that of Petralona (Fig. 2) confirms several differences between the two specimens, including a more Neanderthal-like, relatively narrower face and higher cranium in Apidima (although the exact position and orientation of the two specimens could not be controlled and is not identical). However, Apidima 2 appears to lack the extremely derived Neanderthal nasal morphology, including the very high and protruding nasal bridge. Our estimate of cranial capacity at 1454 cm 3 places Apidima 2 within the Neanderthal range of variation (1200e1700 cm 3 ; Holloway et al., 2004) and above the values reported for Middle Pleistocene specimens (Holloway et al., 2004), although Sima 4 approaches this value at 1390 cm 3 (Arsuaga et al., 1997; Holloway et al., 2004). Similar cranial capacity values are reported for Ehringsdorf (1450 cm 3 ), Reilingen (1430 cm 3 ), and Krapina B (1450 cm 3 ). This estimate agrees with our comparative analysis in pointing to Neanderthal affinities, but is limited in that it is based on three external cranial variables and is not a direct measurement of cranial capacity. In conclusion, our observations suggest that a late Middleeearly Late Pleistocene chronology is most consistent with the morphology the Apidima fossils. Our review of the site s geological setting points to 400e105 ka as the most likely period for the accumulation of the relevant sediments. This time bracket is very wide, but is likely further constrained to the latter part of this time period. It should be pointed out that our results rely on only a small number of metric data without detailed morphological description, and should therefore be considered tentative. A detailed description and a more exhaustive comparative analysis based on additional linear or 3-D data, is crucial to arriving at a conclusive assessment. Nevertheless, the Neanderthal affinities indicated here place the Apidima site and specimens among the Middle Paleolithic localities known from the immediate geographic vicinity, which have yielded a number of well-documented, though fragmentary, fossil human remains (Darlas and de Lumley, 1998; Panagopoulou et al., 2002e2004; Harvati et al., 2003; Richards et al., 2008; Smith et al., 2009).

5 K. Harvati et al. / Journal of Human Evolution xxx (2010) 1e5 5 Acknowledgements We thank Eric Delson for helpful discussion and for kindly providing the photographs used in Fig. 2. Constructive comments were also provided by Andreas Darlas. We are grateful to the Ephoreies of Paleoanthropology and Speleology (of Southern and of Northern Greece) of the Greek Ministry of Culture and to the University of Athens. This work was supported by Eberhard Karls Universität Tübingen and the Senckenberg Center for Human Evolution and Paleoecology. Chris Stringer is a member of the Ancient Human Occupation of Britain project, funded by the Leverhulme Trust. References Arsuaga, J.L., Martinez, I., Gracia, A., Lorenzo, C., The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 219e281. 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