Postcranial hominin remains from the Late Pleistocene of Pešturina Cave (Serbia)

Journal Pre-proof Postcranial hominin remains from the Late Pleistocene of Pešturina Cave (Serbia) Joshua Lindal, Predrag Radović, Dušan Mihailović, Mirjana Roksandic PII:

S1040-6182(20)30061-6

DOI:

https://doi.org/10.1016/j.quaint.2020.02.019

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JQI 8151

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Quaternary International

Received Date: 14 November 2019 Revised Date:

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Accepted Date: 13 February 2020

Please cite this article as: Lindal, J., Radović, P., Mihailović, D., Roksandic, M., Postcranial hominin remains from the Late Pleistocene of Pešturina Cave (Serbia), Quaternary International, https:// doi.org/10.1016/j.quaint.2020.02.019. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.

Postcranial hominin remains from the Late Pleistocene of Pešturina Cave (Serbia) Joshua Lindal a,1, Predrag Radović b,1, Dušan Mihailović c, Mirjana Roksandic d * a

Department of Anthropology, University of Manitoba, 432 Fletcher Argue Building, 15 Chancellor Circle, Winnipeg, MB R3T 2N2, Canada;

b

National Museum Kraljevo, 2 Trg Svetog Save, 36000 Kraljevo, Serbia;

c

Department of Archaeology, Faculty of Philosophy, University of Belgrade, 18-20 Čika Ljubina, 11000 Belgrade, Serbia; d

Department of Anthropology, University of Winnipeg, 515 Portage Avenue, Winnipeg, Manitoba, R3B 2E9, Canada; *Corresponding author. E-mail address: [email protected] (M. Roksandic). 1

These authors contributed equally to this work.

Abstract: The Central Balkans represents a significant geographical gap in the human fossil record of Eurasia. Here we present two new human fossils from Pešturina Cave, Serbia: a partial atlas vertebra (C1) and a fragment of radial diaphysis. The atlas (Pes-1) derives from the lower portion of Layer 2 and conforms to modern human morphology. This layer is characterized by Gravettian industry despite uncertainties caused by bioturbation and difficulties in separating Layers 2 and 3. The radial fragment (Pes-2) was recovered from the contact zone between Layers 3 and 4, both of which represent Mousterian industries, and is tentatively assessed as Neanderthal based on morphology. With the recent publication of a Neanderthal molar (Pes-3) from the same site, Pešturina currently stands as the only Neanderthal fossil-bearing site in Serbia. These additional finds make Pešturina Cave the only site in the Central Balkans which preserves both modern human and Neanderthal remains with associated lithic industries and highlights the importance of Pešturina in the current discourse on hominin dispersals and migrations in the Balkans. Key words: Pešturina, Neanderthal, modern human, Middle Palaeolithic, Upper Palaeolithic, Central Balkans 1. Introduction The past decade has seen an increased interest in the paleoanthropology of the Balkan Peninsula (Harvati and Roksandic, 2016, and chapters therein; Tourloukis and Harvati, 2018). Sitting at the “crossroads of Europe” (Roksandic, 2016), the region is marked by geographical migration corridors that facilitated human and animal movement between Europe and the Levant. It also served as one of three major glacial refugia (Hewitt, 1999; Griffiths et al., 2004; Denell et al., 2011; Roksandic et al., 2018); but in contrast to the Iberian and Apennine Peninsulas, the Balkan refugium was never geographically isolated from the larger hominin “source” population in Asia. For this reason, the region is hypothesized to have supported a greater diversity of hominins than other parts of Europe and greater demographic complexity as isolated western populations, migrating east, encountered populations with Asian and African origins migrating west into 1

Europe. The presence of Neanderthal remains has long been established for Croatia (Janković et al., 2016) and Greece (Harvati, 2016), and non-Neanderthal Middle Pleistocene remains are known from Mala Balanica in Serbia (Roksandic et al., 2011; Skinner et al., 2016; Rink et al., 2013). However, human fossils spanning the Middle to Upper Palaeolithic transition remain scarce. The recent reassessment of Apidima 1 as an early modern human (Harvati et al., 2019) suggests the possibility of a much greater temporal overlap between Neanderthals and modern humans in the Balkans than previously thought, emphasizing the importance of all new human fossils from the Late Pleistocene of the region. Pešturina Cave is the only site in the Central Balkans which records both Middle Palaeolithic (Neanderthal) and Upper Palaeolithic (modern human) occupation levels with associated human remains (Mihailović and Milošević, 2012; Alex et al., 2019), including the first Neanderthal fossil identified in Serbia: Pes-3, an exceptionally well-preserved maxillary first molar (Radović et al., 2019). Here we report two additional human fossils from Pešturina Cave: a partial atlas (C1), and a fragmentary radial diaphysis. 1.1 Location: Pešturina Cave is located north-west of the village of Jelašnica (43°10' N, 21°54' E), some 20 km from the city of Niš, southeastern Serbia (Fig. 1A). The karst cave is set in the Upper Jurassic dolomites/reef limestones on the western slopes of Suva Planina Mt., about 330 m above sea level. The cave is 22 m long, with a 15 m wide by 3.5 m high entrance which faces west (Fig. 1B). An area of around 24 m2 has been explored since 2006 (when the excavations began) to a maximum depth of about 3 m. Five stratigraphic levels have been identified in Pešturina; a simplified stratigraphic section is presented in Figure 1C. The specimen Pes-1 was recovered from the bottom of Layer 2. Layer 2 and the top part of Layer 3 were subject to bioturbation, with clearly outlined root and animal tunnels. The interface between the layers is difficult to define. Despite the disturbance, the specimen was recorded from the undisturbed area in between the burrows. The lithic assemblage of Layer 2 is dominated by Upper Palaeolithic artifacts, with no evidence of Holocene intrusions, while a single quartzite artifact was found in the lowermost part of Layer 2, indicating possible admixture from Layer 3 (Middle Palaeolithic). While we cannot definitely exclude the possibility that the original context of Pes-1 was disturbed, it is not likely a recent Holocene intrusion since the bioturbation appears to have a Pleistocene origin. Therefore, the specimen is most likely associated with the Gravettian assemblage of Layer 2. There is, however, a small possibility that it belongs to the Mousterian sequence, given that the distinction between Layers 2 and 3 is not clear. Three AMS dates were obtained for this layer: a relatively late date (RTD-7148 - 13,400 ± 60 14C yr BP) obtained on a sample from the disturbed context where mixing with the late Pleistocene is likely; a date RTK-6446: 26,100 ± 620 14C yr BP, consistent with the recovered lithic material (Gravettian); and an infinite date RTK-6445 >37,800 14C yr BP. In addition, a date from Layer 3 (RTD-7231B: 28,700 ± 180 14C yr BP, or 33,400–32,0670 cal BP)

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corresponds chronologically to the earliest Gravettian (Alex et al., 2019). Given that the lithic material is Gravettian and that two of four dates are consistent with it, especially since Pes-1 was recovered from the bottom of Layer 2, the specimen is best dated to the end of the MIS3. The second specimen (Pes-2) originated from the contact level between Layers 3 and 4, both of which contained Middle Palaeolithic artifacts. Radiocarbon dating of Layer 3 produced dates between 44.6 and 43.5 ka cal BP (Alex and Boaretto, 2014), while the layer was dated to 38.9 ± 2.5 ka according to ESR method (Blackwell et al., 2014). Therefore, Layer 3 also corresponds to MIS 3. Layer 4 is subdivided into three levels: Layer 4a, with a weighted mean age of 92 ± 4.4 ka; Layer 4b, with an average age of 102.4 ± 3.2 ka and which produced a Neanderthal molar (Pes-3); Layer 4c, with an average age of 117.4 ± 6.6 ka (Blackwell et al., 2014). According to Blackwell et al. (2018), Layer 4a was deposited during MIS 5b, while Layer 4b accumulated at the end of MIS 5c. Layer 4 also yielded a cave bear vertebra with ten subparallel grooves, which were probably made intentionally by hominins (Majkić et al., 2018). 2. Descriptions 2.1 Pešturina 1 (Pes-1) The specimen represents the left lateral mass of an atlas (C1), with upper and lower articular facets and a part of the anterior arch preserved; the transverse process is broken off and the posterior arch is completely missing (Fig. 3A, B). The anterior half of the upper articular facet exhibits pronounced postmortem erosion (cortical weathering). Age and sex cannot be assigned with certainty to a partially preserved vertebra, therefore the discussion provided here is only tentative. According to Scheuer and Black (2000), the principal centers of ossification of human C1 fuse by the sixth year of life; the atlas reaches close to its final adult size by 4–6 years of age; therefore, both growth and closure occur during the early childhood stage (as defined by Roksandic and Armstrong, 2011). Since the articular facets of Pes-1 lack the characteristic porosity of the surface observed in subadult individuals (Gómez-Olivencia et al., 2007), the individual was most likely an adult. While there are published regression equations and discriminant functions for sex determination based on the first vertebra (Marino, 1995), given the lack of population information, and fragmentary nature of the specimen, we did not attempt to assign sex to this individual. The tubercle for the insertion of the transverse atlantal ligament (located just below the medial margin of the upper articular facet) is well-developed and protrudes medially into the vertebral foramen, and can thus be described as ‘projected’ or ‘large’ following Gómez-Olivencia et al. (2007). No pathologies were observed on the specimen. Some measurements are provided in Table 1. 2.2 Pešturina 2 (Pes-2) The specimen represents a proximal to middle portion of a left radial shaft, starting from just below the area of the radial tuberosity (Fig. 4). The size of the specimen indicates a subadult individual in the late childhood stage of development (Roksandic and Armstrong, 2011). 3

Therefore, no sex can be assigned. The shaft displays multiple longitudinal cracks, as well as delamination (exfoliation) of the surface. A large portion of the outer cortical bone is missing from the lateral surface (around the area of the pronator teres insertion), and also a smaller portion from the posterior border. The bone surface exhibits discontinuous, amorphous patches of dull black mineral (manganese) deposition. Pes-2 exhibits a strong lateral curvature, although this might be exaggerated visually by the delamination of the lateral surface (Fig. 4). The nutrient foramen is clearly present on the anterior surface of the specimen, near the interosseous border (which is not particularly strong). In cross-section it displays a narrow medullary cavity and notably thick cortical bone when the young age of the specimen is considered (see measurements in Table 2 and cross-sections in Fig. 4). Pes-2 fragment also shows teardropshaped cross-sections, especially in the region where the interosseous crest is maximally developed (i.e. cross-section 2 in Fig. 4). 3. Discussion The limited number of measurable traits of the fragmentary Pes-1 atlas do not offer much in terms of taxonomic assessment. Pes-1 does not differ significantly from Neanderthal or Sima de los Huesos samples on any measurements (Table 1); it does differ significantly from the recent modern human sample at one measurement, the dorso-ventral length of the inferior articular facet (LAFDvD). Unfortunately, we were not able to statistically compare the Pes-1 measurements to those of Pleistocene modern humans due to the lack of solid reference data, as already noted by other researchers (e.g. Chikisheva et al., 2016). Chikisheva et al. (2016) report an Upper Palaeolithic atlas from Afantova Gora (Siberia) with a distinctly short inferior facet (13.8 mm) while Grine et al. (1998) report a similar atlas fragment from Middle Stone Age deposits at Klasies River Mouth with a notably long inferior facet (21.2 mm). The opposing extremes evidenced by these two comparative specimens suggest that Pleistocene modern humans expressed a high degree of variability in this measurement. The tubercle for the insertion of the transverse atlantal ligament is the only potentially taxonomically informative morphological trait that can be assessed in the Pes-1 specimen. The large projected tubercle of Pes-1 is similar to that most commonly observed in modern humans (see Fig. 3A and C). In contrast, weakly developed or small tubercles (Fig. 3D) dominate both Sima de los Huesos and later Neanderthal samples (Boule, 1911–1913; Gómez-Olivencia et al., 2007, 2013; Gómez-Olivencia and Been, 2019). Gómez-Olivencia et al. (2013) found large tubercles to be almost completely absent in their Neanderthal sample (only one of eight expressed a large tubercle on one side) and uncommon in the Sima de los Huesos sample (expressed bilaterally in two out of six); on the other hand, all modern human samples had high proportions of large tubercles (74-97%). The essentially modern morphology, along with the stratigraphic provenance (i.e. association with Gravettian artifacts), supports the attribution of the Pes-1 specimen to modern Homo sapiens.

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On the other hand, the limited preservation of the Pes-2 radial fragment and its non-adult age precludes a firm taxonomic attribution. The thick cortical bone of the radial shaft appears to be taxonomically non-informative. According to Rodríguez et al. (2016), Neanderthal left radial midshaft shows thicker cortical bone when compared to recent humans, though only when the measurements are not standardized by shaft length. However, it should be noted that the sample studied by Rodríguez et al. (2016) included only two radii (La Ferrassie 1 and La Chapelle-auxSaints 1), both from adult individuals. The narrow medullary cavity seen in the diaphyseal crosssections of Pes-2 is also reported in other Neanderthal specimens (e.g. Marillac 24; Garralda et al., 2014). The teardrop-shaped diaphyseal cross-section present in Pes-2 represents yet another feature cited as being characteristic of (adult) Neanderthal radii (e.g. Vandermeersch and Trinkaus, 1995; Garralda et al., 2014; Rodríguez et al., 2016). Other traits from the radius are considered to be distinct in Neanderthals: compared to the modern human radius, the Neanderthal radius displays a strong lateral curvature of the diaphysis, a well-developed proximal interosseous crest, a more medially placed radial tuberosity, a longer radial neck, and a more ovoid radial head, interpreted as reflecting a strong and cold-adapted short forearm (De Grote, 2011). The last three features cannot be observed on our specimen, while the interosseous crest is moderately expressed (possibly due to the non-adult age of the individual). Although lateral shaft curvature of Pes-2 cannot be evaluated using metrics (due to the specimen’s fragmentary nature), it does appear to be present, even pronounced. This might provide a hint towards a taxonomy of Pes-2 since Neanderthal adult radii are repeatedly reported as having more curved diaphyses relative to modern humans (Heim, 1982; Trinkaus, 1983; Vandermeersch and Trinkaus, 1995; Carretero et al., 1999), and this feature is known to occur even in non-adult Neanderthal specimens such as La Ferrassie 4, Le Moustier 2, Kiik-Koba 2, Cova Negra CN42165, and Kozarnika (Trinkaus et al., 2016; Tillier et al., 2017). The curved radial shaft is also found in various australopithecines (Ardipithecus ramidus, Australopithecus anamensis, Au. sediba) which indicates that it might represent a primitive trait (Pérez-Criado and Rosas, 2017). While the early members of the Neanderthal lineage from Sima de los Huesos also display markedly curved radial shafts (Arsuaga et al., 2015; Rodríguez et al., 2016), Homo antecessor shows long and straight radial diaphysis (Carretero et al., 1999), close to the condition seen in modern humans. 4. Conclusion In addition to the upper first molar from Pešturina Cave (Pes-3), which represents the first confirmed Neanderthal specimen from the territory of Serbia (Radović et al., 2019), two additional hominin fossil specimens were recovered from the cave’s strata: Pes-1 (an atlas fragment) and Pes-2 (a juvenile radius shaft). The fragment of the first vertebra (Pes-1) is consistent with modern human morphology. It originated from Layer 2, associated with a Gravettian lithic assemblage and dated to 31-29 ka cal BP (i.e. MIS 3). Although the juvenile radius (Pes-2) is too fragmentary to attempt a reliable taxonomic attribution, the apparently strong lateral curvature of the shaft is consistent with reported Neanderthal morphology. The

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date of Pes-2 is difficult to establish as it was found within the contact zone between Layers 3 and 4a, giving it a very wide age margin of 38.9 to 92 ka (i.e. between MIS3 and MIS 5b). Similar to Pes-3 molar, the radius shaft was found in association with Middle Palaeolithic tools. 5. Acknowledgments The authors would like to express their gratitude to Katerina Harvati (Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, Eberhard Karls University of Tübingen) for the µCT scanning of the atlas and radius fragments and her comments on an earlier version of this paper. We also wish to thank Ljubica Stajić (Faculty of Philosophy, University of Belgrade) for photographing the specimens. The work was supported by Natural Sciences and Engineering Research Council of Canada (grants nos. DDG-2017-00012, RGPIN2019-04113 and RGPAS-2019-00039) and Ministry of Culture and Information, and the Ministry of Education, Science and Technological Development of the Republic of Serbia (project no. 177023). References Alex, B., Boaretto, E., 2014. Radiocarbon chronology of Pešturina Cave, in: Mihailović, D. (Ed.), Palaeolithic and Mesolithic Research in the Central Balkans. Serbian Archaeological Society, Belgrade, pp. 39–49. Alex, B., Mihailović, D., Milošević, S., Boaretto, E. 2019. Radiocarbon chronology of Middle and Upper Paleolithic sites in Serbia, Central Balkans. J. Archaeol. Sci. Rep. 25, 266–279. https://doi.org/10.1016/j.jasrep.2019.04.010 Arsuaga, J.L., Carretero, J.M., Lorenzo, C., Gómez-Olivencia, A., Pablos, A., Rodríguez, L., García-González, R., Bonmatía, A., Quam, R.M., Pantoja-Pérez, A., Martínez, I., Aranburu, A., Gracia-Téllez, A., Poza-Rey, E., Sala, N., García, N., Alcázar de Velasco, A., Cuenca-Bescós, G., Bermúdez de Castro, J.M., Carbonell, E., 2015. Postcranial morphology of the middle Pleistocene humans from Sima de los Huesos, Spain. Proc. Natl. Acad. Sci. 112(37), 11524– 11529. Blackwell, B., Chu, S., Chaity, I., Huang, Y.E.W., Mihailović, D., Roksandic, M., Dimitrijević, V., Blickstein, J., Huang, A., Skinner, A.R., 2014. ESR dating ungulate tooth enamel from the Mousterian layers at Pešturina, Serbia, in: Mihailović, D. (Ed.), Palaeolithic and Mesolithic Research in the Central Balkans. Serbian Archaeological Society, Belgrade, pp. 21–38. Blackwell, B.A.B., Huang, C.L.C., Mihailović, D., Roksandic, M., Singh, I., Dimitrijević, V., Blickstein, J.I.B., Skinner, A.R., 2018. ESR dating Middle Paleolithic layers from Pešturina, Serbia. Geological Society of America Abstracts with Programs 50(6). Paper No. 275–3. https://doi.org/10.1130/abs/2018AM-319819. Boule, M., 1911–1913. L’homme fossile de la Chapelle aux Saints. Ann. Paléont. (Vert.) 6, 111– 172, 7, 21–56, 85–192; 8, 1–70. 6

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Tables Pes-1

SH mean (SD/n)1

NEA mean (SD/n)1

Recent modern mean (SD/n)2

Diameter in major axis of upper articular facet (UAFMAD)

(20.7)

23.4 (1.8/2) z = -0.09

24.1 (2.2/6) z = -0.56

23.49 (2.09/66) z = -0.66

Diameter at a right angle to the major axis of upper articular facet (UAFTrD)

(10.7)

11.6 (0.4/2) z = -0.15

11.4 (0.7/5) z = -0.33

10.27 (1.30/67) z = 0.16

Lower articular facet dorsoventral diameter (LAFDvD)

20.7

18.2 (0.3/2 z = 0.54

18.2 (1.4/5) z = 0.59

16.57 (1.52/66) z = 1.35

Lower articular facet transverse diameter (LAFTrD)

15.8

16.0 (0.8/2) z = -0.02

15.6 (1.6/5) z = 0.04

15.78 (1.09/65) z = 0.0

Measurement

Table 1. Linear atlas measurements (mm) of Pes-1 compared to extant and fossil human samples using an adjusted z-score method (Scolan et al., 2012); underlined adjusted z-score values lie outside the estimated 95% limit of variation expressed for each group. For each measurement, the sides with higher number of specimens was used; when the sample size was equal between right and left, the measurements for the left side were chosen. Data from Gómez-Olivencia et al. (2007: Table 6)1 and Gómez-Olivencia et al. (2013: Table 4)2. Measurement

Value

Anteroposterior (sagittal) shaft diameter at the most distal aspect

8.9

Mediolateral (transverse) shaft diameter at the most distal aspect

11.4

Anteroposterior (sagittal) shaft diameter at the fragment midpoint

9.3

Mediolateral (transverse) shaft diameter at the fragment midpoint

12.2

Anteroposterior (sagittal) shaft diameter at the most proximal aspect

9.3

Mediolateral (transverse) shaft diameter at the most proximal aspect

10.6

Maximum length of the fragment

104.0

Cortical thickness at anterior proximal point

3.2

Table 2. Measurements (in mm) of Pes-2 radial shaft fragment.

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Figures

Fig. 1. Location of Pešturina Cave in Serbia (A), ground plan and excavated area (B) and simplified stratigraphy (C), with red stars marking the positions of hominin fossils: Pes-1 (1), Pes-2 (2), and Pes-3 (3). Top to bottom stratigraphic sequence includes the following layers: Layer 1 (L1), loose humic silts with Bronze Age material; Layer 2 (L2), consisting of light brown fine-grained silt, containing Gravettian industry; Layer 3 (L3), made up mostly of compact brown fine-grained silt with a “Denticulate” Mousterian industry; Layer 4, with three sub-layers of unequal thickness, composed of reddish sediment with large rock fragments in places (4a), loose darker sediment (4b), and dark brown loose sediment with large rock fragments (4c), with Charentian-like Mousterian artifacts; Layer 5 (L5), consisting of greyish sandy sediment set above tufa.

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Fig. 2. The excavated level of squares O/10 and 11, with the red star marking the position of the Pes-1 atlas fragment in square O/11, quadrant d (A); the northern and eastern (to the right) profiles in square L/11, with the position (star) of the Pes-2 radius shaft (B).

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Fig. 3. Pešturina 1 (Pes-1) atlas fragment in cranial (A) and caudal (B) views, compared to atlases of a medieval Serbian female (C) and a Neanderthal from El Sidrón (SD-1605/1595 - D) in cranial views; the arrows point to the tubercles for the insertion of the transverse ligament; note well-developed tubercles (which protrude into the vertebral foramen) in Pes-1 and the modern human atlas, and weakly developed (small) tubercles in the Neanderthal specimen. Fig. 3D modified from Ríos et al. (2015, Fig. 3A).

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Fig. 4. Pešturina 2 (Pes-2) left radial shaft fragment in anterior (A), medial (B), posterior (C), and lateral (D) projections, with micro-CT cross-sections of the diaphysis (1, 2, and 3).

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Figure 5. Comparison of Pes-2 (A) radial shaft fragment with El Sidrón Neanderthal (B-D), and modern human (E) specimens, in anterior views; (A) Pes-2, (B) SD-1051b+SDR-153, (C) SDR051, (D) SDR-152 (flipped), and (E) a medieval Serbian adolescent. Figs. 5B-C modified after Pérez-Criado and Rosas (2017, Fig. 6).

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Declaration of interests ☐X The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: