A 51,000-year-old engraved bone reveals Neanderthals’ capacity for symbolic behaviour

While there is substantial evidence for art and symbolic behaviour in early Homo sapiens across Africa and Eurasia, similar evidence connected to Neanderthals is sparse and often contested in scientific debates. Each new discovery is thus crucial for our understanding of Neanderthals’ cognitive capacity. Here we report on the discovery of an at least 51,000-year-old engraved giant deer phalanx found at the former cave entrance of Einhornhöhle, northern Germany. The find comes from an apparent Middle Palaeolithic context that is linked to Neanderthals. The engraved bone demonstrates that conceptual imagination, as a prerequisite to compose individual lines into a coherent design, was present in Neanderthals. Therefore, Neanderthal’s awareness of symbolic meaning is very likely. Our findings show that Neanderthals were capable of creating symbolic expressions before H. sapiens arrived in Central Europe. The authors report an incised giant deer phalanx (toe bone), directly radiocarbon dated to at least 51,000 years old. The age and context of the object suggests that it was engraved by Neanderthals.

Since 2014, we have been conducting excavations inside the Jacob-Friesen Gallery, which have yielded six superimposed Middle Palaeolithic layers (D-I) beneath three archaeologically sterile ones (A-C) 51 . Radiometric dates suggest a Holocene age for layer A, an age of >47 ka cal bp for the A/B boundary, >47 ka cal bp for layer B, 54-65 ka bp (electron spin resonance) for layer D and 80-130 ka bp (electron spin resonance) for the earlier layers (E-I).
Excavations also have been undertaken at the prehistoric cave entrance, which is today sealed off by sediments and roof fall (area 4; Supplementary Information and Supplementary Figs. [1][2][3][4]. A first test trench was dug in 1988 (1 × 2 × 3.5 m), but it was not until 2017 that archaeological layers were discovered 51 . The cave roof is partially eroded, while the entrance is c. 3 m wide at the narrowest point. Collapsed roof material (rocks ≤50 cm) was present up to 2 m east of the exposed cave entrance. Sediments are preserved between the northern and the southern entrance walls, as well as along the adjacent slopes. The sediments consist of clayey silt with minor sand components, while weathering indices are high (Supplementary Information and Supplementary Fig. 5). They contain eroded roof material such as rocks and silt (layers 1, 4 and 7), material filled in through a roof cavity (layer 6), and material that sloped down from above the cave roof, followed by in situ weathering (layers 2, 3, 4.1 and 4.5). Layer 4.5 at the former cave entrance probably correlates with layer B inside the Jacob-Friesen Gallery, as both layers show similar sedimentary characteristics, such as grain size distribution, pH-value and mineral content (Supplementary Information and Supplementary Fig. 5).
Excavations at the cave entrance have yielded three non-diagnostic lithic finds ( Supplementary Fig. 2), a cortical flake (top of layer 3), a bladelet fragment with one central ridge (layer 4.5) and a further bladelet fragment with two parallel ridges (layer 7). The lithics are made of siliceous slate that is available from local river gravels 50 .
Bison (Bison sp.), red deer (Cervus elaphus), giant deer (Megaloceros giganteus (Blumenbach 1799)) and cave lions (Panthera spelaea) have been identified in layer 6, while most of the faunal remains from layer 4.5 are taxonomically assigned to bears (Ursus spelaeus; n = 29) and unidentified medium-sized mammals (n = 29; Supplementary Information and Supplementary Table 1). Furthermore, giant deer (M. giganteus; n = 12 including 10 teeth) and bos/bison (Bos/bison sp.; n = 10) have been identified in layer 4.5 ( Supplementary Fig. 6). Despite the small size of the excavated volume in layer 4.5 (1.1 m 3 ), faunal remains are abundant (number of individual specimens = 99). Anthropogenic modifications on layer 4.5 materials are present on bos/bison, giant deer (incised phalanx) and possibly red deer and cave bear bones (n = 17; Supplementary  Fig. 7). Carnivore modifications are frequent (n = 53); however, the degree of damage per specimen is minimal, and the majority of causative agents were small in size. Most of the faunal remains from layer 4.5 are well preserved with limited weathering, low fragmentation, and only a few examples of root etching (Supplementary  Table 2) resulting from rapid sedimentation soon after humans and animals had access to faunal remains.
Among the findings is the engraved giant deer second phalanx (inventory number 46999448-423; Fig. 1). The item was located near the west section of layer 4.5 that consists of brown to grey-brown clayey silt and contains pockets of small, edge-rounded dolomitic stones (1-2 cm diameter) and rocks (<10 cm diameter; Fig. 2 and Supplementary Fig. 4) position with a NNW-SSE orientation in one of the stone-rich pockets that grades into an underlying homogeneous sediment pocket (Supplementary Figs. 4 and 8).
The stone-rich pocket associated with the incised bone shows little evidence for sediment sloping, while the homogeneous sediment contains bones that show increased inclinations and multiple orientations. No indication of slope movement or water flow leading to mono-orientation 52 is observed, instead, the data suggest relatively little disturbance connected to the surroundings of the incised bone, whereas other parts of layer 4.5 and especially layer 6 show clearer signs of movement.
The engraved bone was discovered among an accumulation of cave bear bones, including a skull and two cervid shoulder blades piled on top of each other ( Supplementary Fig. 9). The engravings of the bone item were identified during the cleaning process.
The incised giant deer phalanx. The second phalanx of a giant deer (M. giganteus; length: 56.8 mm; width: 39.9 mm; thickness: 30.9 mm; mass: 36.1 g) with a comparable preservation to the other bones of the layer shows ten carvings on its sinistral side (Fig. 3).
The dominant line pattern consists of a set of six engravings that form five stacked offset chevrons. Sets of lines on either side run more or less parallel and intersect one another in an offset manner. Individual engravings meet at angles of between 92.3 and 100.5°, only engraving 1 has no physical connection to any other engraving (Supplementary Table 3). Line 4 truncates lines 2 and 3. Lines 3 and 6 are in parts preserved, which prohibits identification of a succession with either line 5 or with each other (Supplementary Information and Supplementary  Fig. 10). Lines 2 and 3 are thus older than line 4. Line lengths range from 13.2 (engraving 2) to 29.2 mm (engraving 4). A detailed investigation of engravings 1, 2, 4 and 5 shows that horizontal surfaces (that is, those parallel to the bone surface) are plain and continuous, whereas vertical surfaces of the same feature are often stepped and oblique (Figs. 3 and 4). This suggests that different carving techniques were used to create the two surfaces. Horizontal surfaces can be up to 6.  side (engravings 1-3) and from 66.8 to 102.3° on the right (engravings 4-6; Supplementary Table 2).
A second line pattern consisting of four short lines is located at the proximal end of the bone. Engravings 7-9 run more or less parallel with horizontal inclination angles of between 114 and 123°. Engraving 10 is set apart to the right side with an inclination angle of 98.7°. The lengths of these engravings range from 6.4 (engraving 8) to 10.6 mm (engraving 10).
The observed incisions substantially differ in location, depth and profile from well-known unintentional modifications (for example, butchering, percussion and trampling marks) [53][54][55][56][57] . Cut marks inflicted with lithics commonly create incision depths well below <100 µm, while the incisions on the modified bone are 10 to 50 times deeper. Common cut marks have V-to U-shaped profiles, whereas incisions 1-6 are L-shaped ( Supplementary Fig. 12). Also, unintentional modifications lack the horizontal plane adjacent to the vertical cut that is a typical feature of lines 1-6 ( Figs. 3 and 4).
Furthermore, the item is of no practical use. Its small size, convex surfaces and instability when lain on the ground prohibit efficient usage as a chopping board or a processing surface. Instead, the geometric pattern itself constitutes the central element. The six lines form two interlaced line sets (left side: lines 1-3; right side: lines 4-6) that each are composed of three parallel incisions. The parallel and regularly spaced engravings have comparable dimensions and were very probably created in a uniform approach suggesting an intentional act. Only the composition of individual lines results in a complex design. The use of a giant deer phalanx-a very impressive herbivore-as raw material emphasizes the special character of the modified item, particularly given the paucity of giant deer at 55-35 ka cal bp north of the Alps 58 , which further supports the notion of symbolic meaning.
Potential use-wear such as surface polish or chipping of projected areas ( Fig. 3 and Supplementary Fig. 10), which might indicate wearing, for example, as a pendant 59 , remains inconclusive as similar traces could have been inflicted by post-depositional processes, or during the engraving procedure. The base of the phalanx, on the other hand, is suitable as a platform on which the item stands upright, with the chevrons pointing upwards. This orientation is also suggested by the incisions at the base of the phalanx. A designation as a premeditated object that had symbolic meaning is thus the most plausible interpretation for the incised bone.
Experimental studies. To better understand the manufacturing process of the engraved item, a set of experiments was carried out and results have been compared with features observed on individual engravings (Supplementary Information, and Supplementary Figs. 13 and 14). By doing so, we aimed to address (1) which techniques were used to create the grooves; and (2) what the best conditions were to carve these grooves (carving time, groove depth, workability and success). Purpose-made blades of Baltic flint were used to manually carve five phalanges (phalanx media) of an 18-month-old Limousin cow by cutting (vertical planes) and scraping (horizontal planes). Each phalanx was treated differently: bone 1 was as fresh, bone 2 was room dried, bone 3 was open air dried, bone 4 was boiled once and bone 5 was boiled twice. A test of soaking bone in water to soften the cortical surface thus enabling an easier carving process was unsuccessful (Supplementary Methods).
The phalanges were handheld during the carving experiment, with their proximal end pointed towards the experimenter. The bone surface was first cut vertically at an approximate 90° angle (Fig. 5). Vertical cutting was performed in a back-and-forth motion similar to the use of a saw. This was followed by scraping of the adjacent horizontal surface towards the vertical cut. Whenever the resulting incision was not deep enough (~2 mm), the vertical surface was cut once again followed by a second phase of horizontal scraping. The repetition of the two techniques resulted in engravings of up to 2 mm depth that bear steep, sometimes stepped vertical edges associated with a wider horizontal surface ( Supplementary Fig. 14). Two blades were used to make each incision as their edges became dull within just a few minutes, seemingly depending on bone pre-treatment-sooner with dried bones and later with cooked bones.
To create grooves with a depth of 2 mm, once or repeatedly boiled bones (bones 4 and 5) appear to be the material of choice. They offer a mellow surface and provide enough firm grip to easily handle the tool. Less suitable are dried bones (bones 2 and 3) with soft tissue remains, as steady working of the surface is almost impossible and the bone tissue remains notably harder. Fresh bone (bone 1) seems to be unsuitable, as remaining fresh soft tissue makes the surface greasy and slippery thus leading to total loss of tool control. Similar issues were noticed when decaying bone was cut during experiments 60 .
In conclusion, the use of boiled bones seems the most likely option to create controlled grooves with depths of c. 2 mm in a relatively short time (c. 10 mins each; Supplementary Tables 5 and 6). The carvings on the giant deer phalanx from Einhornhöhle thus could have been made within c. 1.5 h. A combination of cutting and scraping has proved a successful working method and the experimental traces closely resemble those observed on the engraved item. There was no (macroscopically) visual difference between fresh and boiled bone. The profiles of lines 2-5 plunge steeply, after reaching the base of the cut they ascend sharply forming a micro-concavity, whereupon they descend slowly forming a micro-convexity (Figs. [3][4][5]and Supplementary Figs. 12,15 and 16). It can be hypothesized that this pattern results from scraping and was caused by differently applied pressure and/or numbers of repetitions, whereby areas near the vertical surface had been engraved deeper than more distant ones. This can explain the rippled horizontal surface of the deepest incision, line 3, alternatively, different tools/gestures might have been applied. Line 6 is incomplete, but its partially preserved horizontal surface compares well to the surfaces achieved by the experiment.
Rounding and chipping of vertical edge summits, a phenomenon that was also observed during the experiment, might have been caused during the carving procedure.
Radiometric dating. Nine samples from layers 4.5 and 6 were submitted for radiocarbon dating, consisting of three charcoal samples, two non-modified bones, three cut-marked bones and the engraved giant deer phalanx (Supplementary Table 7 Supplementary Fig. 15.    Supplementary Fig. 16. Applying a wider probability range of 95.5%, the minimum calendar age is set at 47.5 ka cal bp, while the older calendar age extends outside the range of the IntCal20 dataset, even implying the possibility of a calibrated age beyond 55 ka cal bp. Two charcoal dates from the same layer delivered infinite age estimates of >47 ka cal bp (Poz-118511: >45 ka bp) and >48 ka cal bp (Poz-119359: >46 ka bp). They corroborate the date of the incised phalanx from the same layer. A younger date of 34.3 to 33.4 ka cal bp (MAMS-45842: 29.3 ± 180 ka bp) comes from an animal jaw fragment that was found above the incised bone in layer 4.5 close to layer 3 (Fig. 2). The jaw does not bear any signs of human processing.
Two cut-marked bones from the underlying layer 6 also delivered infinite dates of >47 ka cal bp (GrM-22136 and GrM-22137: >45 ka bp). A third date on a pine charcoal from this layer equally delivered an infinite age of >49 ka cal bp (Poz-120035: >47 ka bp).
All radiocarbon dates yielded results near or beyond the radiocarbon boundary. They are in good agreement with their stratigraphic order. Only the jaw bone (MAMS-45842) from above the giant deer phalanx (KIA-55192) yielded a deviating age that might best be explained by the very low collagen content (0.2%; Supplementary Table 6) and/or minor contamination generally resulting in much younger age estimates 63 .
In conclusion, the humanly modified phalanx is directly dated and, along with the other radiocarbon dates that are beyond the radiocarbon limit, strongly suggests that the artefact is least 51,000 years old (Supplementary Table 8 and Supplementary Fig. 17).

Discussion
The engraved giant deer phalanx from Einhornhöhle displays a geometric line pattern consisting of two interlaced line sets, each with three parallel lines. A secondary pattern consists of four short lines. The complex production process leading to the creation of the incisions, their systematic arrangement and the scarcity of giant deer north of the Alps, support the notion of an intentional act and of symbolic meaning. Besides the engraved bone from Einhornhöhle, a few bone and rock items with geometric line patterns have been reported from other Middle Palaeolithic contexts that may serve as comparison 30,[41][42][43][44][45][46] (Supplementary Table 9). The materials used as 'canvases' are diverse, including cortical flint, bedrock, tooth and bone. Incisions and engravings on bones have been performed on a range of anatomical body parts coming from animals such as raven, saiga antelope, aurochs and horse. Geometric patterns range from # shapes over zig zags to parallel incisions and circles. In that context, the phalanx from Einhornhöhle with its stacked offset chevrons represents one of the most complex cultural expressions in Neanderthals known so far.
The question remains whether Neanderthals at Einhornhöhle could have been influenced by H. sapiens when creating the carved bone. The earliest evidence for the presence of H. sapiens in Central Europe comes from several sites in the Upper Danube area, some 400 km to the south 1,3,5,9-13 . They provide early ages of 43.5 to 38 ka cal bp, that is, several millennia after the engraved item from Einhornhöhle was deposited. The earliest H. sapiens fossils in remaining Europe come from Southeast Europe, some 1,500 km from Einhornhöhle 14,64,65 . They delivered a maximum age of 45.5 ka cal bp. The geographic and temporal gaps, and the absence of comparable items from early Upper Palaeolithic contexts, make a direct influence improbable. An independent Neanderthal authorship for the engraved bone is thus the most plausible scenario.
The cognitive capacity for creative expressions and social behaviour among early H. sapiens has been acknowledged for a long time. In contrast, evidence for symbolic behaviour among early hominins 66 and Neanderthals has remained far more elusive and its independence from H. sapiens has often been contested. The engraved bone from Einhornhöhle supports the idea of symbolic behaviour among Neanderthals before the arrival of H. sapiens in Central Europe. The cultural influence of H. sapiens as the single explanatory factor for abstract cultural expressions in Neanderthals can no longer be sustained 67 .

Analyses of the engraved bone.
To better understand the character of the engravings of the giant deer phalanx, the find was subjected to macroscopic and microscopic inspections (three domensional (3D) reflected light microscopy), as well as micro-CT scanning.
Micro-CT scanning was performed by Waygate Technologies GmbH with the aid of a phoenix V│tome│xm micro-CT scanner. Scanning time was c. 1.25 h. The acquired micro-CT data were processed in VGSTUDIO MAX 3.3.4. Colour images were produced to visualise the bone's surface from six standard perspectives. Greyscale images were produced for their higher contrast, allowing us to illustrate details of the engraved surfaces and to optimally present technical information. The lengths, profile depths and internal angles of all incisions were manually measured in VGSTUDIO MAX 3.3.4. Profile angles were measured at the mid-point of the total incision length, and again at 30% and at 70% of the total length. Accordingly, incision depth was measured at the mid-point.
The 3D reflected light microscope Keyence VHX-5000 (Keyence, Neu-Isenburg, Germany) was used for non-destructive, high depth-of-field and 3D images at different magnifications. To examine the engravings of the bone, images of the observation fields were captured at magnifications of ×20, ×50 and ×100. At these magnifications, images in 2D and 3D were taken by means of single image capture and image stitching. Up to 36 individual images were combined to create a stitched image. With the use of such 3D images, topographic profiles of the six engravings were produced. The cross-sectional profile-line measurements were conducted by a straight line intersecting the engravings perpendicularly. The measurement position was displayed by a profile graph in the respective images. Table 7). All laboratories apply rigorous pre-treatment and dating protocols that do, however, differ in detail (Supplementary Methods). The samples were obtained from two layers that hold the majority of cut-marked bones, that is, layers 4.5 and 6 ( Fig. 2 and Supplementary Fig. 4). Cut-marked bones and charcoal were preferred for radiocarbon dating. All charcoal samples were cleaned under a binocular microscope before submission and were identified as pine (Pinus sylvestris).

Radiometric dating. Nine samples (3 charcoal, 6 bone) were 14 C dated by accelerator mass spectrometry (AMS) at four different laboratories (Supplementary
The samples from layer 4.5 were selected according to their proximity to the incised bone ( Fig. 2 and Supplementary Fig. 4). One charcoal and two bone samples came from stratigraphic positions above the engraved find (Poz-118511, MAMS-45842 and MAMS-4584). A charcoal and a bone sample were obtained from below the item (Poz-119359 and GrM-x). The modified phalanx was also sampled for absolute dating (KIA-55192). In addition, one charcoal and two bone samples from layer 6 were dated (Poz-120035, GrM-22136 and GrM-22137).
All radiocarbon dates were calibrated with the OxCal 4.4.2 software using the IntCal20 atmospheric curve 61,62 . We also calibrated infinite ages for comparative reasons. To provide a minimum age estimate for them, a theoretical standard deviation of 1,000 radiocarbon years was computed in OxCal 4.4.2 (a similar approach is taken by some radiocarbon labs, such as the Centre for Isotope Research in Groningen). For graphic illustrations the calibrated age ranges were consequently cut off at the minimum age boundary, for example, at 47,000 cal bp for a radiocarbon date >45,000 (Supplementary Fig. 17).

Statistics
For all statistical analyses, confirm that the following items are present in the figure legend, table legend, main text, or Methods section.

n/a Confirmed
The exact sample size (n) for each experimental group/condition, given as a discrete number and unit of measurement A statement on whether measurements were taken from distinct samples or whether the same sample was measured repeatedly The statistical test(s) used AND whether they are one-or two-sided Only common tests should be described solely by name; describe more complex techniques in the Methods section.
A description of all covariates tested A description of any assumptions or corrections, such as tests of normality and adjustment for multiple comparisons A full description of the statistical parameters including central tendency (e.g. means) or other basic estimates (e.g. regression coefficient) AND variation (e.g. standard deviation) or associated estimates of uncertainty (e.g. confidence intervals) For null hypothesis testing, the test statistic (e.g. F, t, r) with confidence intervals, effect sizes, degrees of freedom and P value noted Data Policy information about availability of data All manuscripts must include a data availability statement. This statement should provide the following information, where applicable: All studies must disclose on these points even when the disclosure is negative.

Study description
The study deals with an engraved giant deer toe bone bearing systematic engravings. Radiometric data shows its association with Neanderthals some 51,000 years ago. Micro CT-scans and 3D digital microscopy illustrate the properties of individual engravings. Experimental studies suggest that the bone was carved in a two-step approach and that planning depth was prerequisite. We discuss the meaning of the object in connection with Neanderthals cognitive abilities and its independence form Homo sapiens.

Research sample
The bone item is a single find. However, comparisons are made with further known finds across Eurasia that imply symbolic expressions in Neanderthals.

Sampling strategy
Bone item: The bone item is a single find. Radiocarbon dates: The sampling strategy is described in the main text and the supplement, especially for the engraved bone. Sediment samples: These were taken from the main inplaces profile where no rocks were visible. The aim was to obtain two samples per layer to ensure within-layer consistency

Data collection
On-site data was collected using a total station. Finds and features were recorded in writing, by photographs, drawings and SfM imagery. The microCT-Scans were performed by Waygate Technologies GmbH, a commercial lab. 3D digital microscopy was performed by Tim Koddenberg. Bones and charcoals were selected by Thomas Terberger and Dirk Leder and then submitted to the various labs for radiocarbon sampling and dating. Sediment samples were collected by Dirk Leder during the final week of excavation and processed by Philipp Hoelzmann. The carving experiment was performed by Raphael Hermann and Dirk Leder and empirical data was collected based on observations and discussion.
Timing and spatial scale The relevant samples were taken from a small area measuring about 1.5 x 1.5 x 1.0 metres. The duration of the excavation was 8 weeks in August/September 2019 and five weeks in 2020. Post-excavation processing commenced thereafter. Samples for radiometric dating were submitted between November 2019 and May 2020. Sediment samples were submitted in November 2019. Delays in processing are due to the Covid-19 pandemic and its effects.

Data exclusions
No data was exluded.

Reproducibility
We conducted an experiment on cattle bones to better understand the procedure involved in creating the engravings observed on the original find. Applying a cut-and groove technique, we were able to create about eight engravings on differently pretreated bones. The protocol for radiocarbon dating is outlined in the methods secition of the manuscript and detailed in the supplement. A comparative study can be found in Hüls et al. 2017 Randomization not applicable Blinding Blinding was not applied when carving the bones as the experimentators aimed to create engravings that appear similar to those observed on the original piece.
Did the study involve field work?

Yes No
Field work, collection and transport

Field conditions
The excavtion took place in a mid-latitude broad-leafed forest during summer in front of a former cave entrance that was partially eroded. Weather was mostly sunny, but there were some rainy days. The excavation area was complety sheltered by a white plastic foil roof.

nature research | reporting summary
April 2020 Experiments of concern Does the work involve any of these experiments of concern: No Yes Confirm that both raw and final processed data have been deposited in a public database such as GEO.
Confirm that you have deposited or provided access to graph files (e.g. BED files) for the called peaks.

Data access links
May remain private before publication.
For "Initial submission" or "Revised version" documents, provide reviewer access links. For your "Final submission" document, provide a link to the deposited data.

Files in database submission
Provide a list of all files available in the database submission.
Genome browser session (e.g. UCSC) Provide a link to an anonymized genome browser session for "Initial submission" and "Revised version" documents only, to enable peer review. Write "no longer applicable" for "Final submission" documents.

Methodology Replicates
Describe the experimental replicates, specifying number, type and replicate agreement.

Sequencing depth
Describe the sequencing depth for each experiment, providing the total number of reads, uniquely mapped reads, length of reads and whether they were paired-or single-end.

Antibodies
Describe the antibodies used for the ChIP-seq experiments; as applicable, provide supplier name, catalog number, clone name, and lot number.
Peak calling parameters Specify the command line program and parameters used for read mapping and peak calling, including the ChIP, control and index files used.

Data quality
Describe the methods used to ensure data quality in full detail, including how many peaks are at FDR 5% and above 5-fold enrichment.

Software
Describe the software used to collect and analyze the ChIP-seq data. For custom code that has been deposited into a community repository, provide accession details.

Flow Cytometry
Plots Confirm that: The axis labels state the marker and fluorochrome used (e.g. CD4-FITC).
The axis scales are clearly visible. Include numbers along axes only for bottom left plot of group (a 'group' is an analysis of identical markers).
All plots are contour plots with outliers or pseudocolor plots.
A numerical value for number of cells or percentage (with statistics) is provided.

Sample preparation
Describe the sample preparation, detailing the biological source of the cells and any tissue processing steps used.

Instrument
Identify the instrument used for data collection, specifying make and model number.