Evidence for interpersonal violence in the St. Ce´saire

Christoph P. E. Zollikofer*†, Marcia S. Ponce de Leo´ n*, Bernard Vandermeersch‡, and Franc¸ois Le´ veˆ que§

*Anthropological Institute and MultiMedia Laboratory͞Department of Computer Science, University of Zu¨rich, 8057 Zu¨rich, Switzerland; ‡Laboratoire d’Anthropologie, Universite´de Bordeaux I, 33405 Talence, France; and §Re´sidence Charles Perrault, 3, Rue de Provence, 86000 Poitiers, France

Communicated by Erik Trinkaus, Washington University, St. Louis, MO, February 26, 2002 (received for review December 1, 2001) The St. Ce´saire 1 Neanderthal skeleton of a young adult individual derive from a spatially confined area with a diameter of no more is unique in its association with Chaˆtelperronian artifacts from a than 70 cm (1). The excavation yielded no signs of a burial pit; level dated to ca. 36,000 years ago. Computer-tomographic imag- yet the local inhomogeneity in the distribution of rocks and ing and computer-assisted reconstruction of the skull revealed a implements at the spot where the skeleton was found, as well as healed fracture in the cranial vault. When paleopathological and its association with Dentalium shells (10), may be indicative of an forensic diagnostic standards are applied, the bony scar bears intentional burial (11). The postcranium is represented by direct evidence for the impact of a sharp implement, which was fragments of the axial skeleton and the limb bones, some of presumably directed toward the individual during an act of inter- which were found in anatomical connection. The skull was lying personal violence. These findings add to the evidence that Nean- on its right side, with the upper and lower jaws in anatomical derthals used implements not only for hunting and food process- association. Most of the preserved cranial structures come from ing, but also in other behavioral contexts. It is hypothesized that the right side and comprise the mandible and maxillae (up to the the high intra-group damage potential inherent to weapons might left lateral incisors), the face, and the right anterolateral region have represented a major factor during the of hominid of the braincase. The internal lamina of the cranial vault bones social behavior. is partially eroded, and with the exception of several isolated teeth, the left cranial half is missing (Fig. 1). Deterioration and Chaˆtelperronian ͉ paleopathology ͉ tool use ͉ trauma ͉ computer tomography loss of these elements is probably because of temporary exposure and weathering of the upper layers of the sediment in which the fossil was embedded (1). he St. Ce´saire 1 Neanderthal partial skeleton was discovered The physical reconstruction of the fragmented right hemi- Tin 1979 at the site of La Roche a`Pierrot (near the village of mandible and skull was performed by one of us (B.V.) and St. Ce´saire, Charente Maritime, France), a collapsed rock shelter revealed taphonomic deformation of the face relative to the comprising a sequence of Mousterian, Chaˆtelperronian, and braincase, resulting in an everted position of the cranial vault Aurignacian deposits (1). The skeleton was recovered from level relative to the midplane of the skull. As an effect of the general EJ0P (1), which contains a Chaˆtelperronian assemblage ther- flattening of the cranial morphology, the anatomical connec- moluminescence-dated to Ϸ36,000 years ago (2, 3). This ensem- tions between larger reconstructed pieces remained inconclu- ble represented the first direct evidence for the association of sive. Among these was an apical vault fragment representing with Chaˆtelperronian implements. Together with substantial portions of the right frontal and parietal bones joined a similar association from the site of Arcy-sur-Cure (4), these finds spurred an intense and ongoing debate over the evolution- along the coronal suture. This fragment is delimited by post- ary, paleodemographic, and cultural relationships between local mortem fractures on its anterior, posterior, and lateral sides (Fig. Neanderthal populations and the early modern (EMH) 1). The medial margin, however, exhibits a smooth border, which newcomers during the early Upper Paleolithic in Europe. extends in an anteroposterior direction across the coronal suture The St. Ce´saire 1 skeleton is fragmented and partially eroded, and was initially interpreted as representing the partially fused but the reconstructed craniomandibular and long bone diaphy- sagittal (interparietal) and metopic (interfrontal) sutures. seal morphology permitted significant inferences regarding the To correct the taphonomic deformation of the skull and phyletic status and behavioral specializations of this individual. re-assess the anatomical position of this piece, we performed a The craniomandibular morphology of the specimen largely computerized reconstruction of the skull. Virtual reconstruction corresponds to the ‘‘classical’’ Neanderthal type (5). Tooth was indispensable because the brittleness of the original fossil microwear analysis suggests a meat-rich diet comparable to that material prevented physical disassembly and manipulation of the of earlier Neanderthals and modern hunting societies (6). The specimen. Following three-dimensional data acquisition with morphology of the well-preserved right femoral shaft indicates computer tomography (CT), all fragments were isolated elec- Neanderthal-type hyperarctic body proportions, but cross- tronically from filling material and then recomposed on the sectional biomechanical analysis suggests locomotor patterns computer screen, according to procedures and criteria described closer to those of EMH than of classic Neanderthals (7). in ref. 12 (a detailed account of the new reconstruction will be Here we report on recently discovered paleopathological given elsewhere). One result was that the medial border of the aspects of the morphology of the fossil. During computer- isolated cranial vault piece clearly does not correspond to the assisted reconstruction of the skull, we detected a healed frac- midsagittal plane of the skull (Fig. 1), nor does it represent ture in the cranial vault. When paleopathological diagnostic normal cranial at its true position lateral of the standards (8, 9) are applied, this bony scar bears direct evidence midsagittal plane. for the impact of a sharp implement, which may have been We established a differential diagnostic scheme, according to directed toward the individual during an act of interpersonal which this unusual morphology, its underlying causes, and violence. We discuss the possible behavioral context of this evidence and its implications for hominid behavior during the Middle-to-Upper Paleolithic transition in Europe. Abbreviations: EMH, early modern human(s); CT, computer tomography. †To whom reprint requests should be addressed. E-mail: zolli@ifi.unizh.ch. Materials and Methods The publication costs of this article were defrayed in part by page charge payment. This The St. Ce´saire skeletal remains belong to a young adult, possibly article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. male, individual. All preserved cranial and postcranial elements §1734 solely to indicate this fact.

6444–6448 ͉ PNAS ͉ April 30, 2002 ͉ vol. 99 ͉ no. 9 www.pnas.org͞cgi͞doi͞10.1073͞pnas.082111899 Downloaded by guest on September 30, 2021 margin (Fig. 1) exclude that it represents parts of the interpa- rietal and a supposed metopic suture. On the other hand, a presumed suture in parasagittal position would imply the exis- tence of a large persisting fontanelle or a bregmatic ossicle (15). However, the fairly straight margin does not correspond to a border around a fontanelle or a suture around a bregmatic ossicle. Furthermore, the cross-sectional structure of the bone clearly differs from that of an interosseous suture, which exhibits a corrugated border with less dense cortical bone than the border of a healed wound (Fig. 3). The most probable cause of the observed morphology is therefore bone regeneration following a lesion, a scenario that is corroborated by the close match of the cross-sectional morphology of the St. Ce´saire fragment (Fig. 3a) with that of comparative specimens exhibiting healed trepana- tions and scars (Fig. 3 b, e, and f). In a next step, we analyzed the morphology of the injury with the aim to infer the proximate mechanical causes of the lesion and to reconstruct its posttraumatic history. As evidenced by the nearly straight border of the scar, the individual most probably suffered a lesion from a blade-shaped object. The resulting slash in the cranial vault is preserved on its right (lateral) side over a length of 68 mm; it was probably slightly longer in vivo. The left (medial) side of the groove was lost during fossilization. Judging from the degree of bone remodeling along the margin, the injury reached its greatest depth near the coronal suture, correspond- ing to the presumed primary site of impact. Toward the anterior and posterior ends, the groove tapers off. This morphology most

closely matches the pattern of direct, sharp trauma. Under these biomechanical conditions, the high but localized stresses caused by the impacting object lead to puncturing͞cutting of the scalp and the external lamina of the bone, comminution of the diploe¨, and separation͞displacement of bone fragments from the in- ternal lamina (9). The St. Ce´saire specimen in fact bears evidence that at the primary site of the impact the internal lamina was fractured and parts of it were dislocated whereas, toward the periphery of the slash, it was only partially severed Fig. 1. Computerized reconstruction of the St. Ce´ saire 1 Neanderthal skull (Figs. 1 and 2). The interpretation of the slash as a linear (mirror-imaged completed parts are transparent) showing the bony scar in the fracture resulting from blunt trauma is a less likely scenario right apical cranial vault. The skull is seen from the direction in which the because the compressive forces induced by blunt objects lead hypothetical blow was exerted. Arrows indicate the anteroposterior (a and p) to nonlocal deformation of the cranial vault, typically resulting extent of the preserved lateral border of the injury (c, coronal suture; b, in multiple radial and tangential fractures around the center of bregma; *, location of the coronal cross section through the injury (see Fig. 2b); .(؋, location of the parasagittal cross section through the coronal suture (see impact (9, 16 Fig. 3c); the dotted line indicates the reconstructed position of the midsagittal Comparison with an archeological specimen exhibiting a plane of the cranial vault). Note oblique, off-midline position of the scar. healed slash on the frontal bone permits further inferences (Scale bar ϭ 5 cm.) regarding the severity of the injury and the subsequent healing process (Fig. 2). Given the moderate depth of the St. Ce´saire scar, it appears that the lesion was relatively mild. Cross-sectional behavioral context could be studied at increasing levels of detail CT images (Figs. 2 and 3) show that the injured region was (Table 1). For the comparative analysis of the external and extensively remodeled during lifetime; the severed external internal structure of the bone, we used a sample of adult lamina was smoothed out by bone resorption and deposition, and specimens comprising (i) an archeological specimen exhibiting a the dislocated parts of the internal lamina were fixated, probably healed slash resulting from sharp trauma to the cranial vault through formation of connective tissue in the diploic region. The (13), (ii) three specimens with healed trepanations [one neolithic external and cross-sectional morphology of the injured region (14) and two modern skulls], and (iii) four specimens exhibiting does not show any signs of post-traumatic infection (e.g., peri- metopic sutures and͞or persisting fontanelles. ostitis or osteomyelitis), and the degree of healing is relatively advanced. Considering that bone healing is visible only 2–3 Paleopathology weeks after a traumatic event (9), it can be concluded that the The medial border of the cranial vault fragment of the St. Ce´saire individual survived the injury for at least some months, such that Neanderthal deviates in its external and internal structure from a direct causal connection between the trauma and the individ- both postmortem fractures and interosseous sutures. The exter- ual’s death is unlikely. nal lamina of the bone is rounded off toward the medial margin, and the diploic region is covered with cortical bone (Fig. 2). This Behavioral Context morphology is characteristic of in vivo apposition of bone matrix By using forensic criteria originally developed for trauma anal- and excludes postmortem abrasion and erosion as potential ysis in extant and archeological populations (9), it is possible to mechanisms. Bone apposition at structural boundaries may conceive of various scenarios under which the St. Ce´saire injury occur under two different circumstances: normal periosteal could have occurred, assess their relative likelihood, and discuss growth in sutural tissue and bone regeneration following an their behavioral and motivational implications. The anteropos- injury. The off-axis position and oblique orientation of the terior orientation of the slash as well as its apical position are

Zollikofer et al. PNAS ͉ April 30, 2002 ͉ vol. 99 ͉ no. 9 ͉ 6445 Downloaded by guest on September 30, 2021 Table 1. Differential diagnostic scheme for trauma analysis in fossil hominids Criterion* Range of possible alternatives

Paleopathology, proximate causes Incident In vivo • Postmortem Etiology Trauma • Pathology Epigenetic variant Type of trauma Direct • Indirect Type of lesion Penetrating, sharp • Blunt Severity of trauma Mild • Fatal Post-traumatic Complete healing • Chronic impairment Object causing lesion Implement • Natural object Implement type Stone ? Wood Forensics, ultimate causes Behavioral context Intentional • Accidental Motivation Aggression • Ritual Medical Action Casual (short-term) • Premeditated (long-term) Actor Opponent • Self-infliction Social context Intragroup • Intergroup (intra-͞interspecific) Recovery Autonomous • Supported (nursing)

The position of the • represents the inferred status of St. Ce´ saire between alternatives. *Compiled after refs. 8, 9, 16, 18, and 19.

indicative of a blow or a thrust exerted against the individual forensic evidence suggests that accidental trauma typically af- from the front or from behind, assuming that the individual was fects the sides of the cranial vault, as opposed to the apical in an upright position. These spatial relationships indicate an location of intentional injuries (16). intentional action, effected with an implement rather than a Inferences regarding the nature of the implement, the agents natural object. Accidental injury, such as falling onto a sharp causing the lesion, and the behavioral context must remain edge, a rockfall, or an unintentional blow, such as resulting from tentative. From a mechanical point of view, the severity of sharp a hunting incident, are less likely explanations; comparative trauma depends on the mass, impact velocity, and incisiveness of the weapon. The wide range of possible combinations of these

Fig. 2. Anatomy of a blow. (a) Mediolateral view of the right border of the St. Ce´ saire 1 cranial vault injury (same symbols as in Fig. 1: a and p, anterior and posterior delimitations of the scar, c, position of the coronal suture, and *, location of the cross section in b. The drawing indicates areas of bone Fig. 3. Comparative cross-sectional morphology of bone injuries and su- remodeling (gray) and areas affected by postmortem fracturing (hatched). (b tures. (a and b) Healed scars of St. Ce´ saire 1 and a medieval specimen (same and c) Comparative morphology of the injured vault bones in St. Ce´ saire 1 (b) coronal sections as in Fig. 2 b and c). (c) St. Ce´ saire 1 coronal suture (parasag- and a specimen from a medieval graveyard (13) exhibiting a healed scar ittal section through ؋ in Fig. 1). (d) Metopic suture in a recent specimen resulting from sharp trauma on the left frontal bone (c) (both specimens in (coronal section). (e) Large occipital trepanation during early phases of heal- anteroposterior view, coronal cross sections); the CT sections show bone ing [Ensisheim skull (14), coronal section]. ( f) Healed occipital trepanation in remodeling at the margin of the injured external lamina (*) and a space (‚) a recent specimen (coronal section). Note apposition of dense cortical bone at between the dislocated internal lamina and the diploe¨ , probably filled by the injured borders, resulting in a smooth contour, as opposed to the less connective tissue. (Scale bar ϭ 5 cm.) dense and corrugated aspect of the sutural borders. (Scale bar ϭ 5 cm.)

6446 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.082111899 Zollikofer et al. Downloaded by guest on September 30, 2021 parameters encompasses a correspondingly wide spectrum of lesions (21, 24), it is worth noting that immature specimens of implements that might have been used to inflict the wound. For Neanderthals [Devil’s Tower and Le Moustier (25, 26) and EMH example, the Chaˆtelperronian stone tools recovered from the (Qafzeh 11)] also bear evidence for craniofacial trauma. The site of St. Ce´saire are relatively small and exhibit retouched, elevated frequency of trauma might therefore reflect not only a blunt edges. To attain the kinetic energy necessary to penetrate high risk of injury during close-quarter hunting of medium to bone, considerable acceleration, probably through hafting (17), large-sized game (21), but a physically demanding and stressful would have been essential. Implications regarding the nature of life from early ontogenetic stages (27, 28). the weaponry are complicated by the fact that the function of Against this comparative background, the dearth of direct Chaˆtelperronian implements is poorly understood and the pre- evidence for tool involvement in fossil hominid trauma may be served stone industry probably represents a small fraction of the interpreted in two different ways. On one hand, it may reflect a actual in vivo spectrum of available tools. low in vivo frequency of intentional or accidental tool-inflicted Comparative evidence from historical populations suggests injuries relative to other types of trauma. It also may reflect the that interpersonal conflict behavior resulting in cranial vault limits of paleopathological diagnosis; in a fossil, a lesion induced fractures is relatively frequent (18, 19). Given the characteristic by an implement can be recognized only if evidence of healing apical location of the injury in St. Ce´saire, direct interaction with is still present postmortem and the morphology of the scar another individual is the most parsimonious scenario. Theoret- permits inferences regarding the responsible weapon. The prob- ically, the injury may have resulted from intragroup, intergroup, ability of detecting such injuries is further reduced through the or even interspecific conflict behavior. The first scenario is the effects of diagenesis, which tends to degrade the paleopatho- most likely one because in socially organized species the vast logical evidence (9). Following this line of argument, a relevant majority of interpersonal interactions occur at the within-group proportion of the nondiagnostic injuries may represent tool- level (20). Population densities were low during the Late Pleis- induced trauma and͞or may be seen in the context of interper- tocene, such that mutual avoidance during the rare encounters sonal violence rather than accident. between different groups (both intra- and interspecific) might Data from nonhuman primates indicate that interpersonal have represented the optimum strategy for the resolution of violence within social networks represents a major cause of potential conflict (21). Nevertheless, it must be considered that trauma. For example, in the Gombe chimpanzees more than patchy resource distribution might have induced temporary one-half of the observed skeletal lesions are fractures and bite between-group competition. wounds resulting from intragroup violence (24), and several

Another aspect that requires consideration is the motivational cases of fatal outcome of intragroup clashes have been reported ANTHROPOLOGY background of the conflict in which the St. Ce´saire Neanderthal in both wild and captive chimpanzee groups (29). A question was involved. Motivations may range from a premeditated arises whether there is evidence of tool use in interpersonal assault to a brief argument emerging from a temporary conflict conflict situations in nonhuman primates. The cultural variabil- between individuals, such as over social status, access to poten- ity and contextual diversity of tool production and use have been tial mates, or intragroup resources. Overall, a likely scenario for studied extensively in various primate communities (30–32), the interpersonal violence in St. Ce´saire is intragroup tempers revealing a general behavioral basis to aim objects, but not tools, with available ‘‘weaponry.’’ The immediate effects of the trauma toward conspecifics in the context of conflict behavior. However, were probably serious, implying heavy bleeding, cerebral com- although object-throwing to intimidate group members is fairly motion, and temporary impairment. Although it is possible that common (30, 33), the purposeful and directed use of tools the individual sustained these adverse effects autonomously, it designed for a distinct function during acts of interpersonal can be assumed that it had benefited at least to some extent from violence has not been reported. On the basis of the currently initial intragroup assistance. available evidence, it appears therefore that hominids differ from nonhuman primates in their ability to produce and use tools Discussion in an expanded, multifunctional context, including conflict be- The St. Ce´saire cranial injury adds to the extremely small sample havior. Accordingly, the St. Ce´saire 1 and Shanidar 3 wounds of specimens bearing direct evidence that Neanderthals used indicate that Neanderthals transformed a ‘‘tool’’ into a ‘‘weap- implements during acts of interpersonal violence. The only other on’’; in other words, they used an implement in a functional clearly documented example, probably older than 50,000 years, context which differed from that for which it was originally comes from the Shanidar 3 Neanderthal. This specimen exhibits designed. a slash in the superior margin of the ninth left rib, resulting from The cognitive ability to use tools multifunctionally was most a penetrating implement, which remained stuck between neigh- probably acquired earlier during hominid evolution. Direct boring ribs until the individual’s death, but which was lost evidence for this hypothesis is scant, but it appears that the postmortem (22, 23). These rare cases of tool-mediated wounds cognitive capacities and technical skills of early hominids are must be interpreted in an evolutionary, behavioral, and cultural typically underestimated because relatively little is known about context, using comparative data on trauma in Neanderthals and the in vivo level of complexity of tool production and utilization. fossil EMH, as well as modern evidence on the relationship Nevertheless, evidence for hafting of Mousterian stone imple- among trauma, interpersonal violence, and tool use in human ments with heat-processed bitumen (17, 34) and for the use of and nonhuman primates. aerodynamically designed wooden hunting spears (35) suggest Neanderthals were shown to differ from fossil and extant that the variety, effectiveness, and material sophistication of EMH populations in both the frequency and pattern of skeletal Middle and Late Pleistocene implements, and therefore of their injury: The overall incidence of trauma was comparatively high utilization, was considerable. The intentional use of implements and concentrated to the head and neck (21). Differences in in the context of intragroup conflict must have had a major pattern of trauma between Neanderthals and the EMH from the impact during hominid evolution because the availability of Upper Paleolithic have not yet been investigated systematically, highly effective hunting and͞or food-processing tools in inter- but it appears that the overall frequency of trauma was lower in personal conflict created a new and considerable potential for the EMH populations, whereas the proportion of head and neck intragroup damage, a potential that required specific behavioral injuries was probably as elevated as in the Neanderthals (E. adjustments with which to cope. Intragroup aggression in pri- Trinkaus, personal communication). Taking into account that mate societies must be understood as one specific behavioral injuries tend to accumulate over an individual’s lifetime, such option in a complex network of social interactions, which is that older individuals typically exhibit a greater number of typically balanced by active reconciliatory behavior (20) and͞or

Zollikofer et al. PNAS ͉ April 30, 2002 ͉ vol. 99 ͉ no. 9 ͉ 6447 Downloaded by guest on September 30, 2021 the minimization of social interactions under crowding notably the evidence of burial and a hypothetical case of cranial conditions (36). vault deformation (41). If we adhere to the hypothesis that the St. Ce´saire individual was injured in an act of intragroup violence and was later assisted Conclusions to some extent during healing, this fossil lesion sheds light on To reconstruct the causes and consequences of the traumatic both the disruptive͞deleterious and integrative͞supportive as- event that affected the St. Ce´saire individual, we followed a pects of . This fits well into the picture that maximum-likelihood approach based on comparative fossil and Neanderthals were capable of sustaining severely impaired actualistic data. We come to the conclusion that the cranial individuals over extended periods of time (21), and that this injury was inflicted with a tool during an act of intragroup behavioral competence was already present in the Middle Pleis- interpersonal violence. In a wider context, we suggest that the tocene (37). We must therefore conceive that Neanderthals, basic behavioral and cognitive abilities to use implements during depending on the context, inflicted wounds to conspecifics and interpersonal conflict were probably already present early during nursed the injured, using aggressive and integrative behavioral hominid evolution and may represent a significant aspect of the elements as tools in a network of social interactions. Within this evolution of social tool use. Accordingly, it can be assumed that basic hominid pattern of behavior, implements probably played in this specific respect, no major ‘‘transition’’ from Neanderthal- a crucial role because of their high effectiveness in interpersonal specific to EMH-specific behavioral patterns during the early violence and because they represented an additional level of Upper Paleolithic took place. This process most likely went complexity of social interactions. across species and was eminently patterned, both spatially and The difficulty to infer an indisputable behavioral context from temporally. Although genetic, developmental, and morpholog- the observed skeletal traumatic alterations is therefore not only ical data suggest that Neanderthals and EMH are separated at because of the limitations of paleodiagnosis but also may be the species level (42–44), their ways to balance between aggres- indicative of the behavioral polyvalence of tool use in Neander- sive and cooperative tool-mediated behavioral patterns were thals. Accordingly, the links among form, purpose, and effective largely similar. function of a tool might have been relatively loose. The most prominent behavioral context of Neanderthal tool use directed This study has greatly benefited from discussions with E. Trinkaus, T. toward conspecifics is cannibalism, for which evidence has been Bo¨hni, R. Majcen, C. van Schaik, J. Zilha˜o, H. Thieme, and M. Schultz, advanced since the early days of Neanderthal research (38). as well as from the comments and suggestions of three anonymous However, even the clearest evidence for butchering of conspe- reviewers. The constant support of P. Stucki is gratefully acknowledged. cifics from the site of Moula-Guercy (39, 40) ultimately remains We thank K. Alt, U. Bochsler, and Ch. Lanz for kindly providing the unresolved in terms of its behavioral and motivational context. archeological specimens. We also thank Gea Bijl for technical assistance Implications that Neanderthal tool use was far more sophisti- during CT scanning of the comparative sample. This work was supported cated than generally assumed also comes from other sources, by the Swiss National Science Foundation.

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