zollikofer et al - evidence for interpersonal violence in the st. césaire neanderthal

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behavioral context could be studied at increasing levels of detail(Table 1). For the comparative analysis of the external andinternal structure of the bone, we used a sample of adultspecimens comprising (i) an archeological specimen exhibiting ahealed slash resulting from sharp trauma to the cranial vault(13), (ii) three specimens with healed trepanations [one neolithic(14) and two modern skulls], and (iii) four specimens exhibitingmetopic sutures andor persisting fontanelles.

Paleopathology

The medial border of the cranial vault fragment of the St. CesaireNeanderthal deviates in its external and internal structure fromboth postmortem fractures and interosseous sutures. The exter-nal lamina of the bone is rounded off toward the medial margin,and the diploic region is covered with cortical bone (Fig. 2). Thismorphology is characteristic of in vivo apposition of bone matrixand excludes postmortem abrasion and erosion as potentialmechanisms. Bone apposition at structural boundaries mayoccur under two different circumstances: normal periostealgrowth in sutural tissue and bone regeneration following aninjury. The off-axis position and oblique orientation of the

margin (Fig. 1) exclude that it represents parts of the interpa-rietal and a supposed metopic suture. On the other hand, apresumed 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 aborder around a fontanelle or a suture around a bregmaticossicle. Furthermore, the cross-sectional structure of the boneclearly differs from that of an interosseous suture, which exhibitsa corrugated border with less dense cortical bone than the border

of a healed wound (Fig. 3). The most probable cause of theobserved morphology is therefore bone regeneration followinga lesion, a scenario that is corroborated by the close match of thecross-sectional morphology of the St. Cesaire 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 withthe aim to infer the proximate mechanical causes of the lesionand to reconstruct its posttraumatic history. As evidenced by thenearly straight border of the scar, the individual most probablysuffered a lesion from a blade-shaped object. The resulting slashin the cranial vault is preserved on its right (lateral) side over alength of 68 mm; it was probably slightly longer in vivo. The left(medial) side of the groove was lost during fossilization. Judgingfrom the degree of bone remodeling along the margin, the injuryreached its greatest depth near the coronal suture, correspond-

ing to the presumed primary site of impact. Toward the anteriorand posterior ends, the groove tapers off. This morphology mostclosely matches the pattern of direct, sharp trauma. Under thesebiomechanical conditions, the high but localized stresses causedby the impacting object lead to puncturingcutting of the scalpand the external lamina of the bone, comminution of the diploe,and separationdisplacement of bone fragments from the in-ternal lamina (9). The St. Cesaire specimen in fact bearsevidence that at the primary site of the impact the internallamina was fractured and parts of it were dislocated whereas,toward the periphery of the slash, it was only partially severed(Figs. 1 and 2). The interpretation of the slash as a linearfracture resulting from blunt trauma is a less likely scenariobecause the compressive forces induced by blunt objects leadto nonlocal deformation of the cranial vault, typically resultingin multiple radial and tangential fractures around the center of

impact (9, 16).Comparison with an archeological specimen exhibiting a

healed slash on the frontal bone permits further inferencesregarding the severity of the injury and the subsequent healingprocess (Fig. 2). Given the moderate depth of the St. Cesairescar, it appearsthat the lesionwas relatively mild. Cross-sectionalCT images (Figs. 2 and 3) show that the injured region wasextensively remodeled during lifetime; the severed externallamina was smoothed out by bone resorption and deposition, andthe dislocated parts of the internal lamina were fixated, probablythrough formation of connective tissue in the diploic region. Theexternal and cross-sectional morphology of the injured regiondoes not show any signs of post-traumatic infection (e.g., peri-ostitis or osteomyelitis), and the degree of healing is relativelyadvanced. Considering that bone healing is visible only 2–3weeks after a traumatic event (9), it can be concluded that theindividual survived the injury for at least some months, such thata direct causal connection between the trauma and the individ-ual’s death is unlikely.

Behavioral Context

By using forensic criteria originally developed for trauma anal-ysis in extant and archeological populations (9), it is possible toconceive of various scenarios under which the St. Cesaire injurycould have occurred, assess their relative likelihood, and discusstheir behavioral and motivational implications. The anteropos-terior orientation of the slash as well as its apical position are

Fig. 1. Computerized reconstruction of the St. Cesaire 1 Neanderthal skull

(mirror-imagedcompleted parts aretransparent)showingthe bonyscar in the

right apical cranial vault. The skull is seen from the direction in which the

hypothetical blowwas exerted. Arrows indicate the anteroposterior (a and p)

extent of the preserved lateral border of the injury (c, coronal suture; b,

bregma;*

, locationof thecoronalcrosssectionthrough theinjury(see Fig.2b

);, location of the parasagittal cross section through the coronal suture (see

Fig. 3c); thedotted lineindicatesthe reconstructedpositionof the midsagittal

plane of the cranial vault). Note oblique, off-midline position of the scar.

(Scale bar 5 cm.)

Zollikofer et al. PNAS April 30, 2002 vol. 99 no. 9 6445



indicative of a blow or a thrust exerted against the individualfrom the front or from behind, assuming that the individual wasin an upright position. These spatial relationships indicate anintentional action, effected with an implement rather than anatural object. Accidental injury, such as falling onto a sharpedge, a rockfall, or an unintentional blow, such as resulting froma hunting incident, are less likely explanations; comparative

forensic evidence suggests that accidental trauma typically af-fects the sides of the cranial vault, as opposed to the apicallocation of intentional injuries (16).

Inferences regarding the nature of the implement, the agentscausing the lesion, and the behavioral context must remaintentative. From a mechanical point of view, the severity of sharptrauma depends on the mass, impact velocity, and incisiveness of the weapon. The wide range of possible combinations of these

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. Cesaire between alternatives.

*Compiled after refs. 8, 9, 16, 18, and 19.

Fig. 2. Anatomy of a blow. (a) Mediolateral view of the right border of the

St.Cesaire1 cranial vaultinjury (samesymbolsasin Fig. 1:a andp,anteriorand

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

remodeling(gray) and areasaffectedby postmortem fracturing(hatched). (b

and c) Comparative morphology of the injured vault bones in St. Cesaire 1 (b)

and a specimen from a medieval graveyard (13) exhibiting a healed scar

resulting from sharp trauma on the left frontal bone (c) (both specimens in

anteroposterior view, coronal cross sections); the CT sections show bone

remodeling at the margin of the injured external lamina (*) and a space (‚)

between the dislocated internal lamina and the diploe , probably filled by

connective tissue. (Scale bar 5 cm.)

Fig. 3. Comparative cross-sectional morphology of bone injuries and su-

tures. (a and b) Healed scars of St. Cesaire 1 and a medieval specimen (same

coronal sections as in Fig. 2 b and c). (c) St. Cesaire 1 coronal suture (parasag-

ittal section through in Fig. 1). (d ) Metopic suture in a recent specimen

(coronal section). (e) Large occipital trepanation during early phases of heal-

ing [Ensisheim skull (14), coronal section]. ( f ) Healed occipital trepanation in

a recent specimen (coronal section).Note appositionof densecorticalbone at

the injured borders, resulting in a smooth contour, as opposed to the less

dense and corrugated aspect of the sutural borders. (Scale bar 5 cm.)

6446 www.pnas.orgcgidoi10.1073pnas.082111899 Zollikofer et al.



parameters encompasses a correspondingly wide spectrum of implements that might have been used to inflict the wound. Forexample, the Chatelperronian stone tools recovered from thesite of St. Cesaire are relatively small and exhibit retouched,blunt edges. To attain the kinetic energy necessary to penetratebone, considerable acceleration, probably through hafting (17),would have been essential. Implications regarding the nature of the weaponry are complicated by the fact that the function of Chatelperronian implements is poorly understood and the pre-

served stone industry probably represents a small fraction of theactual in vivo spectrum of available tools.Comparative evidence from historical populations suggests

that interpersonal conflict behavior resulting in cranial vaultfractures is relatively frequent (18, 19). Given the characteristicapical location of the injury in St. Cesaire, direct interaction withanother individual is the most parsimonious scenario. Theoret-ically, the injury may have resulted from intragroup, intergroup,or even interspecific conflict behavior. The first scenario is themost likely one because in socially organized species the vastmajority of interpersonal interactions occur at the within-grouplevel (20). Population densities were low during the Late Pleis-tocene, such that mutual avoidance during the rare encountersbetween different groups (both intra- and interspecific) mighthave represented the optimum strategy for the resolution of potential conflict (21). Nevertheless, it must be considered that

patchy resource distribution might have induced temporarybetween-group competition.

Another aspect that requires consideration is the motivationalbackground of the conflict in which the St. Cesaire Neanderthalwas involved. Motivations may range from a premeditatedassault to a brief argument emerging from a temporary conflictbetween individuals, such as over social status, access to poten-tial mates, or intragroup resources. Overall, a likely scenario forthe interpersonal violence in St. Cesaire is intragroup temperswith available ‘‘weaponry.’’ The immediate effects of the traumawere probably serious, implying heavy bleeding, cerebral com-motion, and temporary impairment. Although it is possible thatthe individual sustained these adverse effects autonomously, itcan be assumed that it had benefited at least to some extent frominitial intragroup assistance.

DiscussionThe St. Cesaire cranial injury adds to the extremely small sampleof specimens bearing direct evidence that Neanderthals usedimplements during acts of interpersonal violence. The only otherclearly documented example, probably older than 50,000 years,comes from the Shanidar 3 Neanderthal. This specimen exhibitsa slash in the superior margin of the ninth left rib, resulting froma penetrating implement, which remained stuck between neigh-boring ribs until the individual’s death, but which was lostpostmortem (22, 23). These rare cases of tool-mediated woundsmust be interpreted in an evolutionary, behavioral, and culturalcontext, using comparative data on trauma in Neanderthals andfossil EMH, as well as modern evidence on the relationshipamong trauma, interpersonal violence, and tool use in humanand nonhuman primates.

Neanderthals were shown to differ from fossil and extantEMH populations in both the frequency and pattern of skeletalinjury: The overall incidence of trauma was comparatively highand concentrated to the head and neck (21). Differences inpattern of trauma between Neanderthals and the EMH from theUpper Paleolithic have not yet been investigated systematically,but it appears that the overall frequency of trauma was lower inthe EMH populations, whereas the proportion of head and neckinjuries was probably as elevated as in the Neanderthals (E.Trinkaus, personal communication). Taking into account thatinjuries tend to accumulate over an individual’s lifetime, suchthat older individuals typically exhibit a greater number of

lesions (21, 24), it is worth noting that immature specimens of Neanderthals [Devil’s Tower and Le Moustier (25, 26) and EMH(Qafzeh 11)] also bear evidence for craniofacial trauma. Theelevated frequency of trauma might therefore reflect not only ahigh risk of injury during close-quarter hunting of medium tolarge-sized game (21), but a physically demanding and stressfullife from early ontogenetic stages (27, 28).

Against this comparative background, the dearth of directevidence for tool involvement in fossil hominid trauma may be

interpreted in two different ways. On one hand, it may ref lect alow in vivo frequency of intentional or accidental tool-inflictedinjuries relative to other types of trauma. It also may ref lect thelimits of paleopathological diagnosis; in a fossil, a lesion inducedby an implement can be recognized only if evidence of healingis still present postmortem and the morphology of the scarpermits inferences regarding the responsible weapon. The prob-ability of detecting such injuries is further reduced through theeffects of diagenesis, which tends to degrade the paleopatho-logical evidence (9). Following this line of argument, a relevantproportion of the nondiagnostic injuries may represent tool-induced trauma andor may be seen in the context of interper-sonal violence rather than accident.

Data from nonhuman primates indicate that interpersonalviolence within social networks represents a major cause of trauma. For example, in the Gombe chimpanzees more than

one-half of the observed skeletal lesions are fractures and bitewounds resulting from intragroup violence (24), and severalcases of fatal outcome of intragroup clashes have been reportedin both wild and captive chimpanzee groups (29). A questionarises whether there is evidence of tool use in interpersonalconflict situations in nonhuman primates. The cultural variabil-ity and contextual diversity of tool production and use have beenstudied extensively in various primate communities (30–32),revealing a general behavioral basis to aim objects, but not tools,toward conspecifics in the context of conflict behavior. However,although object-throwing to intimidate group members is fairlycommon (30, 33), the purposeful and directed use of toolsdesigned for a distinct function during acts of interpersonalviolence has not been reported. On the basis of the currentlyavailable evidence, it appears therefore that hominids differfromnonhumanprimates in their ability to produce and use tools

in an expanded, multifunctional context, including conflict be-havior. Accordingly, the St. Cesaire 1 and Shanidar 3 woundsindicate that Neanderthals transformed a ‘‘tool’’ into a ‘‘weap-on’’; in other words, they used an implement in a functionalcontext which differed from that for which it was originallydesigned.

The cognitive ability to use tools multifunctionally was mostprobably acquired earlier during hominid evolution. Directevidence for this hypothesis is scant, but it appears that thecognitive capacities and technical skills of early hominids aretypically underestimated because relatively little is known aboutthe in vivo level of complexity of tool production and utilization.Nevertheless, evidence for hafting of Mousterian stone imple-ments with heat-processed bitumen (17, 34) and for the use of aerodynamically designed wooden hunting spears (35) suggestthat the variety, effectiveness, and material sophistication of Middle and Late Pleistocene implements, and therefore of theirutilization, was considerable. The intentional use of implementsin the context of intragroup conflict must have had a majorimpact during hominid evolution because the availability of highly effective hunting andor food-processing tools in inter-personal conflict created a new and considerable potential forintragroup damage, a potential that required specific behavioraladjustments with which to cope. Intragroup aggression in pri-mate societies must be understood as one specific behavioraloption in a complex network of social interactions, which istypically balanced by active reconciliatory behavior (20) andor

Zollikofer et al. PNAS April 30, 2002 vol. 99 no. 9 6447



the minimization of social interactions under crowdingconditions (36).

If we adhere to the hypothesis that the St. Cesaire individualwas injured in an act of intragroupviolence andwas later assistedto some extent during healing, this fossil lesion sheds light onboth the disruptivedeleterious and integrativesupportive as-pects of Neanderthal behavior. This fits well into the picture thatNeanderthals were capable of sustaining severely impairedindividuals over extended periods of time (21), and that this

behavioral competence was already present in the Middle Pleis-tocene (37). We must therefore conceive that Neanderthals,depending on the context, inf licted wounds to conspecifics andnursed the injured, using aggressive and integrative behavioralelements as tools in a network of social interactions. Within thisbasic hominid pattern of behavior, implements probably playeda crucial role because of their high effectiveness in interpersonalviolence and because they represented an additional level of complexity of social interactions.

The difficulty to infer an indisputable behavioral context fromthe observed skeletal traumatic alterations is therefore not onlybecause of the limitations of paleodiagnosis but also may beindicative of the behavioral polyvalence of tool use in Neander-thals. Accordingly, the links among form, purpose, and effectivefunction of a tool might have been relatively loose. The mostprominent behavioral context of Neanderthal tool use directed

toward conspecifics is cannibalism, for which evidence has beenadvanced since the early days of Neanderthal research (38).However, even the clearest evidence for butchering of conspe-cifics from the site of Moula-Guercy (39, 40) ultimately remainsunresolved in terms of its behavioral and motivational context.Implications that Neanderthal tool use was far more sophisti-cated than generally assumed also comes from other sources,

notably the evidence of burial and a hypothetical case of cranialvault deformation (41).

Conclusions

To reconstruct the causes and consequences of the traumaticevent that affected the St. Cesaire individual, we followed amaximum-likelihood approach based on comparative fossil andactualistic data. We come to the conclusion that the cranialinjury was inflicted with a tool during an act of intragroup

interpersonal violence. In a wider context, we suggest that thebasic behavioral and cognitive abilities to use implements duringinterpersonal conflict were probably already present early duringhominid evolution and may represent a significant aspect of theevolution of social tool use. Accordingly, it can be assumed thatin this specific respect, no major ‘‘transition’’ from Neanderthal-specific to EMH-specific behavioral patterns during the earlyUpper Paleolithic took place. This process most likely wentacross species and was eminently patterned, both spatially andtemporally. Although genetic, developmental, and morpholog-ical data suggest that Neanderthals and EMH are separated atthe species level (42–44), their ways to balance between aggres-sive and cooperative tool-mediated behavioral patterns werelargely similar.

This study has greatly benefited from discussions with E. Trinkaus, T.Bohni, R. Majcen, C. van Schaik, J. Zilhao, H. Thieme, and M. Schultz,as well as from the comments and suggestions of three anonymousreviewers. The constant support of P. Stucki is gratefully acknowledged.We thank K. Alt, U. Bochsler, and Ch. Lanz for kindly providing thearcheological specimens. We also thank Gea Bijl for technical assistanceduring CT scanning of the comparative sample. This work was supportedby the Swiss National Science Foundation.

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zollikofer et al - evidence for interpersonal violence in the st. césaire neanderthal

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