Henshilwood, C.S., d’Errico, F., Yates, R., Jacobs, Z., Tribolo, C., Duller, G.A.T., Mercier N., Sealy, J.C., Valladas, H., Watts, I. & Wintle, A.G. 2002. Emergence of Modern Human Behaviour: Middle Stone Age engravings from South Afri

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Henshilwood, C.S., d’Errico, F., Yates, R., Jacobs, Z., Tribolo, C., Duller, G.A.T., Mercier N., Sealy, J.C., Valladas, H., Watts, I. & Wintle, A.G. 2002. Emergence of Modern Human Behaviour: Middle Stone Age engravings from South Africa. Science

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  Emergence of Modern HumanBehavior: Middle Stone AgeEngravings from South Africa Christopher S. Henshilwood, 1,2,3 * Francesco d’Errico, 4 Royden Yates, 1 Zenobia Jacobs, 5 Chantal Tribolo, 6 Geoff A. T. Duller, 5 Norbert Mercier, 6  Judith C. Sealy, 7 Helene Valladas, 6 Ian Watts, 1,7 Ann G. Wintle 5 In the Eurasian Upper Paleolithic after about 35,000 years ago, abstract or depictional images provide evidence for cognitive abilities considered integralto modern human behavior. Here we report on two abstract representationsengraved on pieces of red ochre recovered from the Middle Stone Age layersat Blombos Cave in South Africa. A mean date of 77,000 years was obtainedfor the layers containing the engraved ochres by thermoluminescence datingof burnt lithics, and the stratigraphic integrity was confirmed by an opticallystimulated luminescence age of 70,000 years on an overlying dune. Theseengravings support the emergence of modern human behavior in Africa at least35,000 years before the start of the Upper Paleolithic. Archaeological evidence associated withmodern cognitive abilities provides importantinsights into when and where modern human behavior emerged ( 1 ). Two models for thesrcins of modern human behavior are cur-rent: (i) a late and rapid appearance at  40 to50 thousand years ago (ka) associated withthe European Upper Paleolithic and the Later Stone Age (LSA) of sub-Saharan Africa ( 2 , 3 ) or (ii) an earlier and more gradual evolu-tion rooted in the African Middle Stone Age(MSA;   250 to 40 ka) ( 4 ,  5 ). Evidence for modern behavior before 40 ka is relativelyrare and often ambiguous ( 2 ,  6  ). However, insub-Saharan Africa, archaeological evidencefor changes in technology, economy, and so-cial organization and the emergence of sym- bolism in the MSA may support the second model ( 4 ,  5 ,  7–9 ). Examples of these changesinclude standardized formal lithic tools ( 5 ,  8 , 10 ), shaped bone implements ( 5 ,  7  ,  9 ,  11 ),innovative subsistence strategies such as fish-ing and shellfishing ( 10–12 ), and the system-atic use of red ochre ( 10 ,  13 ).Utilized ochre is found in almost all StoneAge occupations in southern Africa that areyounger than 100 ka ( 13 ). The ochre mayhave served only utilitarian functions (e.g.,skin protection or hide tanning) ( 3 ) or mayhave been used symbolically as pigment ( 4 , 10 ,  13 ). Evidence for the latter is a persistentuse of ochre with saturated red hues to pro-duce finely honed crayon or pencil forms ( 10 , 13 ). However, no ochre pieces or other arti-facts older than  40 ka provide evidence for abstract or depictional images, which would indicate modern human behavior ( 2 ,  14 ,  15 ).We have recovered two pieces of engraved ochre from the MSA layers at Blombos Cave,South Africa. Situated on the southern Capeshore of the Indian Ocean, the cave is 35 mabove sea level. A 5- to 60-cm layer of aeoliansand containing no archaeological artifacts(BBC Hiatus; Fig. 1) separates the LSA fromthe MSA occupation layers. The MSA is divid-ed into three substages ( 9 ,  10 ) (Fig. 1): (i) anupper series of occupational deposits, BBC M1,typified by abundant bifacially flaked, lanceo-late-shaped stone points (Still Bay points) ( 10 );(ii) a middle series, BBC M2, containing fewer Still Bay points but relatively abundant in de-liberately shaped bone awls and points thatwere probably hafted ( 9 ,  11 ); and (iii) a lower BBC M3 series with few retouched pieces butwith blades and flakes typical of the MosselBay/MSA 2b subphase ( 10 ). Associated, well- preserved faunal remains from all layers indi-cate that subsistence strategies were wide rang-ing and include terrestrial and marine mam-mals, shellfish, fish, and reptiles ( 10 ,  11 ).More than 8000 pieces of ochre, many bear-ing signs of utilization, have been recovered from the MSA layers at Blombos Cave ( 10 ).Seven of nine pieces are potentially engraved and under study. We report here on the twounequivocallyengravedpiecesrecoveredinsitufrom layer CC, square E6a and layer CD,square H6a (Fig. 1) ( 10 ) during excavations in1999 and 2000, respectively. The engraved ochre piece from layer CC (SAM-AA 8937)was located adjacent to a small hearth, and thatfrom layer CD (SAM-AA 8938) was surround-ed by a number of small, basin-shaped hearths.Both specimens were located in a matrix of undisturbed and consolidated mixed ash and sand. There is no indication of perturbation ineither the overlying 15 to 20 cm of MSA de- posits or in the blanketing aeolian dune sand and no sign of intrusion of younger LSA ma-terials ( 9 ,  10 ). All lithic artifacts in the ochre- bearing and overlying MSA layers are typolog-ically MSA ( 9 ,  10 ).On the 8937 piece (Fig. 2, A and B), boththe flat surfaces and one edge are modified byscraping and grinding. The edge has twoground facets, and the larger of these bears across-hatched engraved design. The crosshatching consists of two sets of six and eightlines partly intercepted by a longer line. Theengraving on 8938 (Fig. 2, C and D) consistsof a row of cross hatching, bounded top and  bottom by parallel lines and divided throughthe middle by a third parallel line that divides 1 Iziko Museums of Cape Town, South African Muse-um, Post Office Box 61, Cape Town, 8000, SouthAfrica.  2 Department of Anthropology, State Universi-ty of New York at Stony Brook, NY, 11794, USA. 3 Centre for Development Studies, University of Ber-gen, Strømgaten, 54, 5007 Bergen, Norway.  4 Institutde Pre´histoire et de Ge´ologie du Quaternaire, UMR5808 du CNRS, Avenue des Faculte´s, 33405, Talence,France.  5 Luminescence Dating Laboratory, Institute of Geography and Earth Sciences, University of Wales,Aberystwyth, SY23 3DB, UK.  6 Laboratoire des Scienc-es du Climat et de l’Environnement, UMR CEA-CNRS,Avenue de la Terrasse, 91198 Gif-sur-Yvette cedex,France.  7 Department of Archaeology, University of Cape Town, Private Bag, Rondebosch, 7701, CapeTown, South Africa.*To whom correspondence should be addressed. E-mail: chenshilwood@iziko.org.za BBC Hiatus CACICBCCCDCJCFB/CFCCFACGACCGBCGAA BBC M1BBC M2BBC M3BBC LSA    0 .   5  m SAM-AA 8938 * SAM-AA 8937 * Unexcavated Fig. 1.  Stratigraphy of Blombos Cave (34°25  S,21°13  E). Sequence of MSA layers in square H6showing relative location of engraved ochrepieces SAM-AA 8937 and SAM-AA 8938, bifa-cial Still Bay points (lanceolate shape), andbone tools. Closed and open symbols for bifa-cial points and bone tools indicate commonand rare occurrences, respectively. The MSAlayers consist principally of sands interlayeredwith consolidated beds, lenses, and stringers of marine shells, organic matter, and wood ash. R  E P O R T S 15 FEBRUARY 2002 VOL 295 SCIENCE www.sciencemag.org 1278  the lozenge shapes into triangles. Some of thelines are well-defined single incisions; othershave parallel tracks along part or all of their lengths. Much of the parallel tracking mayhave resulted from a change in position of theengraving tool causing simultaneous scoringfrom more than one projection. The midlinecomprises three marking events. Examinationof the intersections of the cross-hatched linesindicates that they were not executed as con-secutive cross hatchings but that lines weremade in first one direction and then another;the horizontal lines overlie the cross hatch-ing. The preparation by grinding of the en-graved surface, situation of the engraving onthis prepared face, engraving technique, and final design are similar for both pieces, indi-cating a deliberate sequence of choices. Al-though the engraving on the 8937 ochre hasfewer markings than the 8938 piece, it indi-cates that 8938 is not unique; the engravingon 8938 can be considered a complex geo-metric motif as the cross-hatched lines are bisected and framed by horizontals.Assessing the significance of these engrav-ingsdemandsanaccuratedeterminationoftheir age ( 16  ). The engraved ochres were found within layers containing bifacially flaked stone points; in the South African MSA, these stone point types occur only within or below How-iesons Poort horizons ( 10 ) dated to  65 to 70ka ( 17  ). This association suggests that the en-gravings are older than 65 ka. To independentlyconfirm and refine this time frame, we applied two luminescence-based dating methods to theBlombos Cave layers. Thermoluminescence(TL) dates were obtained for five burnt lithicsamples from the MSA phase BBC M1 (Fig. 1)( 18 ,  19 ). The mean age for the lithic samples is77    6 ka ( 20 ). To confirm the stratigraphicintegrity, we applied optically stimulated lumi-nescence (OSL) dating to the aeolian dune(BBC Hiatus) separating the LSA and MSAlayers (Fig. 1). Multiple grain measurementswith a single aliquot regenerative (SAR) proce-dure ( 21 ) yielded a depositional age of 69  5ka ( 22 ). Single-grain SAR measurements ( 23 )yielded consistent ages ( 24 ), indicating that theaggregate samples were not contaminated bygrains of different ages ( 25 ). Because only1.8% of the 1892 grains analyzed yielded re- producible growth curves, a more representa-tive approach was also used ( 26  ), combiningOSL signals from grains to generate syntheticaliquots. These provide a depositional age of 70  5 ka ( 20 ) and confirm the antiquity of theengraved ochres.Abstract images similar to the BlombosCave engravings occur at Upper Paleolithicsites in Eurasia ( 15 ). The Blombos Cave mo-tifs suggest arbitrary conventions unrelated toreality-based cognition, as is the case in theUpper Paleolithic ( 15 ), and they may have been constructed with symbolic intent, themeaning of which is now unknown. Thesefinds demonstrate that ochre use in the MSAwas not exclusively utilitarian and, arguably,the transmission and sharing of the meaningof the engravings relied on fully syntacticallanguage ( 5 ,  27  ).Genetic and fossil evidence suggests thathumans were anatomically near modern inAfrica before 100 ka ( 5 ,  28 ,  29 ). Key ques-tions are whether anatomical and behavioralmodernity developed in tandem ( 5 ) and whatcriteria archaeologists should use to identifymodern behavior ( 2 ,  4 ,  5 ). For the latter, thereis agreement on one criterion—archaeologi-cal evidence of abstract or depictional imagesindicates modern human behavior ( 2 ,  14 ,  15 ).The Blombos Cave engravings are intentionalimages. In the light of this evidence, it seemsthat, at least in southern Africa,  Homo sapi-ens  was behaviorally modern about 77,000years ago. References and Notes 1. The term “modern human behavior” as used here hasno chronological implication and means the thoughtsand actions underwritten by minds equivalent tothose of   Homo sapiens  today. Key among these is theuse of symbols.2. P. A. Mellars, K. Gibson, Eds.,  Modelling the Early Human Mind   (McDonald Institute Monographs, Cam-bridge, 1996).3. R. G. Klein,  The Human Career   (Chicago Univ. Press,Chicago, IL, 1999).4. H. J. Deacon, J. Deacon,  Human Beginnings in South Africa: Uncovering the Secrets of the Stone Age  (Dav-id Philip, Cape Town, South Africa, 1999).5. S. McBrearty, A. Brooks,  J. Hum. Evol.  38 , 453 (2000).6. F. d’Errico, P. Villa,  J. Hum. Evol.  33 , 1 (1997).7. J. Yellen, A. Brooks, E. Cornelissen, M. Mehlman, K.Stewart,  Science  268 , 553 (1995).8. S. Wurz, thesis, Stellenbosch University, Stellenbosch,South Africa (2000).9. C. S. Henshilwood, F. d’Errico, C. W. Marean, R. Milo,R. Yates,  J. Hum. Evol.  41 , 631 (2001).10. C.S.Henshilwood etal .,  J.Archaeol.Sci. 28 ,421(2001) . 11. C. S. Henshilwood, J. C. Sealy,  Curr. Anthropol.  38 ,890 (1997).12. R. C. Walter   et al. ,  Nature  405 , 65 (2000).13. I. Watts, in  The Evolution of Culture , R. Dunbar, C.Knight, C. Power, Eds. (Edinburgh Univ. Press, Edin-burgh, 1999), pp. 113–146.14. G. A. Clark, C. M. Willermet,  Conceptual Issues inModern Human Origins Research  (de Gruyter, NewYork, 1997). Fig. 2.  Engraved ochres from Blombos Cave. ( A ) SAM-AA 8937 is a flat piece of shale-like ochre thatgrades into silt on the reverse side: weight  39.2 g; maximum length  53.6 mm; breadth  42.6mm, depth    11.7 mm; streak color notation 3060 Y65R ( 33 ). ( B ) Tracing of lines verified asengraved by study under magnification (scale bar, 5 mm). ( C ) SAM-AA 8938 is a rectangular slabof ochreous shale: weight  116.6 g; maximum length  75.8 mm; breadth  34.8 mm; depth  24.7 mm; streak color notation 4050 Y60R ( 30 ). Oblique lighting of specimen accentuates bothengraved lines and irregularities of the surface, some created by grinding before the engraving andothers by the process of engraving. ( D ) Tracing of lines verified as engraved by study under magnification, superimposed on flat-bed scan of engraved surface (scale bar, 10 mm). R  E P O R T S www.sciencemag.org SCIENCE VOL 295 15 FEBRUARY 2002  1279  15. P. Bahn, J. Vertut,  Journey Through the Ice Age  (Wei-denfeld & Nicolson, London, 1997).16. A sediment sample from Blombos was included in anearlier study of coastal sediments, in which it wasfound to date to oxygen isotope stage 5 ( 30 ). How-ever, the dates obtained for unetched quartz andfeldspar grains with TL and infrared stimulated lumi-nescence, respectively, were inconsistent.17. J. C. Vogel, in  Humanity - from African Naissance tocoming Millennia , P. V. Tobias, M. A. Raath, J. Moggi-Cecchi, G. A. Doyle, Eds. (Univ. of Florence Press,Florence, Italy, 2000), pp. 261–268 . 18. The five lithic specimens (a few cm in size and weighingbetween 6 and 35 g) came from the upper phase of occupational deposits BBC M1: Samples BBC24 andBBC23 are from CA/CB and BBC15, BBC20, and BBC22are from CC. Examination of thin sections revealed thepresence of quartz grains embedded in a siliceous ma-trix. The time since they were burnt was computedfrom TL analysis of 100- to 160-  m grains obtained bycrushing after the samples’ outer surfaces had beenremoved with a diamond saw ( 31 ). The equivalent dose( D e ) was determined with a combined additive andregenerative dose protocol ( 19 ). U, Th, and K concen-trationsofthelithicsamplesweremeasuredbyneutronactivation analysis ( 32 ). The total dose rates ( 20 ) werecalculated assuming that the quartz grains were free of radioactive impurities and that all radioisotopes wereconfined to and uniformly distributed within the sur-rounding siliceous matrix. In computing the alpha andbeta dose rates received by the grains, attenuationfactors appropriate for the mean grain size in eachspecimen were taken into account. To determine thegamma dose rates, we buried 24 dosimeters in the cavedeposits for 1 year at points no farther than 1 m fromeach previously excavated lithic. The ages combine toprovide a mean age of 77  6 ka, which is consistentwith the OSL age for the overlying dune layer.19. N. Mercier, H. Valladas, G. Valladas,  Ancient TL  10 , 28(1992).20. Supplementary data including a table containingdose rate,  D e , and age information for TL and OSLanalyses and a supplementary figure showing a radialplot of OSL  D e  values for the “synthetic” aliquot dataare available on  Science  Online at www.sciencemag.org/cgi/content/full/1067575/DC1.21. A. S. Murray, A. G. Wintle,  Radiat. Meas.  32 , 57 (2000).22. The depositional age of the dune layer was deter-mined by OSL dating. OSL analyses on Aber/52-ZB-15 were undertaken on quartz grains to measure theradiation dose that they had received since their lastexposure to daylight. Their equivalent dose ( D e ) wasdetermined with the SAR procedure. The total radi-ation dose rate to the grains ( 20 ) was measured witha combination of thick-source alpha counting, betacounting, and atomic absorption spectroscopy for potassium determination, and a water content of 10  5% (weight water / weight dry sediment) wasused, based on current moisture contents in the cave.The calculated gamma dose rate was consistent withthat measured in the field, and the cosmic ray doserate of 45   Gy/year was based on the thickness of the overlying rock. Quartz grains were extracted after treatment with 10% hydrochloric acid to removecarbonates and 30 vol of H 2 O 2  to remove organics.The sample was sieved to obtain grains from 212 to250   m in diameter. Feldspars and heavy mineralswere removed by density separation at 2.62 and 2.70g/cm 3 . The alpha-irradiated outer layer of the grainswas removed by etching in 48% hydrofluoric acid for 45 min. The initial set of luminescence measure-ments (stimulation at 470 nm with blue diodes) used48 aliquots, each containing about 500 grains. Arange of thermal pretreatments (preheats) from 160°to 300°C for 10 s was used. From 200° to 280°C, the D e  values from 30 replicate aliquots were reproduc-ible and showed no systematic trend with tempera-ture. A weighted mean was calculated, with theindividual  D e  values weighted according to their un-certainty. The uncertainty in the mean was dividedby   N , where  N  is the number of independentestimates of   D e —in this case 30.  D e  values werecalculated with the package Analyst, which combinesuncertainties due to the counting statistics of eachOSL measurement and the error associated with themathematical fitting of the growth curve to theluminescence data. The 30 aliquots gave a value of 47.9  1.7 Gy, resulting in an age of 69  5 ka.23. L. Bøtter-Jensen, E. Bulur, G. A. T. Duller, A. S. Murray, Radiat. Meas.  32 , 523 (2000).24. The single-grain SAR measurements were made in anautomated reader based around a 10-mW, 532-nmNd: YVO 4  laser, whose beam can be directed atindividual grains ( 23 ). A single preheat at 220°C for 10 s was used, with the main OSL measurement ( L )being followed by measurement of the OSL response( T  ) to a test dose as observed after a 160°C cut heat( 21 ). Grains whose natural signal ratio ( L N  /T  N ) doesnot intersect the regeneration growth curve were notused in subsequent analyses. In addition, grainsthought to contain some feldspar were also rejected.The presence of feldspar was identified by makingadditional measurements of a given regenerationdose on each grain. The first measurement is under-taken within the SAR procedure and yields the ratio L 1 / T  1  used in the growth curve. For each grain, twoadditional measurements of   L / T   were made at theend of the SAR procedure. The first duplicates theprevious measurement, as a test of the sensitivitycorrection. The second uses the same regenerationdose, but, before preheating, the grains are exposedto infrared (830 nm) radiation from a 500-mW laser diode for 100 s. If the grains contain feldspar, thenthe infrared exposure will have reduced the magni-tude of   L , and hence the ratio of these last twomeasurements of   L / T   will be substantially less thanunity; for a quartz grain, the ratio will be consistentwith unity. Of the 1892 grains that were measured,22 were rejected on the basis of these criteria. TheOSL signal from many of the remaining 1870 grainswas close to instrumental background, and only 34 yielded reproducible growth curves.25. R. G. Roberts  et al .,  Nature  393 , 358 (1998).26. Single-grain OSL measurements were made with 19aluminum discs, with up to 100 grains on each disc.For each disc, the OSL signals from the unrejectedgrains were combined to generate “synthetic” ali-quots consisting of between 93 and 100 grains. The D e  values for 18 “synthetic” aliquots were combinedto give a weighted mean of 48.5    1.2 Gy, giving adepositional age of 70  5 ka ( 20 ).27. L. Aiello, N. G. Jablonski, Eds.,  The Origin and Diver- sification of Language  (Memoirs of the CaliforniaAcademy of Sciences, San Francisco, 1998).28. C. B. Stringer, in  Contemporary Issues in Human Evo-lution , W. Meikle, N. Jablonski, Eds. (California Acad-emy of Sciences, San Francisco, 1996), pp. 115–134.29. M. Ingman, K. Kaessmann, S. Pa¨a¨bo, U. Gyllensten, Nature  408 , 708 (2000).30. J. C. Vogel, A. G. Wintle, S. M. Woodborne,  J. Ar-chaeol. Sci.  26 , 729 (1999).31. H. Valladas,  Quat. Sci. Rev.  11 , 1 (1992).32. J.-L. Joron, thesis, Universite´ Paris-Sud (1974).33. “Natural Color System Index” (Scandinavian Colour Institute, Stockholm, 1999).34. This work was supported by grants to C.H. from theAnglo American Chairman’s Fund, Centre National dela Recherche Scientifique OHLL, the Leakey Founda-tion, the National Geographic Society, NSF, theSouth African National Research Foundation, and theWenner-Gren Foundation; to F.D. from CNRS Originede l’Homme, du Langage et des Langues (OHLL) andthe Service Culturel of the French Embassy in SouthAfrica; to Z.J. from the Sir Henry Strakosch MemorialTrust and an Overseas Research Student award; toC.T. from CNRS OHLL; to G.D. from the NaturalEnvironment Research Council; to J.S. from the SouthAfrican National Research Foundation and the Uni-versity of Cape Town; and to I.W. from the BritishAcademy. We thank G. Avery at Iziko Museums of Cape Town, the South African Museum, and K. vanNiekerk.30 October 2001; accepted 28 December 2001Published online 10 January 2002;10.1126/science.1067575Include this information when citing this paper. Marine Biodiversity Hotspotsand Conservation Priorities forTropical Reefs Callum M. Roberts, 1,2 * Colin J. McClean, 2  John E. N. Veron, 3  Julie P. Hawkins, 2 Gerald R. Allen, 4,8 Don E. McAllister, 5 † Cristina G. Mittermeier, 4 Frederick W. Schueler, 6 Mark Spalding, 7 Fred Wells, 8 Carly Vynne, 4 Timothy B. Werner 4 Coral reefs are the most biologically diverse of shallow water marine ecosystemsbut are being degraded worldwide by human activities and climate warming.Analyses of the geographic ranges of 3235 species of reef fish, corals, snails, andlobsters revealed that between 7.2% and 53.6% of each taxon have highly re-stricted ranges, rendering them vulnerable to extinction. Restricted-range speciesareclusteredintocentersofendemism,likethosedescribedforterrestrialtaxa.The10 richest centers of endemism cover 15.8% of the world’s coral reefs (0.012% of the oceans) but include between 44.8 and 54.2% of the restricted-range species.Manyoccurinregionswherereefsarebeingseverelyaffectedbypeople,potentiallyleadingtonumerousextinctions.Threatenedcentersofendemismaremajorbiodi-versity hotspots, and conservation efforts targeted toward them could help avertthe loss of tropical reef biodiversity. Coral reefs fringe one-sixth of the world’scoastlines ( 1 ) and support hundreds of thou-sands of animal and plant species ( 2 ). Fifty-eightpercentoftheworld’sreefsarereportedto be threatened by human activities ( 3 ). Terres-trial agriculture, deforestation, and develop-ment are introducing large quantities of sedi-ment,nutrients,andotherpollutantsintocoastal R  E P O R T S 15 FEBRUARY 2002 VOL 295 SCIENCE www.sciencemag.org 1280
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