Proc. Natl. Acad. Sci. USAVol. 93, pp. 3016-3020, April 1996Evolution

Dated co-occurrence of Homo erectus and Gigantopithecus fromTham Khuyen Cave, Vietnam

(paleoanthropology/ESR dating/uranium-thorium dating/Pleistocene geochronology)

RUSSELL CIOCHON*, VU THE LONGt,ROY LARICK$, LUIS GONZALEZ§, RAINER GRJUN¶, JOHN DE Vosil,CHARLES YONGE**, LOIS TAYLOR¶, HIROYUKI YOSHIDAtt, AND MARK REAGAN§*Departments of Anthropology and Pediatric Dentistry and §Department of Geology and Center for Global and Regional Environmental Research, TheUniversity of Iowa, Iowa City, IA 52242; tInstitute of Archaeology, National Center for Social Sciences, Hanoi, Vietnam; tDepartment of Anthropology,University of Massachusetts, Amherst, MA 01003; ¶Quaternary Dating Research Centre, Research School of Pacific and Asian Studies, and ttResearchSchool of Chemistry, Australian National University, Canberra ACT 0200, Australia; IINational Museum of Natural History, P.O. Box 9517, 2300 RALeiden, The Netherlands; and **Department of Physics and Astronomy, University of Calgary, Calgary AB T2N 1N4 Canada

Communicated by F. Clark Howell, University of California, Berkeley, CA, December 21, 1995 (received for review October 3, 1995)

ABSTRACT Tham Khuyen Cave (Lang Son Province,northern Vietnam) is one of the more significant sites to yieldfossil vertebrates in east Asia. During the mid-1960s, excava-tion in a suite of deposits produced important hominoiddental remains of middle Pleistocene age. We undertake morerigorous analyses of these sediments to understand the fluvialdynamics of Pleistocene cave infilling as they determine howskeletal elements accumulate within Tham Khuyen and othereast Asian sites. Uranium/thorium series analysis of spe-leothems brackets the Pleistocene chronology for breaching,infilling, and exhuming the regional paleokarst. Clast analysisindicates sedimentary constituents, including hominoid teethand cranial fragments, accumulated from very short distancesand under low fluvial energy. Electron spin resonance anal-ysis of vertebrate tooth enamel and sediments shows that themain fossil-bearing suite (S1-S3) was deposited about 475thousand years ago. Among the hominoid teeth excavatedfrom S1-S3, some represent Homo erectus and Gigantopithecusblacki. Criteria are defined to differentiate these teeth frommore numerous Pongo pygmaeus elements. The dated co-occurrence ofHomo erectus and Gigantopithecus blacki at ThamKhuyen helps to establish the long co-existence of these twospecies throughout east Asia during the Early and MiddlePleistocene.

Tham Khuyen Cave lies 125 km NNE of Hanoi and 30 kmWSW of the Chinese border in Lang Son Province of northernVietnam (Fig. la). A regional survey in 1964 identified thepaleontological importance of the site (1), and excavations in1965 recovered significant hominoid fossils (2-5). ThamKhuyen has become the best-known hominoid fossil site inVietnam and one of the better-known in east Asia. In the west,Tham Khuyen is reputed for its geological association ofHomoerectus and Gigantopithecus blacki teeth (6-8) and, morerecently, for the taxonomic status of its small sample oforangutan teeth (9, 10). Despite 30 years of investigations,however, basic questions remain about the age of the deposits,the geological processes of sedimentary (and fossil) infilling,and the precise taxonomic attribution for many hominoidelements. We focus on these issues through two lines ofinvestigation: (i) Studies of the Pleistocene fluvial dynamics forthe Tham Khuyen locality suggest that the cave accumulatedindividual teeth through localized, low-energy fluvial andeluvial events. (ii) Electron spin resonance (ESR) analysis ofvertebrate tooth enamel and sediments and uranium/thorium(U/Th) series analysis of speleothems indicate the age for themore important accumulations.

The publication costs of this article were defrayed in part by page chargepayment. This article must therefore be hereby marked "advertisement" inaccordance with 18 U.S.C. §1734 solely to indicate this fact.

Sedimentary DynamicsKarst hills and towers of Carboniferous limestones dominatethe physiography of the province, with recessively erodedoutcrops of intercalated sandstones also providing significantlandscape features (Fig. 1). Tham Khuyen Cave itself issituated 7 km SE of the administrative headquarters for BinhGia District, a few hundred meters W of Lang Vech village,and some 20 m above the valley bottom. The cave containsinfilled passages on two levels (6 m apart) with fossiliferousdeposits confined to the upper level. The sedimentary natureof the upper level deposit is most evident in an area 10 m Nof the cave entrance (Fig. lc, right), where excavators identi-fied a dark red, fossiliferous cave "breccia." In this section, wedesignate 17 sedimentological units representing three lithol-ogies (Fig. lc, right): a basal fluvial conglomerate (C1), 12sandstone/siltstone units (S1-S12), and four travertine/silt-stones (T1-T4) interbedded with S1-S12. Most units exhibitsharp erosional surfaces and variable degrees of calcite ce-mentation. The sandy/silty fluvial conglomerate (C1) ispresent throughout the base of the section. Its clasts consist ofwell-rounded polycrystalline quartz, rounded-to-angular ce-mented cave sediment and soil (pebble-to-granule size), andphosphatic granules. Angular clasts, mostly quartz and sand-stone, are also present (as granules-to-coarse sand) as are rarecobbles and boulders. Unit C1 was certainly deposited alongthe banks of a river that flowed through all passages in thepresent escarpment. Given this fluvial character, the silicatesderive either from formations across the valley or from thepaleodrainage of igneous basement rocks. Fine sediment(sand/silt matrix) and phosphatic grains derive from karst soilsdeveloped on slope deposits (including cave entrances) and theflood plain.

Units S1-S12 are mixtures of overbank deposits and mate-rials eluviated from above the cave. Most clasts fall in the rangeof silt-to-sand, with minor though variable amounts of granulesand pebbles, and very rare cobbles and boulders. Stringers andlenses of pebble conglomerates and granule-bearing sand-stones and/or siltstones are common above some of the sharpdiscontinuities. Small laminated pockets and even cross-bedded lenses are also present, particularly in unit S3. Clayeysoil nodules appear in all units as do pebble-size clasts ofcalcite-cemented sediment reworked from pre-existing ce-mented cave deposits. Sediment color generally varies withcalcite cementation. Poorly cemented sediments are yellowish-red, while well-cemented sectors are brownish-yellow to paleyellow. Units S1-S3 form a homogeneous sedimentary suitethat corresponds to the fossiliferous breccia of the originalreports (1-5). The depositional environment for the suite musthave been complex, but of lower energy levels than previouslyinterpreted. The generally fine texture of the sediments sug-gests an alluvial regime of low velocity, with rare cobble and

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FIG.1.Location, geomorphology, andstrampl Khuyen Cave.(a and b) The ThamKhuyen locality is defined by a large N-S valleywhoseflanks exposil Bearbonates W (ris ingto 660 ), and silicates E (reachimentains an underfit stream (320 m) that meanders

over thick clastic sediments to suggest a major river flowing S-to-N in the past. Caverns exposed along the W escarpment, such as Tham Khuyen,Tham Hai, and Keo Leng (3 km NW of Tham Khuyen), record three stages of Pleistocene evolution for an ancient karst system. The caves wereonce side passages within an underground drainage that was breached from above to form the present valley. The breached cavities were then infilledas the valley episodically choked with alluvium, and they were finally exhumed to produce the present paleokarst features. Dates discussed belowindicate infilling proceeded at least from the middle Pleistocene. An interred stalagmite from Keo Leng (U/Th age range, 42 ka to 37 ka) suggestsa very late Pleistocene transition from infilling to exhumation. (c) Frontal profile of Tham Khuyen Cave, N or right of main entrance. Stratigraphicsection (right) lies 10 m N of cave entrance. Unit Cl, sandy/silty fluvial conglomerate forms the basal infilling throughout the cave passages. Clastsconsist ofwell-rounded polycrystalline quartz, rounded-to-angular cemented cave sediment and soil phosphatic granules, and rare sandstone cobblesand boulders. Fossiliferous units S1-S12 are mixtures of overbank deposits and materials eluviated from above the cave. Clasts range from silt to

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sand, with minor amounts of granules and pebbles and very rare sandstone cobbles and boulders. Travertines T1-T4 contain flowstone or cave

pool deposits that indicate extended periods of nondeposition and consequent speleothem formation. Sedimentation in the cave was episodic as

suggested by the sharp discontinuities between sediment units. Entrance to the intermediate tunnel (left) is located 5 m N of the cave entrance

(5 m S of the main sediment outcrop and stratigraphic section). The tunnel is filled completely with highly fossiliferous sedimentary suite S1-S3.The ESR samples come from poorly cemented pockets of sediment within the tunnel.

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larger-sized clasts incorporated as eluviation from within orabove the cave. Significant in this regard is the calcite-cemented sediment reworked from older infills into clasts.Given the high friability of this material, its preservation inclastic form indicates a nearby source as well as low-energytransport. Consequently, the fragmentary state of the fossilvertebrates must be explained by other than the immediatedepositional environment (9).

Absolute Age. The "Stegodon-Ailuropoda fauna" at ThamKhuyen has always suggested an early to middle Pleistoceneage for this deposit, and pollen analysis seems to corroborate(4, 5). ESR and U/Th series analyses increase the precision.ESR analyses address the S1-S3 suite as preserved within asmall horizontal tunnel, intermediate between the cave en-trance and the main sediment outcrop (Fig. lc, left). Fifteenfossil teeth were extracted from poorly cemented sediment attwo pocket-like sites within the tunnel. Procedures followthose of Griin (11-13), as presented in Table 1. The problemof ESR for dating tooth enamel lies in the uncertain U-uptakehistory for a given specimen, with early uptake (EU) and linearuptake (LU) alternatives (11, 12). Independent comparisonssuggest that true age usually lies between the two models (15,16). Age estimates are therefore computed for both models(average EU = 404 + 51 ka; average LU = 534 + 87 ka) andaveraged to give a general specimen estimate of 475 + 125 ka.The four travertines contain significant amounts of flowstone/dripstone and even calcite crystal arrays that normally form instill cave pools. Calcite crystals within a T2 speleothem arepure enough to analyze with U/Th methods, yielding an ageestimate of 117 + 30 ka (1 r), determined from a uraniumconcentration of 0.035 + 0.004 ppm, 232-thorium not detect-able [(234U)/(238U) = 1.346 + 0.18, (230Th)/(234U) = 0.685 +0.101)]. Unit T2 lies in the middle of the stratigraphic se-quence, one travertine (T1) and 5 sandstone/siltstone units(S4-S8) above the S1-S3 suite (Fig. lc, right). Consequently,the U/Th date for the T2 speleothem corroborates the averageESR date for the S1-S3 suite.

Hominoid TaxonomyHominoids comprise about 5% of approximately 2000 speci-mens of fossil vertebrates from Tham Khuyen Cave [faunal list(8)]. Most are isolated teeth recovered within the sedimentarysuite S1-S3. Fragmentary condition complicates taxonomicassignment as, in considering each tooth a biological individ-ual, the number of individuals multiplies immensely, therebyseeming to increase assemblage diversity. Understanding thiseffect, Vietnamese scientists are conservative in their speciesattributions, relating hominoid fossils to existing taxa (17-19).In the case of orangutan, for example, all teeth are assigned tothe extant species Pongo pygmaeus. For Tham Khuyen, taxo-nomic problems lie rather in misidentification at the genuslevel, especially between Pongo and other hominoid genera.For example, large Pongo teeth have been termed Giganto-pithecus while small worn Pongo teeth have been called Homo.Distinctions between Homo and Pongo molars are especiallytroublesome as they appeal to minor occlusal features thatbecome less visible with wear as Franz Weidenreich saw nearly60 years ago. Regarding occlusal wrinkling, Weidenreich ob-serves that "there is no doubt that wrinkles represent acharacteristic feature of the Sinanthropus molar and that theydisappear gradually in the course of human evolution" (ref. 20,p. 103). Obviously, wrinkling becomes less diagnostic whencomparing heavily worn molars ofHomo. From the other side,Weidenreich cautions that even slightly worn upper molars ofPongo can occasionally exhibit "a pattern of the chewingsurface surprisingly similar to that of Sinanthropus" (ref. 20, p.66). In this same passage, nevertheless, Weidenreich identifiesthe distinguishing feature least sensitive to extreme wear:

upper molars of Pongo uniquely exhibit a doubled crista

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transversa, the mesial trigon crest uniting the paracone andprotocone (ref. 20, p. 66). Peripheral placement of the molarcusps is another diagnostic feature of Homo erectus that standsout on all but the most worn specimens.Homo and Gigantopithecus. Skeletal elements of Homo

erectus are known from Zhoukoudian in northern China toSangiran in eastern Java. This taxon was first identified atTham Khuyen in 1967 by Kha and Bao (21) based on dentalelements excavated in 1965. Kha and Cuong (22-24) laterargued that as many as nine isolated specimens representHomo erectus. Reanalysis of the Tham Khuyen dental sampleconfirms hominid status for five specimens [TK 65/50 (M1),TK 65/53 (M'), TK 65/105 (M2), TK 65/167 (C'), and TK65/8 (dm1) (Fig. 2)] and demonstrates close affinities withequivalent teeth from Zhoukoudian. For the three uppermolars, the human pattern of a single crista transversa andperipheral cusps is apparent. Occlusal morphology for thesethree is very similar to that for the upper molars fromZhoukoudian (ref. 20, plate 14, figures 119-120). In regard tometrics, crown areas (MD x BL) for the two upper first molars

(TK 65/50 = 151 and TK 65/53 = 161) fall within the range(117-162) for six equivalent teeth known from Zhoukoudian,and crown area for the second upper molar (TK 65/105 = 152)falls just above the range (129-149) for the seven equivalentZhoukoudian specimens (ref. 20; table XVI). A similar patternmay be observed for the crown area of upper canine (TK65/167 = 97) which falls within the range (83-109) of six uppercanines from Zhoukoudian (ref. 20; table VII). There isgeneral agreement that the deciduous molar TK 65/8 repre-sents Homo erectus. However, four other teeth attributed toHomo erectus by Kha and Cuong (22-24) either fall outside themetric ranges for Zhoukoudian or lack diagnostic discretefeatures.

Fossil teeth of Gigantopithecus blacki are known fromcentral and southern China, as far south as Daxin Cave,Guangxi Province (25). The identification of this taxon atTham Khuyen Cave, first made by Khai and Long (26), extendsthe range 140 km SW. Lower left canine TK 65/122 (Fig. 2)can be attributed without doubt to Gigantopithecus blacki,based on comparisons with seven lower canines of Giganto-

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FIG. 2. Gigantopithecus blacki canine (left) and Homo erectus molars (right) from Tham Khuyen. TK 65/122, left lower C of Gigantopithecusblacki (MD = 13.0, LL = 18.0, CH = 19.8), TK 65/105 (top right) left upper M2 (MD = 12.0, BL = 12.7), TK 65/50 (bottom right) left upperMl (MD = 11.7, BL = 12.9). Scale bar is in cm. Other hominid teeth identified from Tham Khuyen include TK 65/53, a right upper Ml (MD= 12.1, BL = 13.3), TK 65/167 left upper C (MD = 9.9, LL = 9.8), and TK 65/8, a left upper deciduous Ml (MD = 9.9, BL = 10.8).

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pithecus from China. For these canines Woo (27) calculates ashape index (LL x 100 + MD) with a range of 122-144 (table19 in ref. 27). The index for TK 65/122 (= 139) falls squarelywithin the range of Gigantopithecus blacki. The lower caninesof Chinese Gigantopithecus are very robust and low-crowned,with wear patterns distinct among the Hominoidea. The entirelingual surface (to the apex of the crown) gradually wears flatleaving the tooth wedge-shaped with a sharp cuting edge. TK65/122 reveals this same unique morphological pattern. Withregard to individual comparisons with the seven Gigantopithe-cus canines, TK 65/122 matches the morphology, wear stage,and overall size of PA 27 from Liucheng cave, Guangxi (plate12 in ref. 27), one of the better preserved Gigantopithecuscanines. One other specimen from Tham Khuyen, left lowerincisor TK 65/146, may be attributed to Gigantopithecus blackibased on its buccal-lingual compression, peg-like morphology,and large size. However, joint reanalysis of three other teethoriginally identified as Gigantopithecus [TK 65/61 (right uppercentral incisor), TK 65/124 (left lower incisor), and one otherleft incisor (un-numbered)], are now assigned to Pongo pyg-maeus.

Discussion and Conclusion

Nominally we report the absolute ages for the more significantpaleontological specimens from Tham Khuyen. We proceed animportant step further, however, by linking the fossils andradiometric analysis with the sedimentary dynamics of theTham Khuyen locality to reach two conclusions with implica-tions. First, clast and U/Th series analyses show that whilefluvial processes helped to accumulate skeletal fragments andindividual teeth within the cave, other events and processesfragmented the elements prior to interment. We now mustconsider the role of scavengers in retrieving carcasses or bonesfrom the locality and fragmenting them within the site. Scav-enged bone accumulations play critical roles in the taphonomyof South African early hominid cave sites (28). East Asian sitessuch as Tham Khuyen certainly have bone accumulations ascomplex as their South African counterparts. Second, radio-metric analyses of sediments and fossils suggest thatHomo andGigantopithecus co-occur at Tham Khuyen about a half millionyears ago. It is through this dated co-occurrence that we tieTham Khuyen with larger issues of human evolution.Homo and Gigantopithecus do co-occur at two other sites:

Jianshi Cave, Hubei, China (29), and Longgupo Cave, Sichuan,China (30). Like Tham Khuyen, these localities may haveaccumulated the remains of open-dwelling fauna, not neces-sarily cave inhabitants. Thus, while each individual site holdsevidence for co-occurrence, together they indicate that Homoand Gigantopithecus co-existed on a region-wide basis. More-over, the two lineages shared a common range in east Asia fora very long period. We have recently dated the principaldeposits at Longgupo Cave to more than 1.5 Ma, and perhapsto 1.9 Ma (30). With the Tham Khuyen co-occurrence of 475ka, it is evident that Homo and Gigantopithecus co-existed formore than one million years. During this co-existence in Asia(throughout the early and middle Pleistocene), Gigantopithe-cus blacki increases in size but shows little morphologicalchange while hominids undergo speciation. East Asian earlyhominids thus present two forms: a true Plio-PleistoceneHomo (species undetermined but with affinities to Homoergaster and Homo habilis) at Longgupo (30) and middlePleistocene Homo erectus, sensu stricto, at Tham Khuyen. Itthus becomes clear that east and southeast Asia hold a very

long and complex sequence of Pleistocene human evolution,comparable, in fact, to that of East or South Africa. To pushthe intercontinental comparison further, given the diversity oftheir hominid samples as well as their scavenged, fluviatilebone accumulations, both Tham Khuyen and Longgupo are ascomplex as the South African cave sites. Our studies at ThamKhuyen demonstrate that the east Asian sites will become mostimportant for understanding the totality of human evolution.

Field research during the 1993 season was supported by the L.S.B.Leakey Foundation, the Wenner-Gren Foundation for Anthropolog-ical Research, and the University of Iowa (UI) Committee on Inter-national Travel. Laboratory analysis was funded by the HumanEvolution Research Fund at the UI Foundation, the UI CarverResearch Initiative Grants Program, and the UI Sedimentary Geo-chemistry Laboratory. M. McCulloch (Research School of EarthSciences (RSES, Canberra) provided access to ICP-MS. G. Mortimerand L. Kinsley (RSES, Canberra) prepared samples and evaluatedICP-MS results.

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2. Cu6ng, N. L. (1971) Khao Co Hoc 11/12, 7-11.3. Kha, L. T. & Cu6ng, N. L. (1975) Nhung Phat Hien Moi Ve Khao

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eries and New Views on SomeArchaeological Problems in Vietnam,Papers presented at the 14th Pacific Scientific Congress,Khabarovsk, USSR (Committee on Social Sciences, Hanoi), pp.14-23.

19. Cu6ng, N. L. (1985) in Menschwerdung-Biotischer und Gesell-schaftlicher Entwicklungsprozess, eds. Herrmann, J. & Ullrich, H.(Academy, Berlin), pp. 96-102.

20. Weidenreich, F. (1937) Paleontol. Sinica (new series) Dl, 1-180(text); 1-121 (atlas).

21. Kha, L. T. & Bao, T. V. (1967) in Doc tai Hoi nghi thong bao khaoco hom nam 1967, 12-17.

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