Journal of Archaeological Science (2003) 30, 275–280 doi:10.1006/jasc.2002.0834 The Sima de los Huesos Hominids Date to Beyond U/Th Equilibrium (>350 kyr) and Perhaps to 400–500 kyr: New Radiometric Dates James L. Bischoff, Donald D. Shamp U.S. Geological Survey, Menlo Park, CA 94025, U.S.A. Arantza Aramburu Department of Mineralogy and Petrology, University of Basque Country, Sarriena s/n, 48940 Leioa, Bizkaia, Spain Juan Luis Arsuaga Departamento de Paleontologia, Instituto de Geologia Econo´mica, Facultad de Ciencias Geolo´gicas, Universidad Complutense de Madrid, 28040 Madrid, Spain Eudald Carbonell Laboratori d’Arqueologia, Universitat rovira I Virgili, Plaza Imperial I, 43005 Terragona, Spain J. M. Bermudez de Castro Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientificas, Jose´ Gutie´rrez Abascal 2, 28006 Madrid, Spain (Received 10 January 2002, revised manuscript accepted 25 February 2002) The Sima de los Huesos site of the Atapuerca complex near Burgos, Spain contains the skeletal remains of at least 28 individuals in a mud breccia underlying an accumulation of the Middle Pleistocene cave bear (U. deningeri). Earlier dating estimates of 200 to 320 kyr were based on U-series and ESR methods applied to bones, made inaccurate by unquantifiable uranium cycling. We report here on a new discovery within the Sima de los Huesos of human bones stratigraphically underlying an in situ speleothem. U-series analyses of the speleothem shows the lower part to be at isotopic U/Th equilibrium, translating to a firm lower limit of 350 kyr for the SH hominids. Finite dates on the upper part suggest a speleothem growth rate of c. 1 cm/32 kyr. This rate, along with paleontological constraints, place the likely age of the hominids in the interval of 400 to 600 kyr.  2002 Elsevier Science Ltd. All rights reserved. Keywords: ATAPUERCA, SIMA DE LOS HUESOS, MIDDLE PLEISTOCENE, URANIUM-SERIES. Introduction Here, in an ancient mud-breccia were found the well- preserved remains of at least 28 human individuals, eep within the Cueva Mayor cave system of fragmented and scattered, lying stratigraphically below D the Atapuerca site near Burgos, Spain, far removed from any surface entrance is the enigmatic Sima de los Huesos (SH, ‘‘pit of the bones’’) complex, containing the world’s most extraordinary a jumble of bones of the Middle Pleistocene cave bear (U. deningeri). The SH collection now comprises more than 80% of the Middle Pleistocene record world-wide for the genus Homo and provides for an unprecedented accumulation of Middle Pleistocene fossil humans. study of within-population variations (Arsuaga et al., 275 0305–4403/03/$-see front matter  2002 Elsevier Science Ltd. All rights reserved. 276 J. L. Bischoff et al. Figure 1. Interpretive cross section of the Sima de los Huesos (no vertical exaggeration). The largest concentration of human and bear fossils is at B. Dated speleothem (unit 3) and position of newly discovered human bones is at SRA shown in the inset stratigraphic column. 1997a). The SH hominids are the evolutionary ances- bones have been recovered at SRB and only isolated tors to the Neandertals (Arsuaga et al., 1991, 1993 and bones from SRM, and up to now, none at SRA. The 1997b). Dating of the deposit is clearly of great impor- entire sequence is capped by a sheet of flowstone tance, but has been here-to-for problematical (Bischoff speleothem (Colada), generally earthy and impure. et al., 1997). Previous dating (Bischoff et al., 1997) has been limited by a lack of speleothems, other than the Colada, in stratigraphic context with the bones. U-series and Stratigraphy and Previous Dating radiocarbon dating indicates the Colada formed from The area of excavation (Figure 1) consists of two about 68 kyr to about 25 kyr. The range of U-series connected, sediment-filled chambers, the Rampa and nominal dates for 25 bear bones (88–220 kyr) and for the Sima de los Huesos proper. The Rampa is an 16 human bones (114 to 182 kyr) are similar and rather inclined 9 m long chamber at the foot of which the broad, but are clearly affected by irregular post- Sima de Los Huesos opens into an oblong 8 m by 4 m depositional uranium cycling. Nine additional bear chamber. The human fossils are concentrated in area B bones were analysed by the combined ESR and (Figure 1), in a mud-supported bone breccia. The U-series method (Bischoff et al., 1997). Dates for six of excavation has not yet reached bedrock at B so the these yielded 2004 kyr whereas the other three extent of the bone breccia is unknown. Three 1 m2 pits yielded dates of 3204 kyr. Thus, the earlier results were excavated in the Rampa, at the top (SRA), seemed to provide a firm minimum age of about midpoint (SRM) and foot (SRB). Each pit exposes 200 kyr for the human entry; and suggestive evidence about a metre and a half of section. A few human of possible entry prior to 320 kyr.  The Sima de los Huesos Hominids: New Radiometric Dates 277 Table 1. U-series analyses and derived dates of SRA-3 speleothem from the Sima de los Huesos, Atapuerca Below top USGS U Date 234 (cm) Lab # (ppm) U/238U 230 Th/232Th 230 Th/234U (kyr) Comments 1 01-201 0·760·003 1·410·017 20 0·7980·0125 1535 3 01-203 0·290·003 1·170·018 >100 0·9420·015 257+16/
14 3·5 01-204 0·280·002 1·100·019 >100 0·9490·019 281+28/
23 Hiatus 4 01-205 0·290·001 1·030·013 >100 0·9980·02 >350 230 4·5 01-181 0·320·0007 1·040·009 80 1·280·015 — Excess Th 5·5 01-180 0·530·003 1·030·018 70 1·040·031 >350 7 01-178 0·750·004 1·080·01 >100 0·9500·017 29025 8 01-163 0·550·002 1·020·01 >100 0·9660·019 >350 9·5 01-177 0·570·0016 1·020·008 >100 0·9960·02 >350 9 01-174 0·620·0018 1·020·008 >100 1·030·01 >350 230 10 01-171 0·600·002 1·010·01 >100 1·040·012 >350 Slight excess Th 11 01-170 0·600·002 1·030·01 >100 1·010·17 >350 12·0 01-169 0·600·002 1·100·009 >100 1·000·01 >350 13·5 01-159 0·750·002 1·000·009 >100 1·030·03 >350 New Discovery 0·6 ppm, and the 230Th/232Th ratios are all well in excess of 20, the limiting value below which extraneous During the 2001 field season excavation at SRA, (detrital) Th significantly affects the date (Bischoff & the top of the Rampa, was extended up slope. This Fitzpatrick, 1991). One of the samples yielded a finite excavation exposed a 14-cm thick in situ speleothem date of 290 kyr, whereas two others exhibited 230Th (Figure 1) lying stratigraphically beneath the Colada. activity in excess of its 234U parent (i.e. 230Th/ Immediately below this speleothem, bones belonging 234 U>1·0, Table 1). These differences from strict inter- to at least two complete bears (U. deningeri) were nal equilibrium we ascribe to slight post-depositional recovered, and among the bear bones two human mobility of 234U within the speleothem. Under strict phalanges were found. The phalanges are juvenile, closed system behaviour the U/Th method is capable of probably from the same individual. The newly exposed returning finite dates as old as 500 kyr (Ludwig et al., speleothem is clearly younger than the human bones, 1992), but because of the slight inhomogenieties ob- and is of high purity and crystallinity and, therefore, served in the present suite, we conservatively ascribe excellent material for U-series dating to provide a the limit to about 350 kyr. However, the 10 cm of minimum age for the human bones. The speleothem is speleothem thickness represented by the >350 kyr laminated (c. 1 cm laminae), is pure calcite, and con- dates could represent a significant amount of time tains less than 0·3 wt% organic carbon. The laminae beyond 350 kyr. truncate at about 4 cm below the top, representing a hiatus in speleothem growth. Limits on Maximum Age We consider possible constraints on how much beyond Dating Results 350 kyr the age of the SH assemblage could be. The We report here on the results of 14 samples for U-series growth rate of the upper part of the speleothem that were taken about every centimetre spanning the provides one estimate. The three finite dates above the entire 14 cm thickness. After acid dissolution, Th and hiatus plot on a straight line versus depth (Figure 2), U isotopes were isolated by anion exchange, and implying a linear growth rate of about 1 cm per 32 kyr isotopic ratios were measured by thermal ionization for the upper part of the speleothem. Applying this rate mass spectrometry (Edwards et al., 1986/87). Results to the lower part yields a 600 kyr age for the bottom of (Table 1) show that the three samples above the hiatus the speleothem. yield finite dates in stratigraphic order from 153 to Another estimate is derived from the dominant 281 kyr, a time spanning from the middle of Oxygen normal magnetization of the fossiliferous muds of the Isotope Stage (OIS) 6 to the middle of OIS 8 (Imbrie SH, giving a maximum lower limit of 780 kyr (Pare´s et al., 1984). This interval includes both glacial and et al., 2000). interglacial conditions. Below the hiatus, all samples The presence of Panthera leo in the SH (Garcı´a et al., are at, or close to internal isotopic equilibrium, defined 1997) suggests a maximum age of around 600 kyr; this by 230Th/234U and 234U/238U activity ratios of unity, being the oldest currently accepted age for this species yielding a (conservative) minimum age of 350 kyr. as found at Isernia (Garcı´a & Arsuaga, 1999). Corre- Uranium contents are relatively high averaging lation of the rodent fauna of the SH to the nearby 278 J. L. Bischoff et al. Figure 2. Depth plot of U/Th dates obtained on speleothem SRA-3. Samples analyzed from below the 4 cm hiatus are at internal isotopic equilibrium indicating an age beyond 350 kyr. The three dates from above the hiatus plot on a straight line versus depth implying a growth rate of 1 cm/32 kyr. Gran Dolina provides some other limits. Pliomys lenki Thus, the radiometric results are conclusive for an and Allocricetus bursae occur both in the SH and in age in excess of 350 kyr, with other constraints placing levels TD10 and TD11 of the Gran Dolina (Cuenco- a likely age in the interval of 400 to 500 kyr (OIS Besco´s et al., 1997, 1999) that yielded combined ESR- 12–14) for the SH hominids. U-series dates on mammal teeth of 308–418 kyr (Falgue`res et al., 1999). Moreover, the SH rodent fauna lacks the Lower Pleistocene vole Mimomys savini (Cuenco-Besco´s et al., 1997). This vole is found up to Evolutionary Implications level TD8 in the Gran Dolina (Cuenco-Besco´s et al., The SH humans are ancestral to Neandertals (Arsuaga 1999) that has yielded combined ESR-U-series dates et al., 1991, 1993, and 1997b). The main Neandertal on mammal teeth of 586 to 615 kyr (Falgue`res et al., apomorphy in the skull is a relative forward position of 1999). Thus, M. savini was present in the area up to the dentition resulting in midfacial prognathism, and a about 600 kyr ago, and its absence in the SH assem- retromolar space in the mandible. The SH midface, blage suggests a younger age. Further, genetic esti- however, shows a flexed maxilla, contrasting with the mates for the timing of the split between the ancestors typically flattened maxilla of Neandertals. More of Neandertal/modern lineages is on the order of incipient Neandertal traits are also found in the 500–600 kyr (Ingman et al., 2000; Krings et al., 1997; supraorbital torus and the occipital torus and supra- Krings et al., 1999; Ovchinnikov et al., 2000). These iniac area. There are many postcranial traits shared by estimates would require the SH hominids, already well the SH specimens and the Neandertal fossils, especially onto the Neanderthal/modern divide, to be younger. in the pelvis; however, the pelvic morphology seems to  The Sima de los Huesos Hominids: New Radiometric Dates 279 be primitive and not a specialization (Arsuaga et al., with an absence of Neandertal features. The appear- 1999). In sum, the presence of some Neandertal-like ance of the Neandertal traits in Europe earlier than traits show that Neandertals have roots in Europe at the appearance of modern human traits in Africa least as far back as the age of the SH hominids. could point to a different evolutionary rate in the two Another important European fossil is the continents. Swanscombe back skull, which looks clearly more Thus there could be at least three different lineages Neandertal-derived in the occipital bone morphology evolving at the time of the SH population: in Europe, than the SH specimens. Swanscombe seems to belong Neandertal ancestors (H. heidelbergensis), in Africa, to OIS 11, although this age is not based on radio- modern human ancestors (H. rodesiensis) and in China metric dating (Bowen et al., 1989; Stringer & Hublin, and Java, H. erectus. 1999). The new date of the SH sample, as old or perhaps older than Swanscombe, is consistent with the Acknowledgements primitive occipital morphology of the latter. The Mauer mandible is assigned to OIS 13, and the We thank Richard Klein for helpful discussion and for Arago sample to OIS 12. Some authors consider these suggestions concerning the faunal and DNA limits on specimens, and other European fossils, as part of a the age of SH hominids. The manuscript was improved species called Homo heidelbergensis that would be a by careful critical reading of an earlier draft by Robert common ancestor for both Neandertals and modern Rosenbauer and John Barron. humans, and that would have occurred throughout Europe, Africa and Asia (Rightmire, 1997; Stringer & References Hublin, 1999). In our opinion, however, all the Middle Arsuaga, J. L., Carretero, J. M., Martı´nez, I. & Gracia, A. (1991). Pleistocene European fossils, including the Mauer Cranial remains and long bones from Atapuerca/Ibeas (Spain). mandible and the Arago sample, exhibit more or less Journal of Human Evolution 20, 191–230. Arsuaga, J. L., Martı´nez, I., Gracia, A., Carretero, J. M. & incipient Neandertal traits and are thus ancestral Carbonell, E. (1993). Three new human skulls from the Sima de specifically to the Neandertals (Arsuaga et al., 1997b; los Huesos site in Sierra de Atapuerca, Spain. Nature 362, 534– Martı´nez & Arsuaga, 1997; Carbonell et al., 1995; 537. Bermu´dez de Castro et al., 1997). The last common Arsuaga, J. L., Martı´nez, I., Gracia, A., Carretero, J. M., Lorenzo, ancestor for Neandertals and modern humans is older C., Garcı´a, N. & Ortega, A. I. (1997a). Sima de los Huesos (Sierra de Atapuerca, Spain). The site. Journal of Human Evolution 33, in our opinion, and it is represented by the Lower 109–127. Pleistocene hominid fossils of Gran Dolina (Bermu´dez Arsuaga, J. L., Martı´nez, I., Gracia, A., Lorenzo, C. & Garcı´a, N. de Castro et al., 1977). A fragmentary braincase from (1997b). The Sima de los Huesos crania (Sierra de Atapuerca, Ceprano that is considered on geological grounds to Spain). A comparative study. Journal of Human Evolution 33, 219–281. date to the very early Middle Pleistocene or late Lower Arsuaga, J. L., Lorenzo, C., Carretero, J. M., Gracia, A., Martı´nez, Pleistocene (Ascenzi et al., 1996; Manzi et al., 2001) I., Garcı´a, N., Bermu´dez de Castro, J. M. & Carbonell, E. (1999). could belong to the same population. And, as noted A complete human pelvis from the Middle Pleistocene of Spain. above, the fossil DNA of Neandertal specimens points Nature 399, 255–258. to a split for the Neandertal and Modern Humans Ascenzi, A., Biddittu, I., Cassoli, P. F., Segre, A. G. & Segre- Naldini, E. (1996). A calvarium of late Homo erectus from lineage of around 500–600 kyr. Ceprano, Italy. Journal of Human Evolution 31, 409. The dating of the SH sample is also useful to place Bermu´dez de Castro, J. M., Arsuaga, J. L., Carbonell, E., Rosas, A., the human evolution in Europe in a broader evolution- Martı´nez, I. & Mosquera, M. (1997). A hominid from the Lower ary perspective. The Zhoukoudian H. erectus Skull 5, Pleistocene of Atapuerca, Spain: possible ancestor to Neandertals and Modern Humans. Science 276, 1392–1395. is dated by ESR on animal tooth enamel to OIS 8 Bischoff, J. L. & Fitzpatrick, J. A. (1991). U-series dating of impure (Gru¨n et al., 1997), but firmer new U/Th dating on carbonates: An isochron technique using total-sample dissolution. speleothem samples by Shen et al. (2001) place the Geochimica et Cosmochimica Acta 55, 543–554. skull in OIS 12-14 range. To the latter authors, the Bischoff, J. L., Fitzpatrick, J. A., Leo´n, L., Arsuaga, J. L., Falgue`res, Zhoukoudian H. erectus would represent a stage in C., Bahain, J. J. & Bullen, T. (1997). Geology and preliminary dating of the hominid-bearing sedimentary fill of the Sima de los human evolution anterior to the H. heidelbergensis/ Huesos Chamber, Cueva Mayor of the Sierra de Atapuerca, H. rodhesiensis stage, instead of a different clade. The Burgos, Spain. Journal of Human Evolution 33, 129–154. present dating of the SH sample to the OIS 12-14 range Bowen, D. Q., Hughes, S., Sykes, G. A. & Miller, G. H. (1989). places it more or less coeval with the Zhoukoudian Land-sea correlations in the Pleistocene based on isoleucine H. erectus. epimerization in non-marine molluscs. Nature 340, 49–51. Carbonell, E., Bermu´dez de Castro, J. M., Arsuaga, J. L., Dı´ez, J. C., Thus, our interpretation is that the European lineage Cuenca-Besco´s, G., Sala, R., Mosquera, M. & Rodrı´guez, X. P. evolved into the Neandertals whereas the East Asian (1995). Lower Pleistocene hominids and artifacts from Atapuerca- line could have survived in Java (as represented by the TD6 (Spain). Science 269, 826–830. Ngandong fossils) until its replacement by modern Cuenco-Besco´s, G., Laplana Conesa, C., Canudo, J. I. & Arsuaga, J. humans. With respect to Africa, the modern human L. (1997). Small mammals from Sima de los Huesos. Journal of Human Evolution 33, 175–190. apomorphies do not appear until the late Middle Cuenco-Besco´s, G., Laplana Conesa, C. & Canudo, J. I. (1999). Pleistocene. Before that, the African fossils show Biochronological implications of the Arvicolidae (Rodentia, primitive traits similar to those found in Europe, but Mammalia) from the Lower Pleistocene hominid-bearing level of 280 J. L. Bischoff et al. Trinchera Dolina 6 (TD6), Atapuerca Spain. Journal of Human Krings, M., Geisert, H., Schmitz, R. W., Krainitzki, H. & Pa¨a¨bo, S. Evolution 37, 353–373. (1999). DNA sequence of the mitochondrial hypervariable region Edwards, R., Chen, J. H. & Wasserburg, G. J. (1986/1987). 238U– II from the Neandertal type specimen. Proceedings of the National 234 U–230Th systematics and the precise measurement of time over Academy of Sciences 96, 5581–5585. the past 500,000 years. Earth and Planetary Science Letters 81, Ludwig, K. R., Simmons, K. R., Szabo, B. J., Winograd, I. J., 175–192. Lanwehr, J. M., Riggs, A. C. & Hoffman, R. J. (1992). Mass- Falgue`res, C., Bahain, J. J., Yokoyama, Y., Arsuaga, J. L., spectrometric 230Th–234U–238U dating of the Devils Hole calcite Bermu´dez de Castro, J. M., Carbonell, E., Bischoff, J. L. & vein. Science 258, 284–287. Dolo, J. M. (1999). Earliest humans in Europe: the age of TD6 Manzi, G., Mallegni, F. & Ascenzi, A. (2001). A cranium for the Gran Dolina, Atapuerca, Spain. Journal of Human Evolution 33, earliest Europeans: Phylogenetic position of the hominid from 343–352. Ceprano, Italy. Proceedings of the National Academy of Sciences Garcı´a, N., Arsuaga, J. L. & Torres, T. (1997). The carnivore USA 98, 10011–10016. remains from the Sima de los Huesos Middle Pleistocene site Martı´nez, I. & Arsuaga, J. L. (1997). The temporal bones from Sima (Sierra de Atapuerca, Spain). Journal of Human Evolution 33, de los Huesos Middle Pleistocene site (Sierra de Atapuerca, 155–174. Spain). A phylogenetic approach. Journal of Human Evolution 33, Garcı´a, N. & Arsuaga, J. L. (1999). Carnivores from the Early 283–318. Pleistocene hominid-bearing Trinchera Dolina 6 (Sierra de Ovchinnikov, I. V., Go¨therstro¨m, A., Romanova, G. P., Atapuerca, Spain). Journal of Human Evolution 37, 414–430. Kharitonov, V. M., Lide´n, K. & Goodwin, W. (2000). Molecular Gru¨n, R., Huang, Huan, P.-H., Wu, X., Stringer, C. B., Thorne, A. analysis of Neanderthal DNA from the northern Caucasus. G. & McCulloch, M. (1997). ESR analysis of teeth from the Nature 404, 490–493. palaeoanthropological site of Zhoukoudian, China). Journal of Pare´s, J. M., Pe´rez-Gonza´lez, A., Weil, A. & Arsuaga, J. L. (2000). Human Evolution 32, 83–91. On the age of the hominid fossils at the Sima de los Huesos, Sierra Imbrie, J., Hayes, J. D., Martinson, D. G., McIntyre, A., Mix, A. C., de Atapuerca, Spain: Paleomagnetic evidence. Journal of Physical Morley, J. J., Pisias, N. G., Prell, W. L. & Shackleton, N. J. (1984). Anthropology 111, 451–461. The orbital theory of Pleistocene climate: support from a revised chronology of the marine 18O record. In (A. L. Berger, J. Imbrie, Rightmire, G. P. (1997). Palaeontology: Deep roots for the J. D. Hays, G. Kukla & B. Saltzman, Eds) Milankovitch and Neanderthals. Nature 389, 917–918. Climate, Part 1. Dordrecht: D. Riedel, pp. 269–305. Shen, G., Ku, T.-L., Cheng, H., Edwards, R. L., Yuan, Z. & Ingman, M., Kaessmann, H., Pa¨a¨bo, S. & Gyllensten, U. (2000). Wang, Q. (2001). High-precision U-series dating of Locality 1 Mitochondrial genome variation and the origin of modern at Zhoukoudian, China. Journal of Human Evolution 41, 679– humans. Nature 408, 708–713. 688. Krings, M., Stone, A., Schmitz, R. W., Krainitzki, H., Stoneking, M. Stringer, C. B. & Hublin, J.-J. (1999). New age estimates for the & Pa¨a¨bo, S. (1997). Neanderthal DNA sequences and the origin of Swanscombe hominid, and their significance for human evolution. modern humans. Cell 90, 19–30. Journal of Human Evolution 37, 873–877.