Human hyoid bones from the middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, Spain)

This study describes and compares two hyoid bones from the middle Pleistocene site of the Sima de los Huesos in the Sierra de Atapuerca (Spain). The Atapuerca SH hyoids are humanlike in both their morphology and dimensions, and they clearly differ from the hyoid bones of chimpanzees and Australopithecus afarensis. Their comparison with the Neandertal specimens Kebara 2 and SDR-034 makes it possible to begin to approach the question of temporal variation and sexual dimorphism in this bone in fossil humans. The results presented here show that the degree of metric and anatomical variation in the fossil sample was similar in magnitude and kind to living humans. Modern hyoid morphology was present by at least 530 kya and appears to represent a shared derived feature of the modern human and Neandertal evolutionary lineages inherited from their last common ancestor.     

Non-masticatory uses of anterior teeth of Sima de los Huesos individuals (Sierra de Atapuerca, Spain)

In this study we examine the labial and occlusal surfaces of incisors and canines of hominins recovered from the Sima de los Huesos (SH), middle Pleistocene site, in order to establish the possible extra-masticatory use of anterior teeth. We have compared the microwear of these fossils with microwear from the anterior teeth of Australian Aborigines, a population characterized by ethnographic evidence of the use of their teeth as a third hand. These two samples of teeth were microscopically analyzed using Scanning Electron Microscopy (SEM). Our results support the “cultural” origin of microwear observed on fossil teeth: we conclude that the SH hominins used their anterior teeth as a “third hand” for para- or extra-masticatory activities.     

Early Pleistocene human mandible from Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain): a comparative morphological study

We present a detailed morphological comparative study of the hominin mandible ATE9-1 recovered in 2007 from the Sima del Elefante cave site in Sierra de Atapuerca, Burgos, northern Spain. Paleomagnetic analyses, biostratigraphical studies, and quantitative data obtained through nuclide cosmogenic methods, place this specimen in the Early Pleistocene (1.2-1.3 Ma). This finding, together with archaeological evidence from different European sites, suggests that Western Europe was colonised shortly after the first hominin expansion out of Africa around the Olduvai subchron. Our analysis of the ATE9-1 mandible includes a geometric morphometric analysis of the lower second premolar (LP₄), a combined and detailed external and internal assessment of ATE9-1 roots through CT and microCT techniques, as well as a comparative study of mandibular and other dental features. This analysis reveals some primitive Homo traits on the external aspect of the symphysis and the dentition shared with early African Homo and the Dmanisi hominins. In contrast, other mandibular traits on the internal aspect of the symphysis are derived with regard to African early Homo, indicating unexpectedly large departures from patterns observed in Africa. Reaching the most occidental part of the Eurasian continent implies that the first African emigrants had to cross narrow corridors and to overcome geographic barriers favouring genetic drift, long isolation periods, and adaptation to new climatic and seasonal conditions. Given these conditions and that we are dealing with a long time period, it is possible that one or more speciation events could have occurred in this extreme part of Eurasia during the Early Pleistocene, originating in the lineages represented by the Sima del Elefante-TE9 hominins and possibly by the Gran Dolina-TD6 hominins. In the absence of any additional evidence, we prefer not include the specimen ATE9-1 in any named taxon and refer to it as Homo sp.     

Nonocclusal dental microwear analysis of 300,000-year-old Homo heilderbergensis teeth from Sima de los Huesos (Sierra de Atapuerca, Spain)

Casts of nonocclusal enamel surfaces of 190 teeth from the Middle Pleistocene site of Sima de los Huesos have been micrographed by scanning electron microscopy. Microscopic analyses of striation density and length by orientation show distinct patterns of intrapopulation variability. Significant differences in the number and length of the striations by orientation are found between maxillary and mandibular teeth. This probably reflects differences in the mechanical forces involved in the process of chewing food. Significant differences are present between isolated and in situ teeth that could be caused by postdepositional processes differentially affecting the isolated teeth. In addition, a distinct and very unusual striation pattern is observed in a sample of teeth that can be explained only by a strong nondietary, most probably postmortem abrasion of the enamel surfaces. These teeth have a very high density of scratches, shorter in length than those found on other teeth, that are not indicative of dietary habits. No known depositional process may account for the presence of such postmortem wear since heavy transportation of materials within the clayish sediments has been discarded for the site. Despite this, a characteristic dietary striation pattern can be observed in most of the teeth analyzed. Most likely the diet of the Homo heidelbergensis hominids from Sima de los Huesos was highly abrasive, probably with a large dependence on hard, poorly processed plant foods, such as roots, stems, and seeds. A highly significant sex-related difference in the striation pattern can also be observed in the teeth analyzed, suggesting a differential consistency in the foods eaten by females and males.     

Endocranial traits of the Sima de los Huesos (Atapuerca,Spain) and Petralona (Chalkidiki,Greece) Middle Pleistocene ursids. Phylogenetic and biochronological implications

A complete cranium of Ursus deningeri from Petralona (Chalkidiki, Greece) covered by a thick carbonate crust has been virtually liberated through CT scan and 3D image reconstruction, and compared with a specimen from the Sima de los Huesos, Sierra de Atapuerca (Spain) Middle Pleistocene site. X-ray computed tomography allowed for the identification of previously unrecognized and phylogenetically relevant traits. Analysis of these traits and an additional series of classically defined traits demonstrate the near identity of these specimens, thereby, confirming an early stage of the speloid “(cave bear)” condition. The replicate luminescence ages obtained for the SH deposit provide a combined minimum age estimate of 427 ± 12 ka for the underlying fossils. Based on a series of primitive and derived morphological features of these two crania, a similar age is here proposed for the Petralona and SH U. deningeri.     

Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain)

Systematic excavations at the site of the Sima de los Huesos (SH) in the Sierra de Atapuerca (Burgos, Spain) have allowed us to reconstruct 27 complete long bones of the human species Homo heidelbergensis. The SH sample is used here, together with a sample of 39 complete Homo neanderthalensis long bones and 17 complete early Homo sapiens (Skhul/Qafzeh) long bones, to compare the stature of these three different human species. Stature is estimated for each bone using race- and sex-independent regression formulae, yielding an average stature for each bone within each taxon. The mean length of each long bone from SH is significantly greater (p < 0.05) than the corresponding mean values in the Neandertal sample. The stature has been calculated for male and female specimens separately, averaging both means to calculate a general mean. This general mean stature for the entire sample of long bones is 163.6 cm for the SH hominins, 160.6 cm for Neandertals and 177.4 cm for early modern humans. Despite some overlap in the ranges of variation, all mean values in the SH sample (whether considering isolated bones, the upper or lower limb, males or females or more complete individuals) are larger than those of Neandertals. Given the strong relationship between long bone length and stature, we conclude that SH hominins represent a slightly taller population or species than the Neandertals. However, compared with living European Mediterranean populations, neither the Sima de los Huesos hominins nor the Neandertals should be considered ‘short’ people. In fact, the average stature within the genus Homo seems to have changed little over the course of the last two million years, since the appearance of Homo ergaster in East Africa. It is only with the emergence of H. sapiens, whose earliest representatives were ‘very tall’, that a significant increase in stature can be documented.     

Right handedness of Homo heidelbergensis from Sima de los Huesos (Atapuerca, Spain) 500,000 years ago

Handedness is a product of brain specialization, which in turn seems to be responsible for the higher cognitive capabilities of humans, such as language and technology. Handedness in living humans is well established and shows the highest degree of manual specialization. Studies on hand laterality in nonhuman primates, particularly in chimpanzees, remain a matter of controversy as results tend to vary depending on factors such as the tasks performed and the environment in which the individuals live. Studies in several disciplines have attempted to determine where in the course of human evolution handedness established itself, with evidence collected from sources such as paleoneurological analyses, stone tool flaking, zooarchaeological studies and dental wear analyses, the last one of which have proven the most reliable source of information. Here we report an experimental and paleoanthropological study on hand laterality of a sample of 28 hominids from Sima de los Huesos (Atapuerca, Spain), dated at about 500,000 years ago, and compare our results with dental microwear analysis in other fossil samples such as that from Krapina (Croatia), as well as modern traditional societies. Our results indicate that European Middle Pleistocene Homo heidelbergensis was already as right-handed as modern populations.     

Early Pleistocene human mandible from Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain): a palaeopathological study

Here we present a detailed palaeopathological study of the hominin mandible ATE9-1 found at the Sima del Elefante site (TE), Sierra de Atapuerca, Spain. This fossil represents the earliest hominin remains from Western Europe with an age of ca. 1.3 Ma. The specimen displays several dento-gnathic lesions; the antiquity and geographic location of this fossil justifies a detailed palaeopathological study to determine if the pathologies have significantly altered taxonomically relevant features. Our study reveals severe dental attrition combined with generalized hypercementosis, alveolar root exposure, mild periodontal disease, tooth dislocation, and an anomalous occlusal plane. We have also observed calculus deposits, two cystic lesions and an anomalous wear facet compatible with tooth picking. The majority of these pathological signs can be explained by compensatory eruption. We propose that these lesions are associated as causes, consequences, and amplifiers of one another within the framework of heavy and even traumatic occlusion, masticatory habits, or both traumatic occlusion and masticatory habits. Despite the severity of these lesions, occlusion was at least partially functional so it was unlikely to influence the survival of this individual. In addition, the lesions do not prohibit the taxonomic assessment of the mandible.     

On the age of the hominid fossils at the Sima de los Huesos, Sierra de Atapuerca, Spain: paleomagnetic evidence

We report new paleomagnetic data for the Middle Pleistocene hominid-bearing strata in the Sima de los Huesos, North Spain. Sediments (brown muds with human and bear fossils and the underlying sterile clayey and sandy unit) preserve both normal and reversed magnetic components. The sterile unit has exclusively reversed magnetization, dating back to the Matuyama Chron, and thus is Lower Pleistocene in age. The overlying fossiliferous muds have a dominant normal magnetization that overprints a partially resolved reversed magnetization. These data are compatible with one of the reversal events that occurred during the Brunhes Chron. Combined with the existing U-series dates and evidence from the macro- and microfauna, these paleomagnetic results suggest an age of the hominid fossils between 325 to 205 ka, whereas the underlying sand and silts are older than 780 ka.     

New foot remains from the Gran Dolina-TD6 Early Pleistocene site (Sierra de Atapuerca, Burgos, Spain)

This paper presents and describes new foot fossils from the species Homo antecessor, found in level TD6 of the site of Gran Dolina (Sierra de Atapuerca, Burgos, Spain). These new fossils consist of an almost complete left talus (ATD6-95) and the proximal three-quarters of a right fourth metatarsal (ATD6-124). The talus ATD6-95 is tentatively assigned to Hominin 10 of the TD6 sample, an adult male specimen with which the second metatarsal ATD6-70+107 (already published) is also tentatively associated. Analysis of these fossils and other postcranial remains has made possible to estimate a stature similar to those of the specimens from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain). The morphology of the TD6 metatarsals does not differ significantly from that of modern humans, Neanderthals and the specimens from Sima de los Huesos. Talus ATD6-95, however, differs from the rest of the comparative samples in being long and high, having a long and wide trochlea, and displaying a proportionally short neck.     

Paleoecological and microenvironmental aspects of the first European hominids inferred from the taphonomy of small mammals (Sima del Elefante,Sierra de Atapuerca,Spain)

Unit TE9 of the Sima del Elefante (Sierra de Atapuerca, Burgos, Spain), where the remains of Homo sp. have been discovered (1.2–1.3 Ma), is also a level rich in small mammals. The taphonomic study of these small vertebrates sheds light on the landscape that provided the setting for the activities of these early hominids and allows us to describe what the cave was like during the formation of the level. Small mammal predators identified in the study indicate that during this period the Sierra de Atapuerca was part of a large biome consisting of semi-open riparian forests with meadows nearby. Postdepositional alterations reveal that the production of fossils took place outside the cave, being transported inside by water currents. During the formation of TE9, the cave presented conditions of high humidity, which made it difficult for hominids to establish occupations inside, although these conditions became somewhat less severe in TE9c, the sublevel where human remains are found.     

Matuyama-age lithic tools from the Sima del Elefante site, Atapuerca (northern Spain)

Paleomagnetic results obtained from the sedimentary fill at the Sima del Elefante site in Atapuerca, Spain, reveal a geomagnetic reversal, interpreted as the Matuyama-Brunhes boundary (0.78 Ma). The uppermost lithostratigraphic units (E17 through E19), which contain Mode II and III archaeological assemblages, display normal polarity magnetization, whereas the six lowermost units (E9 through E16) yield negative latitudinal virtual geomagnetic pole positions. Units E9 through E13, all of which display reverse magnetic polarity, contain Mode I (Oldowan) lithic tools, testifying to the presence of humans in the early Pleistocene (0.78-1.77 Ma).     

Restauration d’un fémur fossile humain du site de la Sima de los Huesos (Atapuerca, Espagne)

A fossil human femur of Homo heidelbergensis from the site of the Sima de los Huesos (Atapuerca, Spain) was reconstructed from two main proximal and distal portions and numerous smaller fragments from the diaphysis. The use of an evaporative process to separate the bone fragments during their restoration represents an innovative approach in restoring paleontological materials and the intervention has resulted in the reconstruction of a complete femur. To avoid excessive manipulation of the reconstructed femur, a mold (negative) and cast (positive) were made of the restored specimen. This case study provides general protocols which can be widely applied to the restoration of paleontological materials from the moment of their excavation until they are deposited in a research center.     

A very diverse amphibian and reptile assemblage from the late Middle Pleistocene of the Sierra de Atapuerca (Sima del Elefante,Burgos, Northwestern Spain)

Among the Pleistocene localities of the Sierra de Atapuerca, the site called Sima del Elefante is famous for having delivered in its lower level (TE-LRU) some hominid remains currently considered the oldest in Western Europe (about 1.2 Ma). In its upper part (TE-URU), this site has fossiliferous levels pertaining to the late Middle Pleistocene (350-250 ka). Here we describe for the first time the amphibians and reptiles of these upper levels (TE18 and TE19), which have proved to be one of the richest assemblages of all the localities of the Sierra de Atapuerca. The faunal list is composed of 18 taxa made up of urodeles (Salamandra salamandra and Lissotriton helveticus), anurans (Discoglossus sp., Alytes sp. Pelobates cultripes, Pelodytes punctatus, Bufo bufo, Bufo calamita, Hyla arborea and cf. Rana sp.), a terrestrial tortoise (Testudo s.l.), lizards (Lacerta s.l., Podarcis sp. and Anguis fragilis) and snakes (Natrix natrix, Natrix maura, Coronella cf. girondica and Vipera latasti). For the first time, the genera Lissotriton, Discoglossus and Podarcis are mentioned in the Pleistocene localities of the Sierra de Atapuerca. TE19 also corresponds to the earliest mention for L. helveticus in the Iberian Peninsula. With the exception of tortoises, all these species are currently present in the province of Burgos, and thus suggests that the herpetofauna has a modern aspect since the Middle Pleistocene. This association of amphibians and reptiles suggests a slightly warmer climate than the current one, but may correspond to a “cold and dry” period if compared with other Pleistocene localities of the Sierra de Atapuerca. The landscape was probably composed of a gallery forest along a quiet water river within a Mediterranean environment alternating laterally between dry meadows, rocky or stony areas and open scrubland.     

A geometric morphometric analysis of hominin upper premolars. Shape variation and morphological integration

This paper continues the series of articles initiated in 2006 that analyse hominin dental crown morphology by means of geometric morphometric techniques. The detailed study of both upper premolar occlusal morphologies in a comprehensive sample of hominin fossils, including those coming from the Gran Dolina-TD6 and Sima de los Huesos sites from Atapuerca, Spain, complement previous works on lower first and second premolars and upper first molars. A morphological gradient consisting of the change from asymmetric to symmetric upper premolars and a marked reduction of the lingual cusp in recent Homo species has been observed in both premolars. Although percentages of correct classification based on upper premolar morphologies are not very high, significant morphological differences between Neanderthals (and European middle Pleistocene fossils) and modern humans have been identified, especially in upper second premolars. The study of morphological integration between premolar morphologies reveals significant correlations that are weaker between upper premolars than between lower ones and significant correlations between antagonists. These results have important implications for understanding the genetic and functional factors underlying dental phenotypic variation and covariation.     

A tall-spined ornithopod dinosaur from the Early Cretaceous of Salas de los Infantes (Burgos, Spain)

A tall-spined ornithopod dinosaur from the Pinilla de los Moros Formation (Upper Hauterivian-Lower Barremian) of Salas de los Infantes (Burgos, Spain) is described. The material consists of seven associated axial remains, including five middle dorsal vertebrae, a fragmentary neural spine and a dorsal rib, from a single medium-sized individual. This material was previously referred to Iguanodon cf. fittoni. It is characterised by having a high dorsal neurapophysis that is approximately 4.5 times the height of the centrum. The elongation and vertical orientation of the dorsal neural spines allow it to be distinguished from other ornithopods from the Wealden of Europe, including Hypselospinus and Barilium from the Valanginian, and Iguanodon and Mantellisaurus from the Barremian-Aptian. The material is here referred to Iguanodontia indet. because it is so incomplete, but it is potentially a distinct taxon. Among the ornithopods, only Ouranosaurus and the hadrosaurid Hypacrosaurus possess higher dorsal neural spines.     

The fossil bat assemblage of Sima del Elefante Lower Red Unit (Atapuerca,Spain): First results and contribution to the palaeoenvironmental approach to the site

The fossil bat assemblage from the Lower Red Unit of Sima del Elefante (TELRU) in Atapuerca (Burgos, Spain) has been exhaustively analysed for the first time. Bat fossil assemblages are of particular relevance to palaeoenvironmental approaches to sites. Here we integrate our new data on the chiropteran fauna with the data provided previously by other authors on the basis of the small-vertebrate assemblages and the palynology of the site. Our results are consistent with the earlier results in that they indicate a generally warmer climate than at present in the area and stable environmental conditions throughout the major part of the TELRU sequence. However, fossil bat assemblages sometimes lead to problems when they are used in landscape reconstruction. These problems are discussed here and should be taken into account in future works.     

A geometric morphometric analysis of hominin upper second and third molars, with particular emphasis on European Pleistocene populations

The study of dental morphology by means of geometric morphometric methods allows for a detailed and quantitative comparison of hominin species that is useful for taxonomic assignment and phylogenetic reconstruction. Upper second and third molars have been studied in a comprehensive sample of Plio- and Pleistocene hominins from African, Asian and European sites in order to complete our analysis of the upper postcanine dentition. Intraspecific variation in these two molars is high, but some interspecific trends can be identified. Both molars exhibit a strong reduction of the distal cusps in recent hominin species, namely European Homo heidelbergensis, Homo neanderthalensis and Homo sapiens, but this reduction shows specific patterns and proportions in the three groups. Second molars tend to show four well developed cusps in earlier hominin species and their morphology is only marginally affected by allometric effects. Third molars can be incipiently reduced in earlier species and they evince a significant allometric component, identified both inter- and intraspecifically. European Middle Pleistocene fossils from Sima de los Huesos (SH) show a very strong reduction of these two molars, even more marked than the reduction observed in Neanderthals and in modern human populations. The highly derived shape of SH molars points to an early acquisition of typical Neanderthal dental traits by pre-Neanderthal populations and to a deviation of this population from mean morphologies of other European Middle Pleistocene groups.     

Human cannibalism in the Early Pleistocene of Europe (Gran Dolina, Sierra de Atapuerca, Burgos, Spain).

Human remains belonging to at least six individuals were found in an exploratory excavation made at the site of Gran Dolina (Sierra de Atapuerca, Burgos, Spain). These remains were recovered from the Aurora Stratum of Unit TD6. This stratum has a thickness of approximately 30 cm. The area of the exploratory excavation is about 7 m(2). According to palaeomagnetic analyses, Unit TD6 shows reversed polarity, which is considered to belong to the Matuyama chron. This unit is immediately below TD7, where the Matuyama-Brunhes boundary has been detected, indicating an age of around 780,000 years BP. There is no specific distribution, treatment, or arrangement of the human remains, which were found randomly mixed with abundant faunal remains and stone tools. Most of the faunal and human fossil bones from the Aurora Stratum have human induced damage. Stone tool cutmarks are frequent, and peeling (a type of fracture similar to bending a fresh twig between the hands) provides a specific breakage pattern together with percussion marks and chopmarks. Both nonhuman and human remains show similar intensive exploitation. Slight differences, however, have been observed between fauna and humans (e.g., peeling frequent in humans, rare in fauna), that appear related to different musculature, weight, and bone structure. The characteristics of this fossil assemblage suggest that it is solely the result of consumptive activities as there is no evidence of ritual or other intention. The possibility of distinguishing between dietary vs. survival cannibalism is discussed here.