Correction to: Human behavior and Homo-mammal interactions at the first European peopling: new evidence from the Pirro Nord site (Apricena, Southern Italy).

In the original publication of this article, one of the author names was incorrectly captured. The first name should be Razika, then family name should be Chelli-Cheheb.

Human behavior and Homo-mammal interactions at the first European peopling: new evidence from the Pirro Nord site (Apricena, Southern Italy).

Recent functional and zooarchaeological studies conducted on the archeological finds of Pirro Nord (PN13) produced new, reliable data on early European hominid subsistence activities. The age of the site is estimated to be ~ 1.3-1.6 Ma, based on bio-chronological data, and the archeological excavation of the Pirro Nord 13 fissure led to the discovery of more than 300 lithic artifacts associated with thousands of vertebrate fossil remains of the final Villafranchian (Pirro Nord Faunal Unit). The analysis of the fossil faunal remains allowed for the identification of anthropogenic traces linked to the exploitation of different animal carcass (cut marks and intentional bone breakages). Use-wear traces were also observed on some flint artifacts and have been interpreted as the result of the exploitation of animal resources by early hominids and carnivores. It has not been possible to identify the type of access that hominins developed on the carcasses, although it has been established that the hominins competed with carnivores for animal resources. The stone tools and faunal remains with anthropogenic traces recovered in the PN13 fissure represent among the earliest evidence of hominin faunal exploitation in Europe.

New Neandertal wrist bones from El Sidrón, Spain (1994-2009).

Twenty-nine carpal bones of Homo neanderthalensis have been recovered from the site of El Sidrón (Asturias, Spain) during excavations between 1994 and 2009, alongside ∼2500 other Neandertal skeletal elements dated to ∼49,000 years ago. All bones of the wrist are represented, including adult scaphoids (n = 6), lunates (n = 2), triquetra (n = 4), pisiforms (n = 2), trapezia (n = 2), trapezoids (n = 5), capitates (n = 5), and hamates (n = 2), as well as one fragmentary and possibly juvenile scaphoid. Several of these carpals appear to belong to the complete right wrist of a single individual. Here we provide qualitative and quantitative morphological descriptions of these carpals, within a comparative context of other European and Near Eastern Neandertals, early and recent Homo sapiens, and other fossil hominins, including Homo antecessor, Homo naledi, and australopiths. Overall, the El Sidrón carpals show characteristics that typically distinguish Neandertals from H. sapiens, such as a relatively flat first metacarpal facet on the trapezium and a more laterally oriented second metacarpal facet on the capitate. However, there are some distinctive features of the El Sidrón carpals compared with most other Neandertals. For example, the tubercle of the trapezium is small with limited projection, while the scaphoid tubercle and hamate hamulus are among the largest seen in other Neandertals. Furthermore, three of the six adult scaphoids show a distinctive os-centrale portion, while another is a bipartite scaphoid with a truncated tubercle. The high frequency of rare carpal morphologies supports other evidence of a close genetic relationship among the Neandertals found at El Sidrón.

The costal remains of the El Sidrón Neanderthal site (Asturias, northern Spain) and their importance for understanding Neanderthal thorax morphology.

The study of the Neanderthal thorax has attracted the attention of the scientific community for more than a century. It is agreed that Neanderthals have a more capacious thorax than modern humans, but whether this was caused by a medio-lateral or an antero-posterior expansion of the thorax is still debated, and is key to understanding breathing biomechanics and body shape in Neanderthals. The fragile nature of ribs, the metameric structure of the thorax and difficulties in quantifying thorax morphology all contribute to uncertainty regarding precise aspects of Neanderthal thoracic shape. The El Sidrón site has yielded costal remains from the upper to the lower thorax, as well as several proximal rib ends (frequently missing in the Neanderthal record), which help to shed light on Neanderthal thorax shape. We compared the El Sidrón costal elements with ribs from recent modern humans as well as with fossil modern humans and other Neanderthals through traditional morphometric methods and 3D geometric morphometrics, combined with missing data estimation and virtual reconstruction (at the 1st, 5th and 11th costal levels). Our results show that Neanderthals have larger rib heads and articular tubercles than their modern human counterparts. Neanderthal 1st ribs are smaller than in modern humans, whereas 5th and 11th ribs are considerably larger. When we articulated mean ribs (size and shape) with their corresponding vertebral elements, we observed that compared to modern humans the Neanderthal thorax is medio-laterally expanded at every level, especially at T5 and T11. Therefore, in the light of evidence from the El Sidrón costal remains, we hypothesize that the volumetric expansion of the Neanderthal thorax proposed by previous authors would mainly be produced by a medio-lateral expansion of the thorax.

Three-dimensional morphometrics of thoracic vertebrae in Neandertals and the fossil evidence from El Sidrón (Asturias, Northern Spain).

Well preserved thoracic vertebrae of Neandertals are rare. However, such fossils are important as their three-dimensional (3D) spatial configuration can contribute to the understanding of the size and shape of the thoracic spine and the entire thorax. This is because the vertebral body and transverse processes provide the articulation and attachment sites for the ribs. Dorsal orientation of the transverse processes relative to the vertebral body also rotates the attached ribs in a way that could affect thorax width. Previous research indicates possible evidence for greater dorsal orientation of the transverse processes and small vertebral body heights in Neandertals, but their 3D vertebral structure has not yet been addressed. Here we present 15 new vertebral remains from the El Sidrón Neandertals (Asturias, Northern Spain) and used 3D geometric morphometrics to address the above issues by comparing two particularly well preserved El Sidrón remains (SD-1619, SD-1641) with thoracic vertebrae from other Neandertals and a sample of anatomically modern humans. Centroid sizes of El Sidrón vertebrae are within the human range. Neandertals have larger T1 and probably also T2. The El Sidrón vertebrae are similar in 3D shape to those of other Neandertals, which differ from Homo sapiens particularly in central-lower regions (T6-T10) of the thoracic spine. Differences include more dorsally and cranially oriented transverse processes, less caudally oriented spinous processes, and vertebral bodies that are anteroposteriorly and craniocaudally short. The results fit with current reconstructions of Neandertal thorax morphology.

Neandertal talus bones from El Sidrón site (Asturias, Spain): A 3D geometric morphometrics analysis.

OBJECTIVES: The El Sidrón tali sample is assessed in an evolutionary framework. We aim to explore the relationship between Neandertal talus morphology and body size/shape. We test the hypothesis 1: talar Neandertal traits are influenced by body size, and the hypothesis 2: shape variables independent of body size correspond to inherited primitive features. MATERIALS AND METHODS: We quantify 35 landmarks through 3D geometric morphometrics techniques to describe H. neanderthalensis-H. sapiens shape variation, by Mean Shape Comparisons, Principal Component, Phenetic Clusters, Minimum spanning tree analyses and partial least square and regression of talus shape on body variables. Shape variation correlated to body size is compared to Neandertals-Modern Humans (MH) evolutionary shape variation. The Neandertal sample is compared to early hominins. RESULTS: Neandertal talus presents trochlear hypertrophy, a larger equality of trochlear rims, a shorter neck, a more expanded head, curvature and an anterior location of the medial malleolar facet, an expanded and projected lateral malleolar facet and laterally expanded posterior calcaneal facet compared to MH. DISCUSSION: The Neandertal talocrural joint morphology is influenced by body size. The other Neandertal talus traits do not co-vary with it or not follow the same co-variation pattern as MH. Besides, the trochlear hypertrophy, the trochlear rims equality and the short neck could be inherited primitive features; the medial malleolar facet morphology could be an inherited primitive feature or a secondarily primitive trait; and the calcaneal posterior facet would be an autapomorphic feature of the Neandertal lineage.

Adult Neandertal clavicles from the El Sidrón site (Asturias, Spain) in the context of Homo pectoral girdle evolution.

We undertook a three-dimensional geometric morphometric (3DGM) analysis on 12 new Neandertal clavicle specimens from the El Sidrón site (Spain), dated to 49,000 years ago. The 3DGM methods were applied in a comparative framework in order to improve our understanding of trait polarity in features related to Homo pectoral girdle evolution, using other Neandertals, Homo sapiens, Pan, ATD6-50 (Homo antecessor), and KNM-WT 15000 (Homo ergaster/erectus) in the reference collection. Twenty-nine homologous landmarks were measured for each clavicle. Variation and morphological similarities were assessed through principal component analysis, conducted separately for the complete clavicle and the diaphysis. On average, Neandertal clavicles had significantly larger muscular entheses, double dorsal curvature, clavicle torsion, and cranial orientation of the acromial end than non-Neandertal clavicles; the El Sidrón clavicles fit this pattern. Variation within the samples was large, with extensive overlap between Homo species; only chimpanzee specimens clearly differed from the other specimens in morphometric terms. Taken together, our morphometric analyses are consistent with the following phylogenetic sequence. The primitive condition of the clavicle is manifest in the cranial orientation of both the acromial and sternal ends. The derived condition expressed in the H. sapiens + Neandertal clade is defined by caudal rotation of both the sternal and acromial ends, but with variation in the number of acromia remaining in a certain cranial orientation. Finally, the autapomorphic Neandertal condition is defined by secondarily acquired primitive cranial re-orientation of the acromial end, which varies from individual to individual. These results suggest that the pace of phylogenetic change in the pectoral girdle does not seem to follow that of other postcranial skeletal features.

A geometric morphometrics comparative analysis of Neandertal humeri (epiphyses-fused) from the El Sidrón cave site (Asturias, Spain).

A new collection of 49,000 year old Neandertal fossil humeri from the El Sidrón cave site (Asturias, Spain) is presented. A total of 49 humeral remains were recovered, representing 10 left and 8 right humeri from adults, adolescents, and a juvenile (not included in the analyses). 3D geometric morphometric (GM) methods as well as classic anthropological variables were employed to conduct a broad comparative analysis by means of mean centroid size and shape comparisons, principal components analysis, and cluster studies. Due to the fragmentary nature of the fossils, comparisons were organized in independent analyses according to different humeral portions: distal epiphysis, diaphysis, proximal epiphysis, and the complete humerus. From a multivariate viewpoint, 3D-GM analyses revealed major differences among taxonomic groups, supporting the value of the humerus in systematic classification. Notably, the Australopithecus anamensis (KP-271) and Homo ergaster Nariokotome (KNM-WT 15000) distal humerus consistently clusters close to those of modern humans, which may imply a primitive condition for Homo sapiens morphology. Australopithecus specimens show a high degree of dispersion in the morphospace. The El Sidrón sample perfectly fits into the classic Neandertal pattern, previously described as having a relatively wide olecranon fossa, as well as thin lateral and medial distodorsal pillars. These characteristics were also typical of the Sima de los Huesos (Atapuerca) sample, African mid-Pleistocene Bodo specimen, and Lower Pleistocene TD6-Atapuerca remains and may be considered as a derived state. Finally, we hypothesize that most of the features thought to be different between Neandertals and modern humans might be associated with structural differences in the pectoral girdle and shoulder joint.

The relevance of the first ribs of the El Sidrón site (Asturias, Spain) for the understanding of the Neandertal thorax.

Reconstructing the morphology of the Neanderthal rib cage not only provides information about the general evolution of human body shape but also aids understanding of functional anatomy and energetics. Despite this paleobiological importance there is still debate about the nature and extent of variations in the size and shape of the Neandertal thorax. The El Sidrón Neandertals can be used to contribute to this debate, providing new costal remains ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs are particularly well preserved and offer the opportunity to analyze thorax morphology in Neandertals. The aims of this paper are to present this new material, to compare the ontogenetic trajectories of the first ribs between Neandertals and modern humans, and, using geometric morphometrics, to test the hypothesis of morphological integration between the first rib and overall thorax morphology. The first ribs of the El Sidrón adult Neandertals are smaller in centroid size and tend to be less curved when compared with those of modern humans, but are similar to Kebara 2. Our results further show that the straightening of the first ribs is significantly correlated with a straightening of the ribs of the upper thorax (R = 0.66; p < 0.0001) in modern humans, suggesting modularity in the upper and lower thorax units as reported in other hominins. It also supports the hypothesis that the upper thorax of Neandertals differs in shape from modern humans with more anteriorly projecting upper ribs during inspiration. These differences could have biomechanical consequences and account for stronger muscle attachments in Neandertals. Different upper thorax shape would also imply a different spatial arrangement of the shoulder girdle and articulation with the humerus (torsion) and its connection to the upper thorax. Future research should address these inferences in the context of Neandertal overall body morphology.

Early Pleistocene human hand phalanx from the Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain).

In this study, a new Early Pleistocene proximal hand phalanx (ATE9-2) from the Sima del Elefante cave site (TE - Sierra de Atapuerca, Spain), ascribed to Homo sp., is presented and comparatively described in the context of the evolution of the genus Homo. The ATE9-2 specimen is especially important because of the paucity of hand bones in the human fossil record during the Early Pleistocene. The morphological and metrical analyses of the phalanx ATE9-2 indicate that there are no essential differences between it and comparator fossil specimens for the genus Homo after 1.3 Ma (millions of years ago). Similar to Sima de los Huesos and Neandertal specimens, ATE9-2 is a robust proximal hand phalanx, probably reflecting greater overall body robusticity in these populations or a higher gracility in modern humans. The age of level TE9 from Sima del Elefante and morphological and metrical studies of ATE9-2 suggest that the morphology of the proximal hand phalanges and, thus, the morphology of the hand could have remained stable over the last 1.2-1.3 Ma. Taking into account the evidence recently provided by a metacarpal from Kaitio (Kenya) from around 1.42 Ma, we argue that modern hand morphology is present in the genus Homo subsequent to Homo habilis.

The lithic industry of Sima del Elefante (Atapuerca, Burgos, Spain) in the context of Early and Middle Pleistocene technology in Europe.

This paper presents the lithic assemblages documented at Sima del Elefante (TE) and their importance in the context of the Early and Middle Pleistocene human occupation of Europe. We also study changes in human behaviour within the context of the palaeoenvironmental evolution of the Sierra de Atapuerca. This site has characteristics that are of great value for the study of human evolution. The lower levels of TE (Units TE7-TE14) are an essential reference for understanding the early stages of the colonization of Europe. The TE9c level has provided stone tools (Mode 1), faunal remains, and human fossils dated to 1.22 Ma (millions of years ago). Moreover, this is one of the few European sites with a stratigraphic sequence that includes remains of human occupations predating the Jaramillo subchron (Early Pleistocene) and from the Late Middle Pleistocene (Units TE18-TE19). Despite this, the presence of archaeologically sterile units (TE15-17) prevents us from establishing a continuous relationship between the Early and Middle Pleistocene human settlements and, consequently, between their technological and behavioural differences. We can, however compare the technological and palaeoeconomic strategies adopted by different species of hominins during two key phases of the occupation of Europe.

The first hominin of Europe.

The earliest hominin occupation of Europe is one of the most debated topics in palaeoanthropology. However, the purportedly oldest of the Early Pleistocene sites in Eurasia lack precise age control and contain stone tools rather than human fossil remains. Here we report the discovery of a human mandible associated with an assemblage of Mode 1 lithic tools and faunal remains bearing traces of hominin processing, in stratigraphic level TE9 at the site of the Sima del Elefante, Atapuerca, Spain. Level TE9 has been dated to the Early Pleistocene (approximately 1.2-1.1 Myr), based on a combination of palaeomagnetism, cosmogenic nuclides and biostratigraphy. The Sima del Elefante site thus emerges as the oldest, most accurately dated record of human occupation in Europe, to our knowledge. The study of the human mandible suggests that the first settlement of Western Europe could be related to an early demographic expansion out of Africa. The new evidence, with previous findings in other Atapuerca sites (level TD6 from Gran Dolina), also suggests that a speciation event occurred in this extreme area of the Eurasian continent during the Early Pleistocene, initiating the hominin lineage represented by the TE9 and TD6 hominins.

Genetic evidence for patrilocal mating behavior among Neandertal groups.

The remains of 12 Neandertal individuals have been found at the El Sidrón site (Asturias, Spain), consisting of six adults, three adolescents, two juveniles, and one infant. Archaeological, paleontological, and geological evidence indicates that these individuals represent all or part of a contemporaneous social group of Neandertals, who died at around the same time and later were buried together as a result of a collapse of an underground karst. We sequenced phylogenetically informative positions of mtDNA hypervariable regions 1 and 2 from each of the remains. Our results show that the 12 individuals stem from three different maternal lineages, accounting for seven, four, and one individual(s), respectively. Using a Y-chromosome assay to confirm the morphological determination of sex for each individual, we found that, although the three adult males carried the same mtDNA lineage, each of the three adult females carried different mtDNA lineages. These findings provide evidence to indicate that Neandertal groups not only were small and characterized by low genetic diversity but also were likely to have practiced patrilocal mating behavior.

A new Lower Pleistocene archeological site in Europe (Vallparadis, Barcelona, Spain).

Here we report the discovery of a new late Lower Pleistocene site named Vallparadís (Barcelona, Spain) that produced a rich archeological and paleontological sequence dated from the upper boundary of the Jaramillo subchron to the early Middle Pleistocene. This deposit contained a main archeological layer with numerous artifacts and a rich macromammalian assemblage, some of which bore cut marks, that could indicate that hominins had access to carcasses. Paleomagnetic analysis, electron spin resonance-uranium series (ESR-US), and the biostratigraphic chronological position of the macro- and micromammal and lithic assemblages of this layer reinforce the proposal that hominins inhabited Europe during the Lower Pleistocene. The archeological sequence provides key information on the successful adaptation of European hominins that preceded the well-known fossil population from Atapuerca and succeeded the finds from Orce basin. Hence, this discovery enables us to close a major chronological gap in the early prehistory of Iberia. According to the information in this paper and the available data from these other sites, we propose that Mediterranean Western Europe was repeatedly and perhaps continuously occupied during the late Matuyama chron.

A symbolic Neanderthal accumulation of large herbivore crania.

This work examines the possible behaviour of Neanderthal groups at the Cueva Des-Cubierta (central Spain) via the analysis of the latter's archaeological assemblage. Alongside evidence of Mousterian lithic industry, Level 3 of the cave infill was found to contain an assemblage of mammalian bone remains dominated by the crania of large ungulates, some associated with small hearths. The scarcity of post-cranial elements, teeth, mandibles and maxillae, along with evidence of anthropogenic modification of the crania (cut and percussion marks), indicates that the carcasses of the corresponding animals were initially processed outside the cave, and the crania were later brought inside. A second round of processing then took place, possibly related to the removal of the brain. The continued presence of crania throughout Level 3 indicates that this behaviour was recurrent during this level's formation. This behaviour seems to have no subsistence-related purpose but to be more symbolic in its intent.

Intergroup cannibalism in the European Early Pleistocene: the range expansion and imbalance of power hypotheses.

In this paper, we compare cannibalism in chimpanzees, modern humans, and in archaeological cases with cannibalism inferred from evidence from the Early Pleistocene assemblage of level TD6 of Gran Dolina (Sierra de Atapuerca, Spain). The cannibalism documented in level TD6 mainly involves the consumption of infants and other immature individuals. The human induced modifications on Homo antecessor and deer remains suggest that butchering processes were similar for both taxa, and the remains were discarded on the living floor in the same way. This finding implies that a group of hominins that used the Gran Dolina cave periodically hunted and consumed individuals from another group. However, the age distribution of the cannibalized hominins in the TD6 assemblage is not consistent with that from other cases of exo-cannibalism by human/hominin groups. Instead, it is similar to the age profiles seen in cannibalism associated with intergroup aggression in chimpanzees. For this reason, we use an analogy with chimpanzees to propose that the TD6 hominins mounted low-risk attacks on members of other groups to defend access to resources within their own territories and to try and expand their territories at the expense of neighboring groups.

Neanderthal medics? Evidence for food, cooking, and medicinal plants entrapped in dental calculus.

Neanderthals disappeared sometime between 30,000 and 24,000 years ago. Until recently, Neanderthals were understood to have been predominantly meat-eaters; however, a growing body of evidence suggests their diet also included plants. We present the results of a study, in which sequential thermal desorption-gas chromatography-mass spectrometry (TD-GC-MS) and pyrolysis-gas chromatography-mass spectrometry (Py-GC-MS) were combined with morphological analysis of plant microfossils, to identify material entrapped in dental calculus from five Neanderthal individuals from the north Spanish site of El Sidrón. Our results provide the first molecular evidence for inhalation of wood-fire smoke and bitumen or oil shale and ingestion of a range of cooked plant foods. We also offer the first evidence for the use of medicinal plants by a Neanderthal individual. The varied use of plants that we have identified suggests that the Neanderthal occupants of El Sidrón had a sophisticated knowledge of their natural surroundings which included the ability to select and use certain plants.

Carcass transport decisions in Homo antecessor subsistence strategies.

Pleistocene foragers used several prey acquisition and processing strategies. These strategies and their associated decisions are elucidated by taphonomic studies that cover animal transport, modifications by different agents and archaeological remains. Interpretative models of archaeological sites are by necessity based on natural and experimental observations. Ethno-archaeological data shows that several factors influenced decisions about carcass transport from the kill site to the home site. These factors often have little archaeological visibility. Díez et al. (1999) has previously interpreted the general characteristics of the macro-mammal remains from Gran Dolina Level TD6-2 (Sierra de Atapuerca, Burgos, Spain) as the result of anthropic accumulation, in which the anatomical profiles appeared to be the result of selective transport based on the animals' weight. Recent taphonomic analysis has shown that carcasses with different weights may be subject to similar transport strategies, suggesting that other factors influenced these choices. The hominins that occupied TD6-2 (the TD6-2 hominin group), at least sometimes, transported large carcasses to the cave in their entirety, implying participation by groups of individuals in hunting parties. These individuals delayed their consumption of large amounts of food, instead moving it to Gran Dolina, where it was shared with other group members. These decisions are evidence of social cooperation and food sharing amongst early European hominins.

3D Insights into the Effects of Captivity on Wolf Mastication and Their Tooth Marks; Implications in Ecological Studies of Both the Past and Present.

Human populations have been known to develop complex relationships with large carnivore species throughout time, with evidence of both competition and collaboration to obtain resources throughout the Pleistocene. From this perspective, many archaeological and palaeontological sites present evidence of carnivore modifications to bone. In response to this, specialists in the study of microscopic bone surface modifications have resorted to the use of 3D modeling and data science techniques for the inspection of these elements, reaching novel limits for the discerning of carnivore agencies. The present research analyzes the tooth mark variability produced by multiple Iberian wolf individuals, with the aim of studying how captivity may affect the nature of tooth marks left on bone. In addition to this, four different populations of both wild and captive Iberian wolves are also compared for a more in-depth comparison of intra-species variability. This research statistically shows that large canid tooth pits are the least affected by captivity, while tooth scores appear more superficial when produced by captive wolves. The superficial nature of captive wolf tooth scores is additionally seen to correlate with other metric features, thus influencing overall mark morphologies. In light of this, the present study opens a new dialogue on the reasons behind this, advising caution when using tooth scores for carnivore identification and contemplating how elements such as stress may be affecting the wolves under study.