Elsevier

Journal of Human Evolution

Volume 104, March 2017, Pages 13-22
Journal of Human Evolution

Dietary reconstruction of the El Sidrón Neandertal familial group (Spain) in the context of other Neandertal and modern hunter-gatherer groups. A molar microwear texture analysis

https://doi.org/10.1016/j.jhevol.2016.12.003Get rights and content

Abstract

Here, we present the analysis of occlusal molar microwear textures of eight individuals from the El Sidrón Neandertal group (Spain). The aims of the study were: 1) to document potential age-, sex-, and maternal lineage-related differences in diet within a Neandertal familial group, and 2) to place the diet of El Sidrón individuals in the context of those of other Neandertal groups. This study also offers an interpretation of the diet of the El Sidrón Neandertals by comparing their microwear signatures to those of recent hunter-gatherer populations with diverse but known diets. The intra-group examination of the microwear signatures are consistent with the females of the El Sidrón group having had more abrasive diets or having used their teeth in more para-masticatory activities than did the males. Aside from the potential sex-related differences in diet, no additional intra-group dietary separation, such as by age group or maternal lineage, was observed. In comparison to other Neandertals, El Sidrón individuals, as a group, have microwear signatures most similar to those of other Neandertals from wooded habitats and different from those that lived in more open habitats. This result is expected based on the available paleoenvironmental reconstructions from El Sidrón Cave. The diet of the El Sidrón Neandertals, just like their Neandertal counterparts from similar wooded habitats, is interpreted as having been mixed, consisting of both meat and vegetable foods.

Introduction

Gaining insights into the daily life of a group of extinct hominins is a genuine advance in paleoanthropological research. In the majority of cases, paleoanthropologists are forced to conduct their studies on isolated specimens or a very small number of individuals, usually coming from different layers of a single site, or on aggregates of individuals geographically dispersed and chronologically distant. Studying the human remains from El Sidrón Cave in Spain represents one of the rare exceptions. El Sidrón Cave provides a total of 13 Neandertal individuals (Rosas et al., 2013) all coming from a single archaeological deposit (Fortea et al., 2003). This assemblage has provided a unique opportunity to investigate different patterns of Neandertal behavior, including patrilocality as inferred from mtDNA analyses (Lalueza-Fox et al., 2011), use of medicinal plants and hafting materials (Hardy et al., 2012), handedness (Estalrrich and Rosas, 2013), division of labor (Estalrrich and Rosas, 2015), as well as anthropic exploitation of human bones (Rosas et al., 2006). In this study, we examine the diets of the El Sidrón group by using molar microwear texture analysis to: 1) explore Neandertal intra-group dietary variation by age, sex, and maternal lineage, and 2) place the El Sidrón Neandertals within the dietary context of other Neandertals whose microwear signatures have already been analyzed using the same techniques and methods as those employed here. Specifically, the occlusal molar microwear textures of Neandertals from open-steppe environments reflect a diet consisting almost exclusively of tough food items, consistent with a meat-based diet, whereas with the increase in tree cover, the microwear textures reflect increases in dietary variability and ingestion of greater amounts of hard foods, most probably plants. The microwear signatures of the Neandertals from El Sidrón are expected to align with those of the latter group since paleovegetation cover reconstructions from the El Sidrón paleoanthropological deposit support wooded conditions (Fortea et al., 2003, Badal-García, 2011, Rosas et al., 2011, Sanchíz and Martín, 2011, Sesé, 2011).

El Sidrón site is a karstic cave located in north-western Spain, 40 km east of Oviedo (capital of Principado de Asturias region), in the “Surco Oviedo-Infiesto” – a band of Mesozoic and Cenozoic sediments limited to the north and south by Paleozoic reliefs (Fortea et al., 2003, Rosas et al., 2006). Accidental discovery of Neandertal remains in 1994 highlighted the potential of El Sidrón Cave to provide more fossils. Archaeological excavations in the cave were conducted from 2000 to 2014. These excavations uncovered 415 lithic tools (Santamaría et al., 2010), 51 macro-mammal remains (Rosas et al., 2011), and 2538 Neandertal bone fragments (Rosas et al., 2013) all from the same archaeological unit (Unit III; Cañaveras et al., 2011) of one of the cave's lateral galleries, “Galería del Osario”. Unit III consists of a massive debris flow deposit, comprising a mixture of gravels, mud, and water (Fortea et al., 2003, Cañaveras et al., 2011). The existence of such a debris-flow cone is supported by the spatial projection of the numerous refitted materials (both lithics and bones) (Fortea et al., 2003, Santamaría et al., 2010). This debris flow is associated with a single high-energy event that dragged archaeological and paleoanthropological material, including the Neandertal remains, down from an upper level, either from the surface or from an undiscovered upper gallery (Fortea et al., 2003, Cañaveras et al., 2011, Rosas et al., 2013). Various lines of evidence, including the discovery of several Neandertal skeletal regions (e.g., thoracic cage, arms, foot and hand bones) in correct anatomical articulation, the excellent preservation of bone surfaces with no evidence of weathering or erosion, and the lack of carnivore tooth-marks or other scavenging activities, point to limited post-mortem displacement of the remains and, thus, their brief exposure on the exterior surface prior to the single high-energy event that transported the specimens to the gallery where they were found (Fortea et al., 2003, Rosas et al., 2006, Rosas et al., 2013, Lalueza-Fox et al., 2011, Martínez-Maza et al., 2011). In addition, electron spin resonance, amino acid racemization, and ultrafiltration radiocarbon dating of several Neandertal bones and teeth from the site give a consistent date of around 49,000 before present (BP; Torres et al., 2010, Wood et al., 2013), which is concordant with a synchronic accumulation event for the Neandertal assemblage.

This date places the Neandertals from El Sidrón in Marine Isotope Stage (MIS) 3. The analyses of the scarce faunal remains (large and small mammals, and herpetofauna), as well as the 19 anthracological samples recovered from the same unit (Unit III) as the Neandertals (Fortea et al., 2003, Badal-García, 2011, Rosas et al., 2011, Sanchíz and Martín, 2011, Sesé, 2011), suggest a temperate phase of MIS 3, with environmental conditions similar to those of the present. The landscape was covered with a mix of coniferous and deciduous (Quercus sp.) forests, as well as some Fabaceae that would have formed the bushes and grasslands associated with the forests, in addition to some open spaces and a permanent source of water (Fortea et al., 2003, Badal-García, 2011, Rosas et al., 2011, Sanchíz and Martín, 2011, Sesé, 2011).

A total of 13 Neandertal individuals have been identified from El Sidrón (Rosas et al., 2013). All the remains are housed at the Department of Paleobiology at the National Museum of Natural Sciences (MNCN-CSIC) in Madrid, Spain. These individuals were sexed using mandibular morphological features, canine odontometrics (see Rosas et al., 2012), and the presence/absence of Y-chromosome markers (Lalueza-Fox et al., 2011). Their ages-at-death were estimated based on dental and postcranial skeletal development (Rosas et al., 2012, Rosas et al., 2013). Based on dental development, the individuals have all been assigned to one of three groups: adults, when M3s are fully formed and in full occlusion, adolescents, when M3 crowns are in formation and M2s lack distal facets, and juveniles, when there is a mix of deciduous and permanent dentition, and when M1 roots are in formation and M2 crowns are almost completely formed (Rosas et al., 2013). In sum, the results of these reconstructions show that the Neandertal sample from El Sidrón (Table 1) consists of seven adults (four females, three males), three adolescents (one female, two males), two juveniles (one male, one for which sex determination is still in progress), and one infant (whose sex is indeterminate) (Rosas et al., 2013). It is worth noting that previous studies on El Sidrón adult dental samples noted the slight degree of occlusal wear on these teeth compared to that usually observed for other Neandertal specimens. Indeed, for El Sidrón adults, the cusps and the majority of the occlusal enamel of the post-canine dentition are intact, and only small isles of dentin are apparent, indicating that the El Sidrón individuals were all young adults at the time of death (Rosas et al., 2006, Rosas et al., 2012, Rosas et al., 2013, Estalrrich et al., 2011). Sequencing of mtDNA for 12 out of the 13 individuals to reconstruct maternal genetic lineages has identified three separate mtDNA haplotypes: El Sidrón lineage A (200A-204T-16124A haplotype), carried by seven individuals, El Sidrón lineage B (200G-204C-16124G haplotype), carried by four individuals, and El Sidrón lineage C (200G-204T-16124G haplotype), carried by one individual (Table 1; Lalueza-Fox et al., 2011). It should be noted that all the El Sidrón lineages differ from the Vindija Vi33.16 Neandertal by an A to C transversion at position 16177, indicating that the El Sidrón individuals are closely related (Lalueza-Fox et al., 2011). In addition, the El Sidrón mtDNA diversity is lower than any random subsample of sequences taken from unrelated modern Europeans (Lalueza-Fox et al., 2011), which lends support to the argument that the El Sidrón individuals represent a group with familial relations. This argument is further supported by paleobiological findings that show congenital pathologies consistent with low genetic diversity (Dean et al., 2013, Ríos et al., 2015).

Since the geological and archaeological data indicate that the Neandertal individuals from El Sidrón were members of a single social group, and the genetic signatures of the individuals support familial relatedness among this group, this sample provides an unprecedented opportunity to gain insights into Neandertal group dynamics. One way of gaining such insights is through the exploration of diet, a key factor in shaping an animal's ecological behavior. Aside from examinations of dental calculus, the diet of the El Sidrón group remains unexplored. Although informative of this group's consumption and use of medicinal plants, ingestion of starchy and possibly smoked foods, and the use of bitumen (Hardy et al., 2012), examination of dental calculus does not provide a comprehensive understanding of dietary patterns. In order to provide a broader picture of the diet and dietary variability of the individuals belonging to the El Sidrón Neandertal familial group, we analyze their occlusal molar microwear textures in the context of those of other Neandertal individuals.

Until recently, reconstructions of Neandertal diets have been mainly based on the anthropic modifications of the faunal remains found at Middle Paleolithic sites and the isotopic analyses of Neandertal bones. The former showed that Neandertals were active hunters of big and small prey (e.g., Gaudzinski, 1995, Gaudzinski and Roebroeks, 2000, Patou-Mathis, 2000, Speth and Tchernov, 2002, Stiner, 2005, Rendu, 2010, Gaudzinski-Windheuser and Roebroeks, 2011, Niven et al., 2012), and the latter advocated the idea that they were top-level carnivores (e.g., Richards et al., 2000, Bocheners et al., 2005, Richards and Trinkaus, 2009). Analyses of plant remains from Neandertal sites and from dental calculus samples taken from Neandertal dentition have shed more light on the plant component of the Neandertal diet (Madella et al., 2002, Lev et al., 2005, Henry et al., 2010, Henry et al., 2014, Hardy and Moncel, 2011, Hardy et al., 2012, Salazar-García et al., 2013). Furthermore, studies of Neandertal dental wear are providing more details on Neandertal diet and dietary variability (Lalueza-Fox and Pérez-Pérez, 1993, Pérez-Pérez et al., 2003, El Zaatari et al., 2011, Fiorenza et al., 2011, Fiorenza et al., 2015, Pinilla Pérez et al., 2011, Harvati et al., 2013, Hlusko et al., 2013, Puech and Pinilla, 2014, El Zaatari et al., 2016). Neandertal occlusal molar microwear studies in particular distinguish between Neandertals from cold open-steppe environments, who had a diet that consisted almost exclusively of meat, and those from wooded and mixed environments, who had a diet that, in addition to animal meat, also included an important plant component (El Zaatari et al., 2011, El Zaatari et al., 2016). Since paleovegetation reconstructions indicate that El Sidrón Neandertals lived in wooded habitats, their microwear signature is expected to reflect a mixed diet.

Section snippets

El Sidrón sample

Dental remains are available for 11 of the 13 Neandertal individuals from El Sidrón. The Infant and Juvenile 2 individuals have no associated dentition and thus, it was not possible to include them in the current study.

Neandertal comparative sample

Aside from the El Sidrón specimens, samples of other Neandertals were also included in this study for comparative purposes. The comparative Neandertal sample consists of a total of 21 western Eurasian adult individuals (listed in the Supplementary Online Material [SOM], Table S1)

Methods

For the occlusal molar microwear texture analysis, high-resolution replicas of the first or second molars of the 11 individuals from the site of El Sidrón were prepared following conventional procedures (Bromage, 1987, Teaford and Oyen, 1989, Martínez-Maza et al., 2011). All teeth were cleaned with an artist's paintbrush, having been first soaked with acetone to remove the acetone-soluble preservation material (Paraloid B-72) and afterwards washed with ethanol and distilled water to remove any

El Sidrón's intra-group variation

Photosimulations of the occlusal surfaces of selected El Sidrón teeth are shown in Figure 1. The values for the microwear signatures for the El Sidrón adults and sub-adults (adolescents and juveniles) overlapped widely (Fig. 2 and Table 2). This was also the case when considering mtDNA lineage (Fig. 2 and Table 2). However, when considering sex, males and females from El Sidrón separated based on their complexity values (Fig. 2).

El Sidrón in the context of other Neandertal and modern hunter-gatherer comparative samples

Means and standard deviations for the microwear signatures of the

Diet and paleoecology for El Sidrón adults and sub-adults

The results of this study show that the microwear signature of the El Sidrón adult individuals as a group are most similar to Neandertals from wooded environments, and are clearly distinct from those from open and mixed habitats. This is consistent with the available paleoecological information for the site of El Sidrón (Fortea et al., 2003, Badal-García, 2011, Rosas et al., 2011, Sanchíz and Martín, 2011, Sesé, 2011). The microwear signatures of the El Sidrón group are distinct from those of

Conclusions

This study examined the occlusal molar microwear textures of a single group of Neandertals from the El Sidrón Cave site in Spain. The results of this study indicate that the diet of the Neandertals from El Sidrón was similar to that of other Neandertals from wooded environments, and to the recent Chumash and Khoe-San hunter-gatherer groups. The diet of the El Sidrón adults can be interpreted as mixed, consisting of substantial amounts of both meat and vegetable foods. Our observations of the

Acknowledgements

We are deeply grateful to Prof. Peter S. Ungar for allowing us the use of the microscope facilities at the Department of Anthropology in the University of Arkansas, and encouraging discussions on microwear and diet. Dr. K. Krueger (Loyola University) kindly provided the raw data for the Moula-Guercy sub-adult Neandertals. We also thank all the people working during the El Sidrón fieldwork seasons. We are grateful to Dr. R. Huguet (IPHES) for her thoughtful comments on the discussion of this

References (100)

  • P. Mahoney et al.

    Deciduous enamel 3D microwear texture analysis as an indicator of childhood diet in medieval Canterbury, England

    J. Archaeol. Sci.

    (2016)
  • L. Niven et al.

    Neandertal mobility and large-game hunting: the exploitation of reindeer during the Quina Mousterian at Chez-Pinaud Jonzac (Charente-Maritime, France)

    J. Hum. Evol.

    (2012)
  • A. Pérez-Pérez et al.

    Non-occlusal dental microwear variability in a sample of Middle and Late Pleistocene human populations from Europe and the Near East

    J. Hum. Evol.

    (2003)
  • W. Rendu

    Hunting behavior and Neanderthal adaptability in the Late Pleistocene site of Pech-de-l’Azé I

    J. Archaeol. Sci.

    (2010)
  • A. Rosas et al.

    Les Néandertaliens d’El Sidrón (Asturies, Espagne) Actualisation d’un nouvel échantillon

    L'Anthropologie

    (2012)
  • A. Rosas et al.

    Identification of Neandertal individuals in fragmentary fossil assemblages by means of tooth associations: the case of El Sidrón (Asturias, Spain)

    C. R. Palevol

    (2013)
  • D.C. Salazar-García et al.

    Neanderthal diets in central and southeastern Mediterranean Iberia

    Quatern. Int.

    (2013)
  • R.S. Scott et al.

    Dental microwear texture analysis: technical considerations

    J. Hum. Evol.

    (2006)
  • J.D. Speth et al.

    Middle Paleolithic tortoise use at Kebara Cave (Israel)

    J. Archaeol. Sci.

    (2002)
  • M. Toussaint et al.

    The Neandertal lower right deciduous second molar from the “Trou de l'Abîme” at Couvin, Belgium

    J. Hum. Evol.

    (2010)
  • D.R. Yesner et al.

    Stable isotope analysis of human bone and ethnohistoric subsistence patterns in Tierra del Fuego

    J. Anthropol. Archaeol.

    (2003)
  • E. Badal-García

    La materia vegetal carbonizada

  • C. Barroso Ruíz et al.

    Le gisement Moustérien de la Grotte du Boquete de Zafarraya (Alcaucín, Andalousie)

    L'Anthropologie

    (1984)
  • J.C. Berbesque et al.

    Sex differences in food preferences of Hadza hunter-gatherers

    Evol. Psychol.

    (2009)
  • J.C. Berbesque et al.

    Sex differences in Hadza eating frequency by food type

    Am. J. Hum. Biol.

    (2011)
  • J.C. Berbesque et al.

    Sex differences in Hadza dental wear patterns. A preliminary report

    Hum. Nat.

    (2012)
  • H. Bocheners et al.

    Isotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal: review and use of a multi-source mixing model

    J. Hum. Evol.

    (2005)
  • B. Bonfiglioli

    Le alterazioni dentarie di tipo non masticatorio come indicatore di attività

    (2002)
  • B. Bonfiglioli et al.

    Masticatory and non-masticatory dental modifications in the Epipalaeolithic Necropolis of Taforalt (Morocco)

    Int. J. Osteoarchaeol.

    (2004)
  • T. Bromage

    The scanning electron microscopy replica technique and recent applications to the study of fossil bone

    Scanning Microscop.

    (1987)
  • J.C. Cañaveras et al.

    El modelo de relleno, o cómo llegaron los restos a la Galería del Osario

  • T.S. Carvalho et al.

    Erosive effect of dietary substances on deciduous and permanent teeth

    Clin. Oral Invest.

    (2016)
  • W.J. Conover et al.

    Rank transformations as a bridge between parametric and nonparametric statistics

    Am. Stat.

    (1981)
  • R.J. Cook et al.

    Multiplicity considerations in the design and analysis of clinical trials

    J. R. Stat. Soc. Ser. A

    (1996)
  • S. El Zaatari

    Occlusal microwear texture analysis and the diets of historical/prehistoric hunter-gatherers

    Int. J. Osteoarchaeol.

    (2010)
  • S. El Zaatari

    The diets of the Ipiutak and Tigara (Point Hope, Alaska): evidence from occlusal molar microwear texture analysis

  • S. El Zaatari et al.

    Occlusal molar microwear texture analysis: the method and its application for the dietary reconstruction of the Lakonis Neandertal

  • S. El Zaatari et al.

    Diet of upper paleolithic modern humans: evidence from microwear texture analysis

    Am. J. Phys. Anthropol.

    (2014)
  • S. El Zaatari et al.

    Dental microwear texture analysis and the diet of the Scladina child

  • S. El Zaatari et al.

    Neandertal versus modern human dietary responses to climatic fluctuations

    PLOS One

    (2016)
  • A. Estalrrich et al.

    Handedness in Neandertals from the El Sidrón (Asturias, Spain): evidence from instrumental striations with ontogenetic inferences

    PLOS One

    (2013)
  • A. Estalrrich et al.

    Brief Communication: subvertical grooves on interproximal wear facets from the El Sidrón Neandertal dental sample

    Am. J. Phys. Anthropol.

    (2011)
  • A. Estalrrich et al.

    Unique within his group: high incidence of chipping enamel may reflect a specialized behavior in the El Sidrón Neandertal group

    PESHE

    (2013)
  • L. Fiorenza

    Reconstructing diet and behaviour of Neanderthals from Central Italy through dental macrowear analysis

    J. Anthropol. Sci.

    (2015)
  • L. Fiorenza et al.

    Molar macrowear reveals Neanderthal eco-geographic dietary variation

    PLOS One

    (2011)
  • L. Fiorenza et al.

    Dental wear and cultural behavior in Middle Paleolithic humans from the Near East

    Am. J. Phys. Anthropol.

    (2013)
  • L. Fiorenza et al.

    To meat or not to meat? New perspectives on Neanderthal ecology

    Am. J. Phys. Anthropol.

    (2015)
  • J. Fortea et al.

    La cueva de El Sidrón (Borines, Piloña, Asturias): primeros resultados

    Estud. Geol.

    (2003)
  • S. Gaudzinski-Windheuser et al.

    On Neanderthal subsistence in last interglacial forested environments in Northern Europe

  • J.H. Goodwin

    Archaeology of the Oakhurst Shelter, George

    Trans. R. Soc. South Afr.

    (1938)
  • Cited by (32)

    • The Ice Age diet of the La Quina 5 Neandertal of southwest France

      2022, Anthropologie (France)
      Citation Excerpt :

      Numerous dietary reconstructions have appeared since Neandertal dietary proclivities were first inferred using faunal remains (e.g., Lartet and Christy; Hrdlička, 1927; Binford, 1981). Recent reconstructions have incorporated innovative methodological approaches to infer diet, including analyses of residues on stone tools (B. Hardy and Moncel, 2011) and in dental calculus (Henry et al., 2011, 2014; K. Hardy et al., 2012; Power et al., 2018), dental microwear texture analysis (El Zaatari et al., 2011, 2016; Karriger et al., 2016; Estalrrich et al., 2017; Williams et al., 2018, 2019, 2021), dental macrowear (Fiorenza et al., 2011) and isotopic analyses (Bocherens et al., 2001; Richards and Trinkaus, 2009; Wißing et al., 2016). The remains of small, medium, large and very large faunal remains with cut-marks at Neandertal sites serve as evidence of meat-eating while isotopic values like those of carnivores imply a meat-laden diet (Jaouen et al., 2019).

    • The use of plants by Neanderthals as food, medicine, and raw materials

      2022, Updating Neanderthals: Understanding Behavioural Complexity in the Late Middle Palaeolithic
    • Methodological advances in Neanderthal identification, phylogeny, chronology, mobility, climate, and diet

      2022, Updating Neanderthals: Understanding Behavioural Complexity in the Late Middle Palaeolithic
    • Reconstructing Neanderthal diet: The case for carbohydrates

      2022, Journal of Human Evolution
      Citation Excerpt :

      Another method used to explore Neanderthal diet is dental wear analysis, although questions have been raised about its efficacy before (Owen, 2005; Ben-Dor et al., 2021). This evidence suggests that diet varied according to environmental conditions, from a mixed diet in warmer wooded environments to a higher proportion of meat-eating in colder regions (El Zaatari et al., 2011, 2016; Fiorenza et al., 2011, 2018, 2019, 2020; El Zaatari and Hublin, 2014; Pinilla and Trinkaus, 2014; Fiorenza, 2015; Estalrrich et al., 2017; Droke et al., 2020). But diets are generally more complex than they initially appear.

    View all citing articles on Scopus
    View full text