The Science of Nature

, 104:2

Diet and environment 1.2 million years ago revealed through analysis of dental calculus from Europe’s oldest hominin at Sima del Elefante, Spain

  • Karen Hardy
  • Anita Radini
  • Stephen Buckley
  • Ruth Blasco
  • Les Copeland
  • Francesc Burjachs
  • Josep Girbal
  • Riker Yll
  • Eudald Carbonell
  • Jose María Bermúdez de Castro
Short Communication

DOI: 10.1007/s00114-016-1420-x

Cite this article as:
Hardy, K., Radini, A., Buckley, S. et al. Sci Nat (2017) 104: 2. doi:10.1007/s00114-016-1420-x

Abstract

Sima del Elefante, Atapuerca, Spain contains one of the earliest hominin fragments yet known in Europe, dating to 1.2 Ma. Dental calculus from a hominin molar was removed, degraded and analysed to recover entrapped remains. Evidence for plant use at this time is very limited and this study has revealed the earliest direct evidence for foods consumed in the genus Homo. This comprises starchy carbohydrates from two plants, including a species of grass from the Triticeae or Bromideae tribe, meat and plant fibres. All food was eaten raw, and there is no evidence for processing of the starch granules which are intact and undamaged. Additional biographical detail includes fragments of non-edible wood found adjacent to an interproximal groove suggesting oral hygiene activities, while plant fibres may be linked to raw material processing. Environmental evidence comprises spores, insect fragments and conifer pollen grains which are consistent with a forested environment.

Keywords

Human evolution Sima del Elefante Atapuerca Dental calculus Diet Microfossils Paleoenvironment 

Background

Sima del Elefante is located in the Sierra de Atapuerca, northern Spain, one of the several archaeological and palaeontological sites providing a continuous sequence from 1.2–0.3 Ma (Rodríguez et al. 2011)(Fig. 1). In 2007, a hominin mandibular fragment (ATE9-1) was uncovered in the TE9 stratigraphic level dated to the Early Pleistocene (1.2–1.1 Ma), making this one of the oldest hominin remains in Europe (Carbonell et al. 2008) together with Barranco León (Orce, Spain) (1.02 and 1.73 Ma) (Toro-Moyano et al. 2013). The fragment, and a nearby isolated tooth (lower LP4) from the same individual, is not complete enough for a taxonomic assignment and is therefore referred to as Homo sp. (Bermúdez de Castro et al. 2011). A large assemblage of animal bones suggests meat consumption, while stone tools provide evidence for meat processing and marrow extraction (Carbonell et al. 2008). Here, we investigate ingested and inhaled remains entrapped in dental calculus. Dental calculus results from the calcification of plaque which is formed by the activity of sugars energised by bacteria (Lieverse 1999). It is common on archaeological skeletal material and is a store of environmental and biographical information on past human and hominin populations (Hardy et al. 2012, 2015a, Radini et al. 2016, Warinner et al. 2014).

Methods

Dental calculus is present on all but one of the teeth. Tooth LP4 had significant accumulations of calculus; some of which was in the form of a crescent (Martiñón-Torres et al. 2011) representing the shape of the subgingival crevice. Two fragments of dental calculus (0.5 and 0.8 mg) were removed from this tooth using an ultrasonic scalar (RS Tri-Scalar: compact). The larger sample was analysed using the dual methods of thermal desorption-gas chromatography-mass spectrometry (TD-GC-MS) and pyrolysis-gas chromatography-mass spectrometry (Py-GC-MS) to investigate any surviving chemical compounds (S1). The smaller sample was degraded for microfossil extraction (S2). Microfossils were mounted onto eight microscope slides for optical image analysis following established procedures for contamination control and extraction of the material (Hardy et al. 2015a) (S2). Samples of surrounding sediment and fragments of animal (deer) dental calculus from the same context were also analysed to provide contextual information (S3).

Results

No chemical signatures survived (S1). The earliest age in which they have currently been detected in dental calculus is 300–400,000 years (Hardy et al. 2015a). However, an extensive microfossil assemblage was recovered.

Diet

Several groups of starch granules were identified. Starch occurs as insoluble, semi-crystalline granules in most plant tissues but found in largest amounts in seeds and storage organs. Several small groups of bimodal starch granules (A, 20–30 μm; B, 5–8 μm, Fig. 2.2, 2.3) were found in the hominin calculus and a small group of similar bimodal starches was also detected in the deer dental calculus, confirming that these plants were present in the surroundings and exploited by both the hominin and animal populations. Bimodal distribution of starch granules is a distinctive characteristic present in the edible seeds of the Triticeae tribe and some species of the Bromideae tribe of the grass family (Poaceae). It is plausible that these ancient grasses were ingested as food. Grasses produce abundant seeds in a compact head, which may be conveniently chewed, especially before the seeds mature fully, dry out and scatter. A second plant source is represented by one cluster of granules (5–10 μm) packed tightly together (Fig. 2.1). Though it is not normally possible to identify plant sources on the basis of starch granule morphology alone, in this case and despite the antiquity of the material, their size and form indicate food items rather than transient leaf starch granules, which are small and occur individually due to diurnal cycles of accumulation and breakdown. Accidental inhalation of the starch granules is unlikely because the granules would be enclosed inside a cellular structure in the plant material and not free to be airborne.

Several different types of fibres were recovered in the calculus, including non-edible wood debris as well as other indeterminate fibres of plant origin. Some other fibrous remains lack the characteristics of plant cell walls suggesting an animal origin, possibly fragments of connective tissue such as tendons or ligaments, and likely to be linked to the consumption of food.

Environment

Particles up to 70 μm habitually enter the mouth during oral breathing (Se et al. 2010) and can become embedded in dental calculus. Several conifer (Pinaceae) pollen grains, comparable to the pollen grains extracted from sediment at the same level (Rodríguez et al. 2011), were recovered from the hominin dental calculus (Fig. 2.4). The presence of conifer pollen demonstrates that these species were present and indicates close proximity to a forested environment. At Gesher Benot Ya’aqov, Israel, possible evidence of woodworking occurs a relatively short time later 0.79 Ma (Goren-Inbar et al. 2002), and this is likely to have occurred also at Sima del Elefante. Equally, most conifer trees have edible needles, nuts and inner bark, and these are very likely to have been exploited as food, while the resins have medicinal qualities (Hardy and Kubiak-Martens 2016). The numerous pollen grains in the dental calculus contrast with the paucity of pollen in the sediment (Rodríguez et al. 2011), considered to be due to the oxidative sedimentary environment of the karstic cavities (Carrión 2009), highlighting the value of dental calculus for paleoenvironmental reconstruction.
Fig. 1

The Sima del Elefante site

Two insect fragments, part of a Lepidoptera wing scale (Fig. 2.5) and a fragment of insect leg, and two types of fungal spores (Fig. 2.6, 2.7), including one very similar to the common plant pathogen Alternaria, were recovered. Both the fungal spores and insect remains included the presence of chitin. Fungal spores are common in the environment and are challenging to identify due to the vast numbers of species. Today, Alternaria is a very common genus and has world-wide distribution, with saphrophyte and pathogenic species. Though fruiting fungi, such as mushrooms, are likely to have been eaten, the spores were most likely breathed in as airborne particles or accidentally ingested. A small number of minerals were detected; they most probably reached the mouth, on food or on other dirty items placed in the mouth.
Fig. 2

Microfossils extracted from dental calculus. 1 Cluster of starch granules. 2 Group of bimodal starch granules. 3 Bimodal starch granules. 4 Conifer pollen grains. 5 Plant fibre. 6 Fungal spore. 7 Amorphous animal tissue. 8 Alternaria-type spore. 9 Lepidoptera wing fragment. Scale bar 20 μm

Discussion

Evidence for plant exploitation in the earliest stages of hominin occupation in Europe is extremely limited. The material emerging from dental calculus provides new insights into hitherto unobtainable evidence for use of plants as food, medicine and raw materials (Hardy et al. 2012, Hardy et al. 2015a, Radini et al. 2016, Warinner et al. 2014). When viewed from the broader perspective of animal behaviour, these new insights are unsurprising. All modern chimpanzee behaviour is considered to be within the capability of the chimpanzee/human last common ancestor (CHLCA) (McGrew 2010a) and therefore all hominin species. Chimpanzees demonstrate botanical knowledge (Janmaat et al. 2013), use plant materials to construct composite tools (McGrew 2010b) and exploit a wide range of plants as food and as medicine (Huffman 2003) while even insect species adapt their diet according to their health (Singer et al.,2009). Knowledge and use of plants will have been well within the capabilities of the Sima de Elefante hominins.

The dental wear on this mandible is heavy, indicating prolonged paramasticatory or masticatory behaviours (Martiñón-Torres et al. 2011). The fibrous materials identified from the dental calculus correlate with this evidence and suggest raw material working. A well-developed interproximal groove is present just above the accumulation of calculus which produced the wood fragments. Interproximal grooves, found on teeth of all Homo species since H. habilis, have long been linked to tooth picking (Ungar et al. 2001), while oral hygiene activities using plant materials occur in modern higher primate populations (McGrew and Tutin 1973). A close association between a wood fibre and an interproximal groove was first detected in a 49,000 year old Neanderthal individual (Radini et al. 2016) and the evidence from Sima del Elefante may also be indicative of oral hygiene activity.

The timing of controlled use of fire remains unclear though evidence from south Spain suggests that it was in use at least 800,000 years ago (Walker et al. 2016). The development of fire for cooking is considered an essential part of hominin evolution (Wrangham and Conklin-Brittain 2003), an important feature of brain development through improved access to preformed glucose (Hardy et al. 2015b) and a focus for developing social behaviour (Wiessner 2014). However, the discrepancy between the lack of archaeological evidence and the need for fire in human evolution continues to be problematic (Gowlett and Wrangham 2013). The present study is consistent with the absence of archaeological evidence for controlled use of fire at Sima del Elefante and provides positive evidence for raw food; the intact nature of the starch granules demonstrates a lack of any form of pre-ingestion preparation, while all the fibres detected, both animal and plant, are uncharred.

The previous record for survival of this broad range of dietary and environmental material is 300–400,000 years at Qesem Cave, Israel, where evidence for fire, and chemical compounds demonstrating consumption of essential fatty acids, was identified (Hardy et al. 2015a). The present study significantly extends the age for recovery of a wide range of dietary, environmental remains and cultural activity and highlights the value of dental calculus as a source of biographical information during key stages of human evolution.

Finding evidence for the use of plants during the Lower Palaeolithic is very challenging and the role of plants in these early periods has consequently been largely overlooked. However, humans cannot survive without eating plants (Hardy et al. 2015b). Our evidence for the consumption of at least two different starchy plants, in addition to the direct evidence for consumption of meat and use of plant-based raw materials, suggests that this very early European hominin population had a detailed understanding of its surroundings and a broad diet.

Acknowledgments

Funding was provided by the Spanish Ministry of Science and Innovation. (I+D code HAR2012-3537). Funding was provided by the Spanish Ministry of Science and Innovation (MINECO): grant numbers CGL2015-65387-C3-1 & 3-P, as well as the Junta de Castilla y León. The sample was taken with the collaboration of CENIEH Staff". (I+D code HAR2012-3537).

Supplementary material

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Karen Hardy
    • 1
    • 2
  • Anita Radini
    • 3
  • Stephen Buckley
    • 3
  • Ruth Blasco
    • 4
  • Les Copeland
    • 5
  • Francesc Burjachs
    • 1
    • 6
    • 7
  • Josep Girbal
    • 8
  • Riker Yll
    • 8
  • Eudald Carbonell
    • 6
    • 7
  • Jose María Bermúdez de Castro
    • 4
  1. 1.ICREABarcelonaSpain
  2. 2.Departament de PrehistòriaFacultat de Filosofia i Lletres, Universitat Autònoma de BarcelonaBarcelonaSpain
  3. 3.Department of ArchaeologyUniversity of YorkYorkUK
  4. 4.Centro Nacional de Investigacion sobre la Evolución HumanaBurgosSpain
  5. 5.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia
  6. 6.IPHES, Institut Català de Paleoecologia Humana i Evolució SocialTarragonaSpain
  7. 7.URV, Universitat Rovira i Virgili, Area de PrehistoriaTarragonaSpain
  8. 8.Universitat Autònoma de BarcelonaBarcelonaSpain