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The diet of the first Europeans from Atapuerca

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OPEN The diet of the first Europeans from

Atapuerca
AlejandroPrez-Prez1,*, MarinaLozano2,3,*, AlejandroRomero4,*,
LauraM.Martnez1,*, JordiGalbany5, BeatrizPinilla1, FerranEstebaranz-Snchez1,
received: 01 June 2016 JosMaraBermdezdeCastro6,7, EudaldCarbonell2,8 & JuanLusArsuaga8,9
accepted: 25 January 2017 Hominin dietary specialization is crucial to understanding the evolutionary changes of craniofacial
Published: 27 February 2017 biomechanics and the interaction of food processing methods effects on teeth. However, the diet-
related dental wear processes of the earliest European hominins remain unknown because most of
the academic attention has focused on Neandertals. Non-occlusal dental microwear provides direct
evidence of the effect of chewed food particles on tooth enamel surfaces and reflects dietary signals
over time. Here, we report for the first time the direct effect of dietary abrasiveness as evidenced by the
buccal microwear patterns on the teeth of the Sima del Elefante-TE9 and Gran Dolina-TD6 Atapuerca
hominins (1.20.8 million years ago Myr) as compared with other Lower and Middle Pleistocene
populations. A unique buccal microwear pattern that is found in Homo antecessor (0.960.8Myr), a
well-known cannibal species, indicates dietary practices that are consistent with the consumption
of hard and brittle foods. Our findings confirm that the oldest European inhabitants ingested more
mechanically-demanding diets than later populations because they were confronted with harsh,
fluctuating environmental conditions. Furthermore, the influence of grit-laden food suggests that a
high-quality meat diet from butchering processes could have fueled evolutionary changes in brain size.

The dietary strategies of the European Lower Pleistocene hominins from Atapuerca (Burgos, Spain) have
been inferred solely from faunal assemblages that were found in the same levels where the human remains
were unearthed. The TE9 Unit at the Sima del Elefante site (1.2Myr) has yielded a broad range of medium and
large-sized mammals and even tortoises that show anthropogenic modifications, which indicate that they were
part of the hominin diet1,2. Moreover, the TD6 level at the Gran Dolina site (0.80.96Myr) has provided evidence
not only of hunted and scavenged mammals3 but also of butchered and eaten human remains, which is the most
ancient evidence of human cannibalism4. However, the feeding habits of these hominins have not been inferred
from a wide range of sources of information similar to the Middle Pleistocene European populations. Dental
wear5,6 and isotopic signals7 have provided valuable information of Middle Pleistocene species. The isotopic sig-
nals are indicative of mainly carnivorous dietary regimens for Neandertal populations. However, carnivorous
regimens contrast with the buccal dental microwear analyses that show dietary habits that include significant
amounts of abrasive plant foods that cause highly abrasive loads on enamel surfaces compared with modern
hunter-gatherer populations8,9. Because of these contradictory interpretations and because most of the academic
attention5 has focused on Neandertals, an independent and comprehensive reconstruction of dietary ecology in
Lower Paleolithic European hominins is necessary. We therefore apply a novel approach that is based on buccal

1
Departament de Biologia Evolutiva, Ecologia i Ciencies Ambientals, Secci Zoologia i Antropologia Biolgica,
Universitat de Barcelona. Av. Diagonal, 643, 08028 Barcelona, Spain. 2Institut Catal de Paleoecologia Humana i
Evoluci Social (IPHES), Zona Educacional 4 (Edifici W3), Campus Sescelades, 43007 Tarragona, Spain. 3rea de
Prehistria, Universitat Rovira i Virgili, Av. Catalunya, 35, 43002 Tarragona, Spain. 4Departamento de Biotecnologa,
Facultad de Ciencias, Universidad de Alicante, Ap. C. 99, 03080 Alicante, Spain. 5Center for the Advanced Study of
Human Paleobiology, Department of Anthropology, The George Washington University, 800 22nd Street NW, Ste
6000, Washington DC 20052, USA. 6Centro Nacional de Investigacin sobre Evolucin Humana (CENIEH), Paseo
Sierra de Atapuerca, 09002 Burgos, Spain. 7UCL Anthropology, 14 Taviton Street, London, WC1H 0BW, UK. 8Centro
Mixto UCM-ISCIII de Evolucin y Comportamiento Humanos, Universidad Complutense de MadridInstituto de Salud
Carlos III, 28029 Madrid, Spain. 9Departamento de Paleontologa, Facultad de Ciencias Geolgicas, Universidad
Complutense de Madrid, 28040 Madrid, Spain. *These authors contributed equally to this work. Correspondence
and requests for materials should be addressed to A.P.-P. (email: martinez.perez-perez@ub.edu) or M. L. (email:
mlozano@iphes.cat)

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dental microwear to reconstruct the dietary habits of the well-documented first inhabitants of Europe and com-
pare them with other Pleistocene species.
Buccal dental microwear refers to the microscopic-scale (106m) wear on non-working enamel surfaces of
premolar and molar teeth that is caused by dietary abrasions1012. Scratches of different lengths and orienta-
tions are formed across buccal enamel surfaces during food breakdown by particles such as silica phytoliths
or exogenous quartz grits11,13. The type and amount of abrasives in chewed foods have been shown critical to
buccal enamel scratch formation processes11,12, which demonstrate a relationship between buccal microwear pat-
terns and abrasive properties despite the lack of attritional tooth-to-tooth contact9,11. The predicted critical loads
required to fracture enamel in humans exceed 500 Newtons (N), whereas the loads required to produce individual
microwear traces are in the order of milli-Newtons (mN)10. In addition, scratch formation is aided by particle
kinetic energy10, producing sufficient load for abrasives to scratch buccal enamel surfaces. Furthermore, in vivo
models have shown that microwear features are produced on buccal enamel surfaces of volunteers consuming
soft diets and that scratch formation is a dynamic process that develops over time and reflects long-term trends in
dietary habits11. The scratch densities on buccal enamel surfaces clearly relate to the increased abrasiveness of the
dietary habits of hunter-gatherer and farmer populations9,12.
The hominins from Sima del Elefante (ATE91; n=1) and Gran Dolina-TD6 (H. antecessor; n=7) are both
from the Sierra de Atapuerca (Burgos, Spain) and cover a chronological range between 1.2 and 0.8Myr14. The
buccal microwear patterns from premolar and molar teeth of these specimens were compared with the buccal
microwear patterns of Lower and Middle Pleistocene hominins (Table1 and Supplementary Text 1), including
the fossil specimens of H. ergaster (1.50.7Myr; n= 7), H. heidelbergensis (0.60.2Myr; n=21, which comprise
individuals from Arago, Kabwe, Pontnewydd and Sima de los Huesos), and H. neanderthalensis from the Iberian
Peninsula (0.050.03Myr; n=6, including Cova Forad, El Sidrn, Figueira Brava and Sima de las Palomas ).
Scanning Electron Microscopy (SEM) micrographs of well-preserved buccal enamel surfaces were recorded at
100magnification. Only buccal enamel surfaces that clearly showed ante-mortem scratches without sedimen-
tary trampling or chemical alterations9,11,12 were considered for microwear analyses (Fig.1a). Diet-induced buccal
microwear shows a scratched pattern with scratches of various lengths and predominant occlusal-to-cervical
orientation11. Instead, non-dietary post-depositional processes are readily identifiable, showing enamel cracks,
abrasion effects from sedimentary particles with scratches usually larger in width (>20 m), erosive effects eras-
ing dietary-related microwear signatures, and enamel prism exposure9,15,16 (see Supplementary Text 2 and Fig.S1
for a detailed description on enamel preservation).
Buccal dental microwear was analyzed from selected SEM micrographs of each individual by using
feature-based established protocols8,9. The buccal microwear patterns were defined by the density (NT), aver-
age length (XT, in m), and standard deviation () of the length (ST) of the overall scratches, as well as classi-
fied by 45 orientation intervals into vertical (V), horizontal (H), mesio-occlusal to disto-cervical (MD), and
disto-occlusal to mesio-cervical (DM) scratch categories in density, length and their dispersion () to identify
the influence of dietary abrasiveness and inter-specific variability in microwear signatures9,12 (see Methods for a
detail description).

Results
We found significant variation in the overall multivariate model (MANOVA: Wilks = 0.108; P= 0.005) indi-
cating that buccal microwear patterns vary among the species examined. The buccal microwear of the earli-
est hominins from Atapuerca stands out among other Pleistocene hominins for the higher total scratch density
(NT= 254.13 25.98; ) compared with the samples of H. ergaster (NT= 198.43 81.19), H. heidelbergensis
(NT= 151.71 67.16) and Iberian Neandertals (NT= 141.50 75.61) (Fig.1b) (extended data TablesS1S3).
Univariate analyses of variance (ANOVAs) comparing the group means revealed significant differences among
the four species for the total (NT: F= 4.430, P=0.009), horizontal (NH: F= 2.913, P=0.047) and disto-mesial
(NDM: F= 8.592, P=0.0005) scratch densities. Pairwise comparisons (Tukeys HSD post-hoc test) showed
that H. antecessor differed from H. ergaster for NDM (P= 0.012), from H. heidelbergensis for NDM (P= 0.001)
and NT (P=0.009), and from Iberian Neandertals for NDM (P=0.000) and NT (P=0.035). The oldest spe-
cies (1.50.8Myr), including H. ergaster, ATE91 and TD6 hominins (H. antecessor), showed the highest den-
sities of scratches, whereas H. heidelbergensis and Neandertals presented lower scratch density values on the
buccal enamel surfaces. No significant differences were observed in the H. heidelbergensis populations (Arago,
Pontnewydd and Sima de los Huesos specimens). A Canonical Variate Analysis (CVA) was conducted to max-
imizes the among species variation using a linear combination of microwear variables9. The CVA included 39
fossil specimens (excluding the specimens from ATE91, Kabwe and Mauer that were classified post-hoc), and
all 15 microwear variables analyzed. The taxa compared, showing similar sample sizes (from 6 to 8 specimens),
correspond to H. ergaster, the well-defined populations of H. antecessor and H. heidelbergensis, and the Iberian
Neandertals. Five canonical variates were extracted (Wilks = 1.467, P=0.039) (extended data TableS4). The
first two CVs (Fig.2) explained 70.247% of the total variance. Individual ANOVAs showed significant differences
among the groups for both CV1 (43.153%; F= 19.951, P<0.001) and CV2 (27.094%; F= 18.557, P< 0.001).
CV1 mainly correlated (Pearson r, P<0.05) with XDM (r=0.392) and NMD (r=0.330). The Gran Dolina-TD6
hominins formed a cluster with the highest CV1 values and were clearly distant from the H. ergaster and Iberian
Neandertal specimens, which showed less and longer mesio-distal scratches (NMD and XMD, respectively).
Otherwise, CV2 significantly correlated (Pearson r, P<0.05) with NDM (r=0.680) and NT (r=0.553). All the
density variables positively correlated with CV2, and most length variables (except XV) negatively correlated
with this factor. Significant differences in CV2 scores were found between the earliest Gran Dolina specimens
and all other groups because of overall higher density and shorter scratches. Furthermore, differences were found
between H. ergaster and H. heidelbergensis (P=0.016) but not with the Iberian Neandertals analyzed (P> 0.05).
The post-hoc probability of correct classification of the CVA was 74.36% (33.33% after Jackknife cross-validation)

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Taxon and specimen Known age (Myr) Tooth

Homo ergaster 1.50.7
KNM-ER 806 LM1
KNM-ER 807 RM3
KNM-ER 820 LM1
KNM-ER 992 RM1
KNM-WT 15000 RM1
OH 23 LP4
SK15 LM1
Homo sp.
AtapuercaSima del Elefante (TE) 1.2
ATE9-1 LP4
Homo antecessor
AtapuercaGran Dolina (GD-TD6) 0.8
H1 RM1 (ATD6-5)
H2 Lm1 (ATD6-14)
H3 LM1 (ATD6-69)
H5 RM1 (ATD6-94)
H7 LM1 (ATD6-96)
H10 LM2 (ATD6-113)
H11 Lm1 (ATD6-112)
Homo heidelbergensis 0.60.2
Mauer RM1
AtapuercaSima de los Huesos (SH)
IV RM1 (AT-3178)
VII LM2 (AT-270)
VIII LM1 (AT-3177)
XVII RM1 (AT-20)
XIX LM1 (AT-576)
XX LM1 (AT-406)
XXII RM2 (AT-588)
XXVI RM1 (AT-561)
Arago
A7 RP4
A13 RM1
A21 RM2
A40 RM1
A54 RM1
A69 RM2
Pontnewydd
PN1 RM2
PN5 RP4
PN7 LP3
PN12 LM1
PN20 LP3
Kabwe
BH1 RM1
Homo neanderthalensis 0.050.03
Cova Forad
CF-1 LM1
El Sidrn
SDR-007d LM1
SDR-012 LM1
Sima de las Palomas
SP-29 RM2
SP-59 LM1
Figueira Brava
FB LP4

Table 1. Fossil teeth samples included in the buccal microwear analysis. A single premolar or molar tooth
was used to represent each individual. The tooth samples comprised high-resolution casts that were made from
the original specimens and were stored at the Zoology and Biological Anthropology section, Faculty of Biology
(University of Barcelona). The specimen arrangement and dating results are from scientific publications (see
Supplementary Text 1 for sample details).

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Figure 1. Buccal microwear pattern variability of the studied fossil groups. (a) The well-preserved buccal
enamel surface of the El Sidrn Neandertal (the left SEM image) and H. antecessor (ATD6-5) specimens. Note
the highly abraded surfaces in the H. antecessor H1 specimen. Each micrograph represents an enamel patch
of 0.56mm2 on the mandibular first molars at 100magnification. The scale bar is 100m (common to both
images). (b) Dot-plot showing the scratch density (NT) and average scratch length (XT, in m) values for the
analyzed species or individual. Interspecific differences in abrasiveness that relate to dietary habits are observed.
The error bars denote 1 standard deviation. The grey square areas delimit the mean values for all samples. See
Table1 and Supplementary Text 1 for the samples composition and details.

(extended data TableS5). The Atapuerca ATE91 specimen was classified into the H. antecessor group with an
88.4% post-hoc probability, and Kabwe was grouped with H. ergaster with a probability of 95.8%. The Mauer
individual was classified with varying probabilities as Sima de los Huesos (44.1%), Arago (38.6%) or Pontnewydd
(15.0%) but not as H. antecessor (2.4%), H. ergaster or Neandertal (0% in both cases).

Discussion
The clearly distinct position of the earliest hominins from Atapuerca supports the hypothesis that their dietary
habits included higher amounts of fracture-resistant foods. Between 1.2 and 0.8Myr ago, the paleoenvironmental
records of Sierra de Atapuerca indicate a rich and stable ecosystem. Woodland areas with conifers and mesic
Mediterranean trees dominated the region, and the hominins lived in open landscapes with an abundance of
humid meadows and woodlands17. Cut and percussion marks in the long bones of mammals are evidence of the
TE9 hominins ability to chew meat and bone marrow18. The wide spectrum of animals that were consumed has
been interpreted as an opportunistic subsistence-behavior1. The mammal species diversity at Gran Dolina-TD6
(0.960.8Myr), including herbivores, carnivores and cannibalized hominins, along with evidence of skinning,
defleshing, marrow extraction and bone chewing activities suggest that hominin subsistence strategies included
systematic hunting and corpse exploitation with a more developed Mode 1 technology than TE93,19,20. In addition,
recent evidence of Celtis seeds at this site indicates the consumption of wild plant matter21.
Buccal dental microwear patterns cannot discriminate the diet composition among populations, but it is
clearly indicative of overall dietary-related habits, abrasive particle content (both intrinsic to foodstuffs and
gritty contaminants) and food processing techniques, such as lithic technology or other food processing meth-
ods11,12,22. Current archaeological evidence indicates no regular use of fire for cooking in the European Middle

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Figure 2. Bivariate plot of scores for the first two canonical variates (70.24% of total variance) showing
interspecific variability in buccal microwear patterns. Note that H. antecessor individuals exhibit a distinct
buccal microwear pattern that is characterized by high scratch densities, whereas H. ergaster more closely
resembles Iberian Neandertals. Significant overlap is recorded among the Sima de los Huesos (open triangles
pointing downwards), Arago (open triangles pointing upwards), and Pontnewydd (filled triangles) populations,
which reflect similar dietary abrasiveness. The symbols are similar to the previous plots (see Fig.1). All analyzed
individuals are plotted. The isolated ATE91 (open square), Kabwe (BH1, filled diamond) and Mauer (Ma,
open diamond) tooth specimens were classified post-hoc with the derived canonical variates. Convex hulls
show the distribution limits of each considered species. See Table1 and Supplementary Text 1 for a sample
description.

Pleistocene until approximately 300,000400,000 years ago23. Because of the absence of fire evidence at both
Atapuerca sites, ATE9-1 and Gran Dolina-TD6 hominins have been assumed to have consumed food items
raw2,24. This assumption is consistent with the presence of features on human and other animal bone surfaces that
are caused by human chewing in Gran Dolina-TD6. This assumption is also consistent with microwear fabrics
(pits and chipping) on the occlusal surfaces of the anterior teeth of ATE9-1 and H. antecessor that resulted from
highly demanding dietary regimes with a heavy loading bite that is compatible with bone crushing to access the
marrow24,25. Thus, non-thermal processed foods, including tough and/or hard items, as well as contaminant grit
from the soil, are expected to have been part of the diets of H. antecessor more than H. heidelbergensis. Both
H. heidelbergensis and Neandertals show a clear reduction in microwear densities compared with H. antecessor
that may relate to the differences in food-processing techniques concerning the use of more advanced tool tech-
nologies (Modes 2 and 3 might be more efficient than Mode 1), which has already been suggested to interpret the
interspecific microwear variability of the Sima de los Huesos specimens regarding Neandertals8,9. Accordingly,
the distinct microwear patterns of H. antecessor, characterized by high microwear densities, suggest that it might
have specialize in the consumption of harder and/or tougher foods (more mechanically-challenging) than
H. ergaster and Neandertals. The microwear texture analyses on occlusal enamel surfaces of H. ergaster specimens
have been suggested to be indicative of a broad-based diet with neither extremely hard nor tough foods26. The
isotope-based dietary signal suggests that European Neandertals (~37,000120,000 years ago) would have con-
sumed significant amounts of animal proteins7. However, meat could not be an exclusive food item in Neandertal
diets because the plant micro-remains that have been found in the dental calculus indicates that their diet would
have included starch-rich plant foods, mainly from grass seeds and underground storage organs (USOs)27,28. The
buccal microwear patterns of Neandertal teeth have been interpreted as indicative of the consumption of gener-
alized diets that are consistent with the consumption of some plant foods9. A substantial preparation previous to
ingestion may have resulted in a less-abrasive diet in Neandertals than in the H. heidelbergensis specimens, which
place Neandertals in a range of buccal microwear signatures between archaic H. heidelbergensis hominins8,9 and
modern human hunter-gatherer populations12.

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Meat and USOs differ mechanically in resistance and fracture properties22, but their stiffness and abrasive-
ness during microwear formation depend greatly on food processing methods and bite forces11. The mechanical
properties of abrasive particles in foodstuffs are responsible for enamel indentation5,13. Plant phytoliths seem less
capable of fracturing enamel than quartz dust, which is directly involved in the overall scratching and erasing of
enamel surfaces during long periods11,29. In this regard, the highly abraded buccal surfaces of H. antecessor could
indicate the ingestion of a large amount of grit-laden foodstuffs.
The highly abraded enamel microwear patterns that have been observed in the earliest Atapuerca hominins
(1.20.8Myr ago) are clearly distinct from Iberian Neandertals and H. heidelbergensis. Our findings suggest that
Homo antecessor could have specialized in the exploitation of tough, hard and brittle foodstuffs with adhered
grit particles, which may include underground plants (including grit), collagen or connective tissue, and bone.
This mechanically-demanding diet would have required strong shearing and grinding processes during food
consumption, although unprocessed meat breakdown requires less chewing force than tough plant foods that
increase the scratch formation rates29. Thus, hunting or scavenging to obtain animal resources30 may also be
consistent with the highly abrasive microwear pattern that is observed. A high-quality diet including meat con-
sumption may have not only fueled the energy gain that is needed to support an enlarged brain31, which is the
case of H. antecessor with a brain size of approximately 1,000cc compared with H. ergaster (764cc)32, but also
represented a significant food source in a highly demanding environment where preferred foods fluctuated sea-
sonally. Furthermore, not-fully developed tool technologies for food preparation, either lithic or otherwise, may
have resulted in scarcely processed foods that included high amounts of abrasives that would also contribute to
the highly abraded enamel surfaces that were observed. Whatever the relative significance of each of these fac-
tors, the buccal microwear patterns that are shown by the earliest hominins from Atapuerca likely signal a highly
demanding diet that evolved to cope with both ecological and cultural constraints.

Methods
Data acquisition. Original tooth crowns were cleaned with acetone and ethanol solutions using a cotton-
ear-bud and air-dried prior to molding. Whole tooth crown molds were made with President MicrosystemTM
polysiloxane vinyl impression material (Coltne-Whaledent Corp.) following standard procedures33,34. High-
resolution casts were made with Epo-tek 301 (Epoxy Technologies, Inc. Billerica, MA) epoxy resin34. The casts
were examined at 40with a stereomicroscope to determine their suitability for microwear analysis. The casts
were mounted on aluminum stubs and sputter-coated with a ~15nm layer of gold-palladium and analyzed under
Scanning Electron Microscopy (SEM) at 100magnification, an 1825mm working distance (WD), and 15kV
of acceleration voltage9,33. Variations in the SEM WD did not affect the microwear feature measures because all
analyzed images were cropped to exactly the same square area (see below). During scanning, the buccal enamel
surface of each tooth crown was placed perpendicular to the electron beam, with the occlusal crown rim facing
upwards in all SEM images. The micrographs were taken in the middle third of the crown to avoid both the occlu-
sal and cervical thirds of the buccal crown surface9,35. The micrographs were cropped with Adobe Photoshop
CS5 to exactly cover 0.56mm2 (748.33 748.33 m) of enamel surface, and all micrograph measurements were
properly scaled prior to analysis8,9. A high-pass (50 pixels) filter and automatic grey level adjustment were applied
to all cropped digital grey-scale selected micrographs to reduce shadows and enhance the images contrast9,33.

Microwear analysis. Only micrographs showing well-preserved enamel surfaces, without post-mortem
physical or chemical alterations, were selected for microwear analysis9,15,16 (Supplementary Text 2 and Fig.S1).
Following previous procedures8,9,12, the length (in m) and slope (with respect to the horizontal occlusal plane)
of all observed scratches in the studied enamel patch were measured by using a semi-automated procedure with
SigmaScan Pro 5.0 (SPSSTM) software, including scratches truncated by the edge of the micrographs9,11,35. Both
parallel and overlapping scratches were measured as independent lineal abrasion units. Scratches that measured
less than 10m in length (approximately 4 times the average width of the scratches) were discarded.
The buccal microwear variables measured included the scratch density (N), the average length (X) and the
standard deviation of the length (S) of all the recorded scratches (T) in each analyzed micrograph (variables
NT, XT and ST), as well as for the four 45 orientation categories (H, V, MD, DM)8,35. The classification of each
scratch to an orientation category varied depending on the tooth position (upper, lower) and side (left, right)
and on the angle of orientation with respect to the Cemento-Enamel Junction (CEJ, 0 of orientation)35 as fol-
lows: mesio-occlusal to disto-cervical (mesio-distal, MD) scratches (22.5< angle67.5 for upper, left or
lower, right teeth; or 112.5 angle<157 for upper, right or lower, left teeth); disto-occlusal to mesio-cervical
(disto-mesial, DM) scratches (22.5< angle67.5 for upper, right or lower, left teeth; or 112.5 angle< 157
for upper, left or lower, right teeth); vertical (V) scratches (67.5< angle<11.5) and, horizontal (H) scratches
(157.5 angle22.5). Consequently, a total of 15 variables (NT, XT, ST, NV, XV, SV, NH, XH, SH, NMD, XMD,
SMD, NDM, XDM, and SDM) accounted for the buccal-microwear pattern derived for each studied tooth.
Since the inter-observer error is a major concern in microwear research, both for the occlusal36 and buccal37
enamel surfaces, the micrographs of the specimens under study were measured by a single observer (LMM).
However, inter-observer error analyses have not shown significant differences in the buccal microwear measure-
ments among experienced researchers37.

Statistical Analysis. All the studied variables passed the Kolmogorov-Smirnov normality tests (Z= 0.441.24;
P>0.05). A multivariate analysis of variance (MANOVA) was calculated with the values for every microwear
density and length attributes as dependent variables, to determine the significance of the inter-specific varia-
bility in microwear signatures9,11. One-way analyses of variance (ANOVA) and post hoc pairwise comparisons
that used the Tukeys Honest Significant Difference (Tukeys HSD) test were used in the ANOVA tests to check
the inter-specific and population differences in the microwear patterns. Finally, a Canonical Variates Analysis

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(CVA) was performed to show the major trends in the buccal microwear patterns among the groups considered,
not including the isolated teeth of the ATE91, Kabwe (BH1) and Mauer specimens for which the CV values
were computed by using the functions that were derived from the analysis. The descriptive statistics and tests at
=0.05 significance level were conducted by using Addinsoft XLSTAT-3.02.

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Acknowledgements
We want to express our gratitude to the Atapuerca Team and to the institutions that granted permission to study
the fossil materials. This work was supported by the research grants, from the Direccin General de Investigacin
of Ministerio Ciencia y Tecnologa (Spain), numbers CGL2007-60802/BTE, CGL2011-22999, CGL2012-
38434-C03-01/02/03 and CGL2014-52611-C2-1-P, as well as by the grant 2009SGR884 Group of Study on the
Evolution of Hominins and other Primates and grant 2014SGR900 Group of Analyses on Socio-Ecological
Processes, Cultural Changes and Population Dynamics during Prehistory (GAPS) and CERCA Programme of the

Scientific Reports | 7:43319 | DOI: 10.1038/srep43319 7

www.nature.com/scientificreports/

Generalitat de Catalunya. Scanning electron micrographs were obtained at the Centres Cientfics i Tecnolgics
(CCiT) of the Universitat de Barcelona and Serveis Tecnics dInvestigaci of the Universitat dAlacant.

Author Contributions
A.P.P. and M.L. conceived the study and designed the research. J.L.A., J.M.B.C. and E.C. collected the Atapuerca
sample. A.P.P. collected the hominin comparative samples. L.M.M., A.R., B.P. and F.E. prepared the dental casts
and obtained SEM images. L.M.M. measured the buccal microwear patterns in all SEM images. A.P.P., A.R. and
J.G. analyzed the data. A.P.P., M.L. and A.R. wrote the paper, and all authors discussed the results and commented
on the manuscript. A.P.P., J.L.A., J.M.B.C. and E.C. provided the funding and contributed to the study design.

Additional Information
Supplementary information accompanies this paper at http://www.nature.com/srep
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Prez-Prez, A. et al. The diet of the first Europeans from Atapuerca. Sci. Rep. 7, 43319;
doi: 10.1038/srep43319 (2017).
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Scientific Reports | 7:43319 | DOI: 10.1038/srep43319 8

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