Chronological reassessment of the Middle to Upper Paleolithic transition and Early Upper Paleolithic cultures in Cantabrian Spain

Abstract

Methodological advances in dating the Middle to Upper Paleolithic transition provide a better understanding of the replacement of local Neanderthal populations by Anatomically Modern Humans. Today we know that this replacement was not a single, pan-European event, but rather it took place at different times in different regions. Thus, local conditions could have played a role. Iberia represents a significant macro-region to study this process. Northern Atlantic Spain contains evidence of both Mousterian and Early Upper Paleolithic occupations, although most of them are not properly dated, thus hindering the chances of an adequate interpretation. Here we present 46 new radiocarbon dates conducted using ultrafiltration pre-treatment method of anthropogenically manipulated bones from 13 sites in the Cantabrian region containing Mousterian, Aurignacian and Gravettian levels, of which 30 are considered relevant. These dates, alongside previously reported ones, were integrated into a Bayesian age model to reconstruct an absolute timescale for the transitional period. According to it, the Mousterian disappeared in the region by 47.9–45.1ka cal BP, while the Châtelperronian lasted between 42.6k and 41.5ka cal BP. The Mousterian and Châtelperronian did not overlap, indicating that the latter might be either intrusive or an offshoot of the Mousterian. The new chronology also suggests that the Aurignacian appears between 43.3–40.5ka cal BP overlapping with the Châtelperronian, and ended around 34.6–33.1ka cal BP, after the Gravettian had already been established in the region. This evidence indicates that Neanderthals and AMH co-existed <1,000 years, with the caveat that no diagnostic human remains have been found with the latest Mousterian, Châtelperronian or earliest Aurignacian in Cantabrian Spain.

Full text

RESEARCH ARTICLE
Chronological reassessment of the Middle to
Upper Paleolithic transition and Early Upper
Paleolithic cultures in Cantabrian Spain
Ana B. Marı
´n-Arroyo
1,2
*, Joseba Rios-Garaizar
3
, Lawrence G. Straus
4
, Jennifer R. Jones
1
,
Marco de la Rasilla
5
, Manuel R. Gonza
´lez Morales
1
, Michael Richards
6
, Jesu
´s Altuna
7
,
Koro Mariezkurrena
7
, David Ocio
8
1Instituto Internacional de Investigaciones Prehisto
´ricas de Cantabria, (Universidad de Cantabria,
Santander, Gobierno de Cantabria), Santander, Spain, 2Leverhulme Centre for Evolutionary Studies,
Department of Archaeology, University of Cambridge, Cambridge, United Kingdom, 3Centro Nacional de
Investigacio
´n de la Evolucio
´n Humana, Burgos, Spain, 4Department of Anthropology, MSC01 1040,
University of New Mexico, Albuquerque, New Mexico, United States of America, 5Departamento de Historia,
Universidad de Oviedo, Oviedo, Spain, 6Department of Archaeology, Simon Fraser University, Burnaby,
British Columbia, Canada, 7Centro de Conservacio
´n e Investigacio
´n de los Materiales Arqueolo
´gicos y
Paleontolo
´gicos de Gipuzkoa, Donostia/San Sebastia
´n, Spain, 8Department of Civil and Environmental
Engineering, Imperial College London, London, United Kingdom
*marinab@unican.es
Abstract
Methodological advances in dating the Middle to Upper Paleolithic transition provide a better
understanding of the replacement of local Neanderthal populations by Anatomically Modern
Humans. Today we know that this replacement was not a single, pan-European event, but
rather it took place at different times in different regions. Thus, local conditions could have
played a role. Iberia represents a significant macro-region to study this process. Northern
Atlantic Spain contains evidence of both Mousterian and Early Upper Paleolithic occupa-
tions, although most of them are not properly dated, thus hindering the chances of an
adequate interpretation. Here we present 46 new radiocarbon dates conducted using ultra-
filtration pre-treatment method of anthropogenically manipulated bones from 13 sites in the
Cantabrian region containing Mousterian, Aurignacian and Gravettian levels, of which 30
are considered relevant. These dates, alongside previously reported ones, were integrated
into a Bayesian age model to reconstruct an absolute timescale for the transitional period.
According to it, the Mousterian disappeared in the region by 47.9–45.1ka cal BP, while the
Cha
ˆtelperronian lasted between 42.6k and 41.5ka cal BP. The Mousterian and Cha
ˆtelperro-
nian did not overlap, indicating that the latter might be either intrusive or an offshoot of the
Mousterian. The new chronology also suggests that the Aurignacian appears between
43.3–40.5ka cal BP overlapping with the Cha
ˆtelperronian, and ended around 34.6–33.1ka
cal BP, after the Gravettian had already been established in the region. This evidence indi-
cates that Neanderthals and AMH co-existed <1,000 years, with the caveat that no diagnos-
tic human remains have been found with the latest Mousterian, Cha
ˆtelperronian or earliest
Aurignacian in Cantabrian Spain.
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 1 / 20
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OPEN ACCESS
Citation: Marı
´n-Arroyo AB, Rios-Garaizar J, Straus
LG, Jones JR, de la Rasilla M, Gonza
´lez Morales
MR, et al. (2018) Chronological reassessment of
the Middle to Upper Paleolithic transition and Early
Upper Paleolithic cultures in Cantabrian Spain.
PLoS ONE 13(4): e0194708. https://doi.org/
10.1371/journal.pone.0194708
Editor: John P. Hart, New York State Museum,
UNITED STATES
Received: August 11, 2017
Accepted: March 8, 2018
Published: April 18, 2018
Copyright: ©2018 Marı
´n-Arroyo et al. This is an
open access article distributed under the terms of
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This research has been supported by the
European Commission through FP7-PEOPLE-
2012-CIG (Ref: 322112), the Spanish Ministry of
Economy and Competitiveness (HAR2012-33956
and RYC-2011-00695), Cantabria Campus
International and University of Cantabria to ABMA.
The Instituto Internacional de Investigaciones

Introduction
The Middle to Upper Paleolithic transition is generally associated with the replacement of
local Neanderthal populations by Anatomically Modern Humans (AMH) in western Eurasia
[1]. One of the most debated issues is the precise chronology of the replacement of the popula-
tion and its potential relationship with major biological, environmental and cultural events.
Due to recent revisions of archaeological, chronological and geographical data, the spatio-tem-
poral delimitation of the Middle to Upper Paleolithic transition in central and western Europe
has improved [1–5]. Methodological developments in radiocarbon dating that remove young
carbon contamination from old organic samples [6–7] have been crucial for establishing accu-
rate chronologies, especially at the radiocarbon limit around ~50,000 years ago, when the Mid-
dle to Upper Paleolithic transition took place. Thus, the re-dating of several key sites in Europe
has produced older ages than previously thought [1]. The timing of Neanderthal disappearance
in northwestern Iberia (~48-46ka uncal BP) and Italy (~44-42ka cal BP) and the age of so-
called “transitional industries” (Cha
ˆtelperronian and Uluzzian, both 44 to 40ka cal BP) have
been recently delimited [1,3]. While the attribution to Neanderthals of the Cha
ˆtelperronian
in northern Iberia and southwestern France is seldom contested (but see [8]), the question of
the makers of the Uluzzian is still debated. Human deciduous teeth found in Southern Italy
(Grotta del Cavallo) suggest that AMH were the makers of the Uluzzian [9], whereas other
researchers continue to argue for Neanderthal authorship [10]. Those “Transitional techno-
complexes” (especially the Cha
ˆtelperronian), have been interpreted as an evidence of a short
period of coexistence between local and immigrant human populations [1,11], with the early
phases of the Aurignacian complex (Proto-Aurignacian and early Aurignacian) being attrib-
uted to the first modern humans in Europe, as early as 42 ka cal BP, during GI10. In Iberia, the
end of the Mousterian has been shown to have been earlier in the North than once thought,
while the Early Upper Paleolithic in the South (Gravettian) is older than was previously
believed [12]. Thus, the hypothesis of a very early appearance of Aurignacian in northern Ibe-
ria is no longer supported [2,4].
Here, we focus on the Cantabrian region in northern Iberia, where the archaeology, stratig-
raphy and chronology of several key sites—El Castillo, Labeko Koba, La Viña, Esquilleu and
Morı
´n—have been recently reviewed [2,5,13], providing an initial framework for the Middle
to Upper Paleolithic transition. However, further research at more representative sites in this
region with Mousterian, Cha
ˆtelperronian, Aurignacian and Gravettian materials, that either
lacked radiocarbon dates or had dates obtained in the late 20th century before the develop-
ment of rigorous pre-treatment methods, is needed to securely establish the chronology by
including more archaeological sites. As part of a wider project to reconstruct the climate and
local and regional environmental conditions that late Neanderthals and early AMH faced in
the region during Marine Isotopic Stage 3 (MIS3), using stable isotopic analyses (δ
13
C, δ
15
N,
δ
18
O and δ
34
S), first we performed a complete review of the chronological data from 13
regional sites that included 28 Middle and Early Upper Paleolithic archaeological levels. Out of
51 samples that were processed for radiocarbon dating, 5 failed and the remaining 46 received
an AMS measurement using new ultrafiltration method that is more rigoruous in removing
possible bone collagen contamination, from contemporaneous sites which either lacked dates
or had previously produced problematic dates.
The new
14
C radiocarbon dates obtained in this project, in combination with other available
ultrafiltered dates from the region, have allowed the development of an independent, radio-
metric chronology of previously undated sites in the Cantabrian region, which had until now
been attributed only through stratigraphic position and/or material culture characteristics to
the Mousterian, Cha
ˆtelperronian, Aurignacian or Gravettian techno-complexes. Re-dating of
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 2 / 20
Prehisto
´ricas de Cantabria is sponsored by the
University of Cantabria, the Government of
Cantabria and Banco Santander. This paper was
mainly written during a research stay by one of us
(ABMA) at the Leverhulme Centre for Evolutionary
Studies, Department of Archaeology, University of
Cambridge funded by Spanish Ministry of
Education, Culture and Sports (Jose de Castillejo
Program, Ref no. CAS15_00054). The funders had
no role in study design, data collection and
analysis, decision to publish, or preparation of the
manuscript.
Competing interests: The authors have declared
that no competing interests exist.

sequences that had previously been dated using conventional or early AMS
14
C methods was
undertaken, producing significant changes in previous interpretations of relevant sites, some-
thing that has also been verified by reviewing the lithic technocomplexes. The results provide
greater temporal precision for the Middle to Upper Paleolithic transition in the Cantabrian
Region by building a Bayesian model using samples treated with a robust pre-treatment
methodology. The model includes new Mousterian modelled dates within the range of the
calibration curve and defines the boundaries for the start and end of each of the Early Upper
Paleolithic techno-complexes.
This research presents new possibilities for addressing the timing of the critical processes of
cultural change, local extinctions and population replacement that happened during the Mid-
dle-Upper Paleolithic transition in northern Spain and more generally in Europe. The dating
results reported here will also serve to discuss the stratigraphic integrity and cultural attribu-
tion of the sites analysed.
Material
Thirteen sites were dated as part of this project, including a total of three Middle Paleolithic
and twenty-five early Upper Paleolithic archaeological levels. These sites are located in the
modern-day regions of Asturias in the west, Cantabria in the center and the Basque Country
in the east of the Cantabrian Region (Fig 1). These archaeological levels were selected because
of their attribution to the Mousterian (n = 3), Cha
ˆtelperronian (n = 1), Aurignacian (n = 11)
and Gravettian (N = 13) techno-complexes, previously determined based on their stratigraphic
position, material culture, available dating or a combination of these factors. The Mousterian
levels dated were Amalda VII [14], Axlor IV [15] and Llonı
´n VI [16–20], while the only Cha
ˆtel-
perronian level was Ekain Xa [21]. The Aurignacian levels were Aitzbitarte (Cave III-entrance
area) Vb center [22], Ekain IXb, Cobrante V and VI [23], El Ruso Cave I IVb [24], El Otero IV,
V and VI [25], Morin 7c [26], Covalejos B (2) and C (3) [27]. Finally, the Gravettian levels
Fig 1. Location of sites in the Cantabrian region, northern Spain. 1: La Viña, 2: La Gu¨elga, 3: Llonı
´n, 4: Esquilleu, 5: El Castillo, 6: Covalejos, 7: Ruso I, 8:
Morı
´n, 9: Cobrante, 10: El Otero, 11: Miro
´n, 12: El Cuco, 13: Arrillor, 14: Axlor, 15: Bolinkoba, 16: Labeko Koba, 17: Ekain, 18: Amalda, 19: Aitzbitarte Cave III.
https://doi.org/10.1371/journal.pone.0194708.g001
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 3 / 20

were Aitzbitarte (Cave III-entrance area) IV, Va and Vb upper, Amalda V and VI, Bolinkoba
VI/F [28–29], El Cuco III and Vb [30–31], La Viña VII, VIII, IX and X [32–36] and Llonı
´n V.
Other regional sites with contemporaneous cultural attributions, but unclear stratigraphy,
insufficient archaeological information, or those that are currently still under study were not
included here. We also took into consideration the radiocarbon dates recently published for
the regional sites of La Viña, Esquilleu, La Gu¨elga, El Castillo, Morı
´n, El Miro
´n, Arrillor and
Labeko Koba [2–5,37–38] that have been achieved using the same ultrafiltration method as
this study, making them comparable and appropriate to include in the Bayesian models. We
have initially accepted the culture-stratigraphic designations for individual levels proposed by
the excavators/analysts of the various sites. This brings with it the consequence of incorporat-
ing differing classificatory criteria (including differing approaches to “lumping” versus “split-
ting” in such designations) among the many different researchers who studied the various
artifact assemblages, some of which contain more definitive temporally/culturally bounded
and thus diagnostic artifacts than others. However, the Bayesian approach applied here has the
capacity to challenge these prior attributions, prompting a reinterpretation of the lithic assem-
blages and the stratigraphy. Where mismatches were identified, sites were revisited, and if nec-
essary, attributions changed according to our reviews. In case of doubt, dates were discarded
to avoid any bias in the conclusions.
51 samples were processed for radiocarbon dating on bones with evidence of human
manipulation such as anthropogenic fractures and/or cut marks. Sample information for each
specimen, including site, archaeological level, context, sample number, animal species and
anatomical element is included in S1 Table. The location of the archaeological material in
regional museums and institutions is indicated in the description of each site in S1 File. This
research implies a remarkable increase in the number of reliable radiometric dates in the
region and period of study, which currently comprises 61 determinations [4,5,12–13] [S3
Table]. The selection of the fauna samples in museum collections was based on the following
criteria: 1) stratigraphic position of the remains at the site; 2) selection of bones preferably
directly labelled to assure their provenance within the site; 3) selection of animal bones taxo-
nomically and anatomically identifiable and 4) selection of anatomical elements with clear
anthropogenic marks.
Methods
Radiocarbon dating
Prior to radiocarbon dating, a subsample of all specimens was analysed to obtain δ
13
C and
δ
15
N values, which also established the state of collagen preservation. Of the bones previously
analysed for stable isotopic analyses, specimens yielding >1% collagen were selected for dating
to maximise the likelihood of achieving a successful radiocarbon date. All samples met the
quality assurance criteria as shown in S1 Table. Collagen extraction and analysis for radiocar-
bon dating were undertaken at the Oxford Radiocarbon Accelerator Unit (ORAU). Collagen
was obtained following the method detailed by Brock et al [39], which involves the deminerali-
sation of the mineral component (and any exogenous carbonates) of drilled bone power using
0.5M HCL at 5˚C overnight, before removal of organics and humic acid using 0.1M NaOH
solution for 30 minutes at room temperate (RT), and a final wash in 0.5M HCL for 1 hour at
RT. The collagen was gelatinised in a 0.001M HCL solution for 20 hours at 70˚C. EZEE™bio-
logical filters (45–90 μm) were used to remove smaller soluble components, before ultrafiltra-
tion using cleaned 30 kDa MWCO Vivaspin™15 ultrafilters. Combustion of the collagen using
an elemental analyser (ANCA-GSL), linked to an isotope ratio-mass spectrometer (Sercon 20–
20) produced Carbon and Nitrogen stable isotope data, and samples were dated using an
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 4 / 20

Accelerator Mass Spectrometer following conversion of excess CO
2
into graphite using an
iron catalyst [40].
Bayesian modelling
Individual Bayesian age models could be built for La Viña (S1 Fig), Covalejos (S2 Fig), El
Cuco (S3 Fig), Ekain (S4 Fig) Amalda sites (S5 Fig) and Aitzibitarte (Cave III) (S6 Fig) using
OxCal4.2 software [41] and the INTCAL13 calibration curve [42]. No chronological models
were built for the other sites, because of the limited number of dates. The Bayesian model
enables to modify the calibrated Probability Distribution Function (PDF) of individual dates
based on the existing relative stratigraphic and other relative age information. Both new ultra-
filtration dates and previous ones recently published for the period of study in northern Spain
were considered for completeness (see S2 Table). The presence of problematic determinations
that do not agree with the prior framework was considered by adopting a t-type outlier model
with an initial 5% probability for each determination to be an outlier. Likewise, a s-type outlier
model was used to test the coherence of two radiocarbon dates obtained from the same bone
remain [43]. A resolution of 20 years was assumed, being a reasonable balance between
required accuracy and computational costs, and a sensitivity test on the outlier model and
prior boundary test was conducted to ensure the robustness of the results. A discussion of each
archaeological site and cultural attribution according to the dates are discussed individually in
S1 File. CQL codes are also reported there (S1 and S2 Codes). An Order function in the OxCal
was used to calculate the probability that one PDF predated another, providing information to
assess synchronicity and temporal overlap of individual archaeological levels and cultural
phases in each of the six individual sites modelled. In all cases, convergence was greater than
95% and the model agreement index close to 100% except in the case of La Viña, where it is
still clearly above the 60% validity threshold.
Once models for individual sites were conducted, modelled dates from each industry (pos-
terior PDFs) were grouped within a single cultural phase (inserted as priors) without assuming
any order. This was achieved by placing them within a single Phase with start and end bound-
aries. Individually calibrated dates coming from sites were no individual site model could be
conducted (such as Cobrante Level VI, Llonı
´n V, Bolinkoba VI/F and Morin 4), as well as
other existing reliable modelled dates in the region (from Labeko Koba [4], El Castillo [5] and
La Viña [13]), were included. These new unordered Bayesian age models enabled determining
a regional PDF of the temporal boundaries between Mousterian, Cha
ˆtelperronian, Aurigna-
cian and Gravettian, as well as an easier comparison between sites. The advantage of this analy-
sis in comparison with individual models is that it enables further constraining the uncertainty
of the boundaries by assuming that the onset and disappearance of cultures were regional pro-
cesses rather than localised phenomena. This is reasonable given the known level of regional
interconnection during Late Pleistocene in northern Iberia. Likewise, it reduces the potential
bias at one particular site, as pooling together several sites in one region serves to increase the
reliability of the results, which can be interpreted regionally with more confidence (see S11
Figure in [3] and see Figure 8 in [5]). The difference between the PDFs of the start and end
boundaries was also calculated to estimate the likely duration of the phase. The results were
compared with the Greenland Oxygen Isotopic record (NGRIP) [44,45] as a global climatic
record to define the different cultural periods in the Cantabrian region.
All Bayesian models were run 4–5 times and results compared to check consistency. They
disclosed acceptable levels of reproducibility when compared, although key boundary parame-
ters were usually within 50–100 years of one another with repetition of the model. This is the
usual accuracy expected when using this approach, and consequently, all dates reported here
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 5 / 20

have been rounded to the nearest century. Finally, the youngest and oldest dates for each cul-
tural period were removed and Bayesian models were rerun to test the dependence of the con-
clusions on them.
Results and discussion
Out of the 51 dates processed for radiocarbon dating, 46 produced successful AMS measure-
ments as they had enough collagen to provide viable results. Four samples failed due to low
collagen yields and one due to a high C:N value. Collagen was generally well preserved and
only one sample from El Cuco yielded less than 1% collagen, but it had a C:N ratio of 3.39 was
within the acceptable range for in vivo collagen [46]. Of the 46 dates, 3 dates were beyond the
radiocarbon limit and 13 showed mismatches with their defined cultural attribution providing
a chronology younger than initially attributed either by cultural artefacts found within that
level or previous dating (S1 Table). Consequently, in this study, a substantial dataset of 30 valid
new dates was obtained and only with those dates Bayesian models were generated.
The 13 dates that show discrepancies between the cultural attributions determined by the
new dates obtained and those based on traditional analyses of the archaeological materials cor-
respond to 7 of the 13 studied sites (11 of the 28 levels). This might be caused by one or several
reasons such as excavation methods (e.g., failure to see or identify stratigraphic differences,
attributions based on very small, not very diagnostic artifact collections from limited excava-
tions or test pits) or curatorial issues with the faunal material, as several of the regional muse-
ums have been moved repeatedly to different locations over several decades. For each site,
possible reasons for those inconsistencies are discussed in S1 File.
Individual Bayesian models were created for sites where samples belonged to more than
one layer, such as La Viña (S1 Fig), Covalejos (S2 Fig), El Cuco (S3 Fig), Amalda (S5 Fig) and
Aitzbitarte III (S6 Fig). For Ekain two dates for Level IXb were also modelled (S4 Fig). CQL
codes are presented in S1 and S2 Codes. This allowed, considering the stratigraphy of the sites
as prior information for the dates, leading to more robust results. The robustness of the results
has also been verified by means of a sensitivity test (see S4 Table), which resulted in marginal
changes to the relevant boundaries between cultures.
In several archaeological levels, typological chronologies have been challenged by the new
dating evidence. Thus, in Asturias, the site of Llonı
´n Level V, attributed to the Gravettian [16–
20], yielded two very different results: one coherent with an Early Gravettian attribution (~28k
uncal BP) and another date of 20k uncal BP, which could correspond to an early Solutrean or a
very late phase of the Gravettian, younger than Morı
´n Level 4 [47] and similar to the AMS
dates of Level III from Aitzbitarte III [48]. These results suggest either a much longer forma-
tion for Level V (more than 8,000 years for only 9 cm of stratigraphy), although we cannot dis-
miss the possibility of some disturbance or admixture with overlying Solutrean Level IV which
remains undated. In the Autonomous Community of Cantabria, the new chronology of El
Otero, which was previously undated, indicates a Magdalenian chronology (~15–10 ka uncal
BP, and hereafter) instead of an Aurignacian one as traditionally proposed [25]. Despite the
presence of apparently characteristic artifacts [25,49–50], this result urges caution in the dating
of levels solely using artifacts that are not temporally diagnostic. In Level V of Cobrante, identi-
fied as Aurignacian, despite its lack of characteristic material culture [51] the obtained dates
correspond to the Solutrean instead (~18k uncal BP). The apparent absence of characteristic
Aurignacian lithics, and the presence of at least one piece with partial invasive (Solutrean)
retouch [51], support this attribution. Cobrante Level VI was interpreted as Archaic Aurigna-
cian because of the presence of characteristic lithic tools, such as Dufour bladelets, large “Auri-
gnacian” blades and carinated end-scrapers, which appeared alongside Mousterian-looking
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 6 / 20

tools [51]. New two dates show an incoherence between them: one with a date beyond the
radiocarbon limit and another with a contemporaneous regional Early Aurignacian date.
Curational or stratigraphical issues could be the reason for this incoherence as explained in S1
File. In El Cuco, the Levels III and Vb previously defined [30] both as Gravettian provided
Aurignacian (~35k uncal BP) and Mousterian (~49k uncal BP) dates, respectively. The lower
levels of this sequence (VII-XIII) have been recently reassessed through new 14C AMS dating
on shells and a technological lithic study. These new analyses confirm a Mousterian attribution
to levels previously defined as Aurignacian and an Aurignacian chronology to levels defined
as Gravettian [31]. In El Ruso, Level IVb originally defined as Evolved Aurignacian [52], pro-
vided a Gravettian date (~28k uncal BP). Although the small lithic assemblage is not very
diagnostic, the presence of a flat-nosed end-scraper and a double carinated end-scraper was
mentioned.
In Bizkaia, the Gravettian Level VI of Bolinkoba provided a contemporaneous date for this
regional period, while a second one is much younger (~10k uncal BP), attributable to the
regional Azilian, suggesting significant mixing or curational problem as no diagnostic Azilian
lithic material has been recovered or identified in Level VI assemblage [53]. In Amalda (Gipuz-
koa), three dates provided younger dates than expected [54]. One sample from Mousterian
Level VII provided a date within a Gravettian time range (~28k uncal BP), possibly reflecting a
limited admixture between Levels VI and VII [55]. Another sample from the Gravettian Level
VI gave a medieval date. Its location close to the cave entrance, where the upper levels were
exposed, points towards the possibility that materials from historic times were inserted into
Last Glacial sediments. A further sample from the Gravettian Level V provided a Magdalenian
age (~14k uncal BP), maybe deriving from unknown problems during excavation or curation.
In Aitzbitarte cave III Level Vb (center) yielded a single date that is older than the normative
attribution (likely Early Aurignacian rather than Evolved Aurignacian) [56], evidencing a pos-
sible presence of an Early Aurignacian at the base of the level. In Ekain (Gipuzkoa), Level Xa,
undated, was interpreted as a Cha
ˆtelperronian hunting camp, with a small lithic collection,
including a single typical Cha
ˆtelperronian point, and three other backed blades and bladelets
[57]. The new date for Level Xa is 34 ka uncal BP, which is far too young for the regional Cha
ˆ-
telperronian, dated at 37-38k uncal BP in nearby Labeko Koba [4]. The location of the bone
sampled at the site and the significant presence of cave bears do not rule out the possibility of
admixture caused either by those carnivores or by other post-depositional processes not identi-
fied during the excavation of Ekain.
These discordances are particularly relevant for sites profusely used in the past to investi-
gate the cultural adaptations during the Cantabrian Upper Paleolithic and reflect the complexi-
ties of attributing archaeological levels based solely on lithic typology or technology. It also
reveals the problems caused by the attributions based on single dates without taking into
account the characteristics of the archaeological assemblage.
The regional chronological framework for each cultural period as obtained from the Bayes-
ian age model is presented in Figs 2–4. No regional model for the Cha
ˆtelperronian is included
as only ultrafiltered dates are available for Level IX lower of Labeko Koba and this site has been
modelled elsewhere (see Figure S20 in [3]). Regarding the chronology of the Late Mousterian
in the Cantabrian region, the dates from Axlor go beyond the radiocarbon limit and samples
from Llonı
´n Level VI failed. However, two new dates, both from Level VII in Amalda, add
important new evidence to the existing record. The updated Bayesian model for the Upper to
Middle Paleolithic transition shows that the end boundary PDF for the Mousterian in the
region is 47.9–45.1ka cal BP (all probability ranges are expressed at 95,4% hereafter), confirm-
ing that it occurred earlier in the Atlantic zone than in the northeastern Iberia and in western
and northern Europe [3]. The apparent end of the Mousterian came immediately before and
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 7 / 20

during GI12 (Fig 2). No Cha
ˆtelperronian dates were obtained in this project, despite Level Xa
of Ekain having originally been defined as Cha
ˆtelperronian based on lithic typology. However,
the date obtained from Ekain was too young for the regional range of the Cha
ˆtelperronian,
which is found in the Cantabrian Region in Morı
´n and Labeko Koba, but is only reliably dated
in the latter at 42.6–41.4ka cal BP (see SI pp.47 in [3]).
The earlier disappearance of those Mousterian groups in the Cantabrian region (northern
Atlantic Iberia), while they still survived in Catalonia (north-eastern Mediterranean Iberia)
for a few more millennia until just before 42 cal BP [2,58], as dated in Romani and L‘Arbreda,
might have been caused by as yet unknown factors and requires further research.
The age model data reveals that there was an interval of 2,700 to 5,800k (95.4% probability),
with a median of 4,400 years between the end of the Mousterian and the start of the Cha
ˆtelper-
ronian in the Cantabrian Region (Table 1). The Cha
ˆtelperronian appears to start several
millennia after the Mousterian completely disappeared in the region, while in France this “tran-
sitional” technocomplex appears before the end of the Mousterian [2]. If Neanderthals were
responsible for both Mousterian and Cha
ˆtelperronian technocomplexes in the Cantabrian
Fig 2. Radiocarbon dates for the uppermost dates of the Mousterian assemblages from the Cantabrian region (Asturias, Cantabria and
the Basque Country) calibrated against IntCal13 [42] in OxCal v.4.2 [41] assuming each sample has a 5% prior probability of being and
outlier within the general t-type outlier model [43]. All dates have been obtained using the ultrafiltration protocol [40]. References are
given in S1 Table. A
model
= 99.8. denotes previously unmodelled dates introduced as R-dates while the others are modelled dates at
individual sites introduced as Prior PDFs.
https://doi.org/10.1371/journal.pone.0194708.g002
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
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Fig 3. Radiocarbon dates for the Aurignacian assemblages from the Cantabrian region (Asturias, Cantabria and the
Basque Country) calibrated against IntCal13 [42] in OxCal v.4.2 [41] assuming each sample has a 5% prior
probability of being and outlier within the general t-type outlier model [43]. All dates have been obtained using the
ultrafiltration protocol [40]. References are given in S1 Table. A
model
= 84.2. denotes previously unmodelled dates
introduced as R-dates while the others are modelled dates at individual sites introduced as Prior PDFs.
https://doi.org/10.1371/journal.pone.0194708.g003
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 9 / 20

Fig 4. Radiocarbon dates for the Gravettian assemblages from the Cantabrian region (Asturias, Cantabria and the BasqueCountry) calibrated
against IntCal13 [42] in OxCal v.4.2 [41] assuming each sample has a 5% prior probability of being and outlier within the general t-type outlier
model [43]. All dates have been obtained using the ultrafiltration protocol [40]. References are given in S1 Table. A
model
= 104.4. denotes previously
unmodelled dates introduced as R-dates while the others are modelled dates at individual sites introduced as Prior PDFs.
https://doi.org/10.1371/journal.pone.0194708.g004
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 10 / 20

region, this would suggest a Cha
ˆtelperronian intrusion from southwestern France to the eastern
(in Labeko Koba) and central (in Morı
´n) sectors of Cantabrian Spain, after Mousterian popula-
tions had already disappeared. This could be due to pressure from expanding populations of
modern humans, but any hypothesis of this sort requires further exploration.
The Bayesian modelled results suggest that the end boundary for the Cha
ˆtelperronian was
42.4–41.4ka cal BP (S1 Table). According to the dating results, the Cha
ˆtelperronian phase was
relatively short (with the caveat that only one level is dated by ultrafiltration within the whole
region) and partially overlaps with the start of the Aurignacian. Cha
ˆtelperronian dates range
between 42.8 and 41.4ka cal BP which coincides in time with its final boundary due to the
short duration. The interval between the end of the Cha
ˆtelperronian and the start of the Auri-
gnacian is 1,400 years (Table 1). If Neanderthals were responsible for the Cha
ˆtelperronian
and AMH for the Aurignacian, the implication is that there was a short duration of overlap
between the Cha
ˆtelperronian and Aurignacian, indicating a brief period of coexistence
between both human species with a quick replacement of the Neanderthals in this region.
However, there is a lack of diagnostic human remains in the region in association with any of
these techno-complexes and “authorship” of these will only be fully demonstrated with the dis-
covery of skeletal evidence.
The start boundary for the Aurignacian techno-complex in the region falls between 43.3–
40.5ka cal BP and the end at 34.6–33.1ka cal BP (95.4% probability) (Fig 3 and S2 Table). This
chronology is consistent with Zilhao’s suggestion [59] that the occurrence of the Aurignacian
in northern Iberia was before GI10, around c.42ka cal BP. The Proto-Aurignacian at El Castillo
appears during GS11, which is earlier than in Labeko Koba, although the OxA-22200 date in
Level 16 of 38,600 ±1,000 is found to have a 15% likelihood of being an outlier. Cobrante,
which contains diagnostic lithic elements corresponding to a Proto-Aurignacian technocom-
plex, is situated between the Proto-Aurignacian dates of Labeko Koba Level VII. The high-
precision chronometric dates show a distinction between Proto and Early Aurignacian
Table 1. Results of the 68% and 95% PDF range of the boundaries, duration of technocomplexes and temporal lapse between archaeological phases.
Modelled ranged (cal BP)
(68.2% prob.) (95.4% prob.)
From To From To
Boundaries
End Mousterian 47,298 46,048 47,914 45,078
Start Cha
ˆtelperronian 42,508 41,930 42,868 41,686
End Cha
ˆtelperronian 42,142 41,632 42,406 41,370
Start Aurignacian 42,406 41,000 43,270 40,478
End Aurignacian 34,376 33,784 34,604 33,140
Start Gravettian 35,914 35,206 36,818 35,030
Duration of industry
Cha
ˆtelperronian 0 720 0 1,160
Aurignacian 7,152 8,788 6,500 9,840
Time between industries Median
End Mousterian/Start Cha
ˆtelperronian: 3,704 5,100 2,662 5,752 4,354
Start Aurignacian / Start Cha
ˆtelperronian: -482 1,122 -1,404 1,768 274
End Cha
ˆtelperronian/Start Aurignacian: -798 740 -1,750 1,400 -90
End Aurignacian/Start Gravettian: -2,172 -1,080 -3,258 -756 -1,702
End Mousterian/End Cha
ˆtelperronian: 4,050 5,436 3,028 6,116 4,714
End Mousterian/ Start Aurignacian: 3,674 5,646 2,340 6,516 4,588
https://doi.org/10.1371/journal.pone.0194708.t001
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
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assemblages and Evolved Aurignacian ones in this region. The exception to this is El Castillo,
where the Proto and Early Aurignacian occurred during GI10 and GI9, and before H4. After
the Proto-Aurignacian, the Early Aurignacian appears to spread rapidly after GI9 through
GI8. In Covalejos, a quick replacement between Proto (Level C/3) and Early Aurignacian
(Level B/2) is also apparent. The most recent phase of the Aurignacian techno-complex, the
Evolved Aurignacian, occurred in the region during or immediately after GI8, starting first in
the east at the sites of Aitzbitarte III and Ekain and spreading west as far as La Viña (Fig 3).
Despite the proposal that the combination of Heinrich Event 4 with the Campanian Ignimbrite
eruption (CI) and the Bond cooling trend might have destabilised the ecological niches and
the distribution of biotic resources during MIS 3, acting as a possible triggering factor for the
demise of the Neanderthals [60–62], this might not be true for the Cantabrian region, as the
Neanderthals had apparently already disappeared some time earlier. However, those climatic
oscillations may have affected the movement of modern humans from eastern and central
Europe through southern France and into northern Iberia, as they expanded into new,
resource-rich territories such as the Cantabrian and Catalonian regions, where Neanderthal
populations may already have been either sparse or non-existent.
By comparing the start and end boundary PDFs for both Gravettian and Aurignacian, the
Gravettian appears to have started before the end of the Aurignacian around 36.8-35ka cal BP,
during GI7, immediately after the first Late Aurignacian assemblages appeared in the region
(Table 1,S1 and S2 Tables). The interval between the end of Aurignacian and the start of the
Gravettian ranges from -3300 to -800 years, might indicate a long overlap between the two
techno-complexes. By looking at the spatio-temporal distribution of the Gravettian in the
region, the earliest occurrences appeared in the Basque Country at Aitzbitarte III, which might
indicate, first, an early arrival of Gravettian artifacts from western Pyrenean France into
Vasco-Cantabria or a local origin within the eastermost part of the region (including Bizkaia,
Gipuzkoa and French Basque country) and, second, a dispersal of the technocomplex from
east to west. In fact, the earliest Gravettian dates are in Aitzbitarte III at the eastern end of the
Basque province of Gipuzkoa (35.6–34.8ka cal BP), whilst a much later start is seen in the west-
ernmost site, La Viña, in Asturias (33.7–32.4ka cal BP) (Fig 4). These Gravettian dates would
indicate the oldest directly dated evidence of this technocomplex in Western Europe.
The conclusions given above are not significantly altered when the oldest and youngest
dates are removed from each cultural phase (see S5 Table), apart from the estimated overlap
between the Cha
ˆtelperronian and the Aurignacian. The start of the Aurignacian is dependent
on the validity of the date obtained from Level 16 of El Castillo. Without that date, the Auri-
gnacian would be pushed forward around 1,200 years, reducing drastically the probabilities of
a coexistence of both cultures in the region. The cultural attribution of that level to Proto-Auri-
gnacian is clear [63] and the date was obtained with ultrafiltration methodology with no prob-
lems arising from its analysis [5]. However, more dates would be desirable to confirm the
potential overlap between the Cha
ˆtelperronian and the Aurignacian in the region.
Conclusion
The new radiocarbon dates and the subsequently derived Bayesian models that include both
new and previously run high-quality dates, provide high-precision chronological resolution
for reconstructing the spatio-temporal evolution of the Middle to Upper Palaeolithic transition
in the Cantabrian Region. This research has generated a substantial dataset of 30 valid new
dates, adding to the pre-existing 61 dates achieved using the ultrafiltration protocol and
adopted as truthful. A total of 91 high-quality radiocarbon dates (S3 Table) for the regional
Mousterian, Cha
ˆtelperronian, Aurignacian and Gravettian periods are now available (of the
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
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128 attempted), enabling the construction of a much more precise chronological framework
and spatio-temporal understanding of the transition and subsequent development of early
Upper Paleolithic cultures in northern Iberia (Fig 5).
Detailed assessment of the sites that had previously been attributed until now to the Middle
to Upper Paleolithic transition has found that not all of these can continue to be considered as
belonging to this period. In addition, the dates show that for some of the sites, further work
(including the acquisition of larger collections through future and controlled excavation) is
required to review the industries and sedimentological units in order to arrive at definitive
cultural attributions. Curatorial work may also be required to solve apparent problems of pro-
venience among certain collections. Although this might challenge previous interpretations
such as those concerning subsistence strategies during this period of bio-cultural transition in
Northern Spain [64], it will contribute in the long term to a better understanding of this key
era in a very important region for the study of the European Paleolithic.
The Bayesian model for the Mousterian in the Cantabrian Region shows that the dates
obtained in this project are consistent with other, previously dated late Mousterian assem-
blages in Esquilleu, La Gu¨elga, Morı
´n, El Miro
´n and Arrillor [2,3,5,38] (S3 Table). The results
allow us to confirm that the end of the Mousterian occurred between ~48-45ka cal BP (at
95.4% probability). This analysis highlights the earlier disappearance of the Mousterian in
north-central Iberia in comparison with sites such as Romani and L’Arbreda in north-eastern
Iberia or Pech de l’Aze
´in south-western France [3]. No new dates were obtained for the Cha
ˆ-
telperronian; however, the Bayesian model confirms a brief overlap between the Cha
ˆtelperro-
nian and the Aurignacian in the Cantabrian region (despite the fact that this conclusion is
highly dependent on a single date from the Proto-Aurignacian Level 16 of El Castillo). With
these data, it is difficult to discuss the various hypothesis that have been proposed for the ori-
gins of Cha
ˆtelperronian technocomplex (acculturation, autonomous development, stimulus
diffusion), but at the regional scale an apparent gap between the late Mousterian and the Cha
ˆ-
telperronian supports the absence of a local development and the potentially intrusive nature
of the Cha
ˆtelperronian. Alternatively, the presently available archaeological record could sim-
ply be missing sites dating to the intervening period of time, as yet undiscovered. The Aurigna-
cian appears at ~43 ka cal BP, overlapping with the Cha
ˆtelperronian at least within the error
ranges of the few available dates. The Bayesian model for the Aurignacian shows two clusters
of dates: ones falling between GI10 and GI8 and corresponding to the Proto and Early Auri-
gnacian with an overlap, and a second group of dates, immediately before GI7 and extending
until GS7, which correspond to the Evolved Aurignacian. The nature and causes of the spread
of Aurignacian technologies and presumably modern humans remain critical subjects for
ongoing paleoenvironmental and archaeological research.
The appearance of the Gravettian techno-complex was a relatively localized-process in the
region and the dates obtained here increase our knowledge about its spatio-temporal develop-
ment. In Aitzbitarte III a relatively quick cultural replacement of the Aurignacian by the
Gravettian with Noailles burins is seen. This reinforces the hypothesis of a local origin for the
Noaillian facies of the techno-complex so deeply rooted and long-lasting in the Basque Coun-
try [49]. The older Gravettian dates appear during GI7 in Aitzbitarte III, with more recent
ones found further to the West in Asturias at Llonı
´n and La Viña during GI6 and GI5, imply-
ing an East-West penetration of this culture into the region.
Despite the new evidence obtained here, establishing the end of the Mousterian, the time
span of the Cha
ˆtelperronian and the start of the Aurignacian in the Cantabrian region would
still benefit from more radiocarbon dates in order to resolve still existing uncertainty. How-
ever, this possibility is dependent on the availability and high-quality excavation of new sites
with the required degree of preservation to ensure the presence of collagen. However, while
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 13 / 20

Fig 5. A spatio-temporal comparison of the late Mousterian, Cha
ˆtelperronian, Aurignacian and Gravettian
assemblages from the Cantabrian region (Asturias, Cantabria and the Basque Country).
https://doi.org/10.1371/journal.pone.0194708.g005
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 14 / 20

awaiting the appearance of new sites, the reliability of the potential overlap between the Cha
ˆtel-
perronian and the Aurignacian could be increased by further sampling in the key levels 16 of
El Castillo and 10 of Cueva Morin in the center of the Autonomous Community of Cantabria.
Supporting information
S1 File. Supporting information manuscript with a detailed description of each archaeo-
logical site sampled in this study.
(DOCX)
S1 Table. Radiocarbon AMS dates produced in this study. Collagen was extracted using the
ultrafiltration protocol in all the samples. A contextual information of each archaeological
level is provided, including a description of the lithic and bone artefacts and the archaeological
context. Also, sample reference, animal species and skeletal element sampled including its
taphonomic alterations is specified. For a reliable date, % yield should be >1%; %C >30% and
C:N between 2.9 and 3.4 [65]. References to the original studies are cited and included below.
(DOCX)
S2 Table. Results of the Order function comparing the PDF’s of the boundaries dating the
start and the end of the archaeological industries from the Cantabrian region. Cells con-
taining probabilities of >95% are coloured in green, 68–94% in orange and <68 in grey.
(DOCX)
S3 Table. Radiocarbon accelerator dates from the Cantabrian region mentioned in this
work. Only bone samples with ultrafiltration methods are included. ABA: charcoal fragment
treated with a series of acid and base washes; ABOx-SC: charcoal treated with acid and base
washes, followed by an oxidation stage and pre-combustion; UF AMS: collagen extracted
using the ultrafiltration protocol.
(DOCX)
S4 Table. Results of sensitivity test conducted on individual models.
(DOCX)
S5 Table. Results of sensitivity test conducted on regional models.
(DOCX)
S1 Fig. Radiocarbon dates from La Viña modelled in OxCal4.2 [41,43] against INTCAL13
[42].
(TIF)
S2 Fig. Radiocarbon dates from Covalejos modelled in OxCal4.2 [41,43] against
INTCAL13 [42].
(TIF)
S3 Fig. Radiocarbon dates from El Cuco modelled in OxCal4.2 [41,43] against INTCAL13
[42].
(TIF)
S4 Fig. Radiocarbon dates from Ekain modelled in OxCal4.2 [41,43] against INTCAL13 [42].
(TIF)
S5 Fig. Radiocarbon dates from Amalda modelled in OxCal4.2 [41,43] against INTCAL13
[42].
(TIF)
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 15 / 20

S6 Fig. Radiocarbon dates from Aitzbitarte III modelled in OxCal4.2 [41,43] against
INTCAL13 [42].
(TIF)
S1 Code. CQL individual codes.
(DOCX)
S2 Code. CQL regional codes.
(DOCX)
Acknowledgments
This research has been supported by the European Commission through FP7-PEOPLE-2012-
CIG (Ref: 322112), the Spanish Ministry of Economy and Competitiveness (HAR2012-33956
and RYC-2011-00695), Cantabria Campus International and University of Cantabria to
ABMA. The Instituto Internacional de Investigaciones Prehisto
´ricas de Cantabria is sponsored
by the University of Cantabria, the Government of Cantabria and Banco Santander. The
authors want to acknowledge the Museo de Prehistoria y Arqueologı
´a de Cantabria, Museo
Arqueolo
´gico de Bizkaia (specially to D. Garate) and the Centro de Patrimonio Cultural del
Departamento de Cultura del Gobierno Vasco for the facilities provided during the sampling
and studying material. They warmly appreciate the significant help of archaeologist P. Rasines,
R. Montes and E. Muñoz during sample selection. This paper was mainly written during a
research stay by one of us (ABMA) at the Leverhulme Centre for Evolutionary Studies, Depart-
ment of Archaeology, University of Cambridge funded by Spanish Ministry of Education,
Culture and Sports (Jose de Castillejo Program, Ref no. CAS15_00054). ABMA and DO are
grateful to Prof. Robert Foley and Prof. Marta Mirazo
´n-Lahr for their institutional support.
Author Contributions
Conceptualization: Ana B. Marı
´n-Arroyo.
Data curation: Ana B. Marı
´n-Arroyo.
Formal analysis: Ana B. Marı
´n-Arroyo, Joseba Rios-Garaizar, David Ocio.
Funding acquisition: Ana B. Marı
´n-Arroyo.
Investigation: Ana B. Marı
´n-Arroyo, Joseba Rios-Garaizar, Jennifer R. Jones.
Methodology: Ana B. Marı
´n-Arroyo.
Project administration: Ana B. Marı
´n-Arroyo, Jennifer R. Jones.
Resources: Ana B. Marı
´n-Arroyo, Marco de la Rasilla, Manuel R. Gonza
´lez Morales, Michael
Richards, Jesu
´s Altuna, Koro Mariezkurrena.
Software: Ana B. Marı
´n-Arroyo, David Ocio.
Supervision: Ana B. Marı
´n-Arroyo.
Validation: Ana B. Marı
´n-Arroyo, Lawrence G. Straus, David Ocio.
Visualization: Ana B. Marı
´n-Arroyo, Joseba Rios-Garaizar, David Ocio.
Writing – original draft: Ana B. Marı
´n-Arroyo, Joseba Rios-Garaizar, Lawrence G. Straus,
Jennifer R. Jones, David Ocio.
Chronological reassessment of the Middle to Upper Paleolithic transition in Cantabrian Spain
PLOS ONE | https://doi.org/10.1371/journal.pone.0194708 April 18, 2018 16 / 20

Writing – review & editing: Ana B. Marı
´n-Arroyo, Joseba Rios-Garaizar, Lawrence G. Straus,
Jennifer R. Jones, Marco de la Rasilla, Manuel R. Gonza
´lez Morales, Michael Richards,
Jesu
´s Altuna, Koro Mariezkurrena, David Ocio.
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