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LETTER doi:10.1038/nature13621
The timing and spatiotemporal patterning of
Neanderthal disappearance
Tom Higham
1
, Katerina Douka
1
, Rachel Wood
1,2
, Christopher Bronk Ramsey
1
, Fiona Brock
1
, Laura Basell
3
, Marta Camps
4
,
Alvaro Arrizabalaga
5
, Javier Baena
6
, Cecillio Barroso-Ruı
´z
7
, Christopher Bergman
8
, Coralie Boitard
9
, Paolo Boscato
10
,
Miguel Caparro
´s
11
, Nicholas J. Conard
12,13
, Christelle Draily
14
, Alain Froment
15
, Bertila Galva
´n
16
, Paolo Gambassini
10
,
Alejandro Garcia-Moreno
17,37
, Stefano Grimaldi
18
, Paul Haesaerts
19
, Brigitte Holt
20
, Maria-Jose Iriarte-Chiapusso
5
,
Arthur Jelinek
21
, Jesu
´s F. Jorda
´Pardo
22
, Jose
´-Manuel Maı
´llo-Ferna
´ndez
22
, Anat Marom
1,23
, Julia
`Maroto
24
, Mario Mene
´ndez
22
,
Laure Metz
25
, Euge
`ne Morin
26
, Adriana Moroni
10
, Fabio Negrino
27
, Eleni Panagopoulou
28
, Marco Peresani
29
, Ste
´phane Pirson
30
,
Marco de la Rasilla
31
, Julien Riel-Salvatore
32
, Annamaria Ronchitelli
10
, David Santamaria
31
, Patrick Semal
33
,
Ludovic Slimak
25
, Joaquim Soler
24
, Narcı
´s Soler
24
, Aritza Villaluenga
17
, Ron Pinhasi
34
& Roger Jacobi
35,36
{
The timing of Neanderthal disappearance and the extent to which they
overlapped with the earliest incoming anatomically modern humans
(AMHs) in Eurasia are key questions in palaeoanthropology
1,2
. Deter-
mining the spatiotemporal relationship between the two populations
is crucial if we are to understand the processes, timing and reasons
leading to the disappearance of Neanderthals and the likelihood of
cultural and genetic exchange. Serious technical challenges, however,
have hindered reliable dating of the period, as the radiocarbon method
reaches its limit at 50,000 years ago
3
. Here we apply improved accel-
erator mass spectrometry
14
C techniques to construct robust chro-
nologies from 40 key Mousterian and Neanderthal archaeological
sites, ranging from Russia to Spain. Bayesian agemodelling was used
to generateprobability distribution functions to determine the latest
appearance date. We show that the Mousterian ended by 41,030–39,260
calibrated years BP (at 95.4% probability) across Europe. We also dem-
onstrate that succeeding ‘transitional’ archaeological industries, one
of which has been linked with Neanderthals(Cha
ˆtelperronian)
4
, end
at a similar time. Our data indicate that the disappearance of Nean-
derthals occurred at differenttimes in different regions. Comparing
the data with results obtained from the earliest dated AMH sites in
Europe, associated with the Uluzzian technocomplex
5
, allows us to
quantify the temporal overlap between the two human groups. The
results reveal a significant overlap of 2,600–5,400 years (at 95.4% prob-
ability). This has important implications for models seeking to explain
the cultural, technological and biological elements involved in the
replacement of Neanderthals by AMHs. A mosaic of populations in
Europe during the Middle to Upper Palaeolithic transition suggests
that there was ample time for the transmission of cultural and sym-
bolic behaviours, as well as possible genetic exchanges, between the
two groups.
European Palaeolithic sites contain the best evidence for thereplace-
ment of one human group (Neanderthals) by another (AMHs)
1
. The
nature and process of the replacement, both in cultural and genetic terms,
has been the focus of extensive research
1,6,7
. Recent studies of complete
Neanderthal and modern human genomic sequences suggest that Nean-
derthals and AMHs interbred outside Africa
7
. This resulted in an intro-
gression of 1.5–2.1% of Neanderthal-derived DNA
8
, or perhaps more
9
,
in all modern non-African human populations. The analysis of three
Neanderthal mitochondrial DNA (mtDNA) genomes from Denisova
(Russian Altai), Vindija (Croatia) and Mezmaiskaya (Russian North Cau-
casus) indicates that the greatest amount of gene flow into non-African
AMHs occurred after these Neanderthal populations had separated from
each other
8
. At present it is not clear whether interbreeding occurred once
or several times outside Africa
10
, or where it happened. After the inter-
breeding episode(s), Neanderthals and their distinctive material cul-
ture disappeared and were replaced across Eurasia by AMHs, but the
precise timing of this has remaineddifficult to identify in the absence of
a reliable chronological framework
3
.
Recent research has shownthat radiocarbon ages haveusually under-
estimated the true age of Palaeolithic remains, sometimes by several
millennia
3
. This is due largely to problems in removing young carbon
contamination from old organic samples at the limit of the
14
C method.
The application of more rigorous chemical protocols
11–13
has recently
resulted in improved reliability and accuracy. Several determinations
{Deceased.
1
Oxford Radiocarbon Accelerator Unit, Research Laboratory for Archaeology & the History of Art, University of Oxford, Oxford OX1 3QY, UK.
2
Research School for Earth Sciences, Australian National
University, Canberra 0200, Australia.
3
School of Geography, Archaeology and Palaeoecology (GAP), Queen’s University Belfast, Belfast BT7 1NN, UK.
4
School of Languages, Literatures and Cultures, College
Park, 4102 Jime
´nez Hall, University of Maryland, Maryland 20742-4821, USA.
5
Research Team on Prehistory (IT-622-13), IKERBASQUE, University of the Basque Country (UPV-EHU), Toma
´s y Valiente
Street, 01006 Vitoria-Gasteiz, Spain.
6
Departimento Prehistoria y Arqueologı
´a, Universidad Auto
´noma de Madrid, Campus Cantoblanco, 28049 Madrid, Spain.
7
Fundacio
´n Instituto de Investigacio
´nde
Prehistoria y Evolucio
´n Humana, Plaza del Coso 1, 14900 Lucena, Co
´rdoba, Spain.
8
URS, 525 Vine Street, Suite 1800, Cincinnati, Ohio 45202, USA.
9
8 rue des Sapins, 67100 Strasbourg, France.
10
Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, U.R. Preistoria e Antropologia, Universita
`degli Studi di Siena, Via Laterina 8, 53100 Siena, Italy.
11
De
´partement de Pre
´histoire, Muse
´um
National d’Histoire Naturelle, 75013 Parı
´s, France.
12
Abt. A
¨ltere Urgeschichte und Quarta
¨ro
¨kologie, Universita
¨tTu
¨bingen, Schloss Hohentu
¨bingen, 72070 Tu
¨bingen, Germany.
13
Tu
¨bingen Senckenberg
Center for Human Evolution and Paleoecology, Schloss Hohentu
¨bingen, 72070 Tu
¨bingen, Germany.
14
Service public de Wallonie, DGO4, Service de l9Arche
´ologie, rue des Martyrs, 22, B-6700 Arlon,
Belgium.
15
Laboratoire d’E
´co-antropologie et Ethnobiologie, Muse
´e de l’Homme, 17 place du Trocade
´ro, 75116 Paris, France.
16
Departamento de Prehistoria, Arqueologı
´a, Antropologı
´a e Historia Antigua,
Universidad de La Laguna, Campus de Guajara, 38071 Tenerife, Spain.
17
Monrepos Archaeological Research Centre and Museum for Human Behavioural Evolution, Schloss Monrepos, D-56567 Neuwied,
Germany.
18
Laboratorio di Preistoria ‘B. Bagolini’, Dipartimento di Lettere e Filosofia, Universita
`degli Studi di Trento, via Tommaso Gar, 14 I-38122 Trento, Italy.
19
Institut Royal des Sciences Naturelles de
Belgique, rue Vautier 29, B-1000 Brussels, Belgium.
20
Department of Anthropology, University of Massachusetts, 103 Machmer Hall, Amherst, Massachusetts 01003, USA.
21
School of Anthropology, Emil
W. Haury Building, University of Arizona, Tucson, Arizona 85721-0030, USA.
22
Departamento de Prehistoria y Arqueologı
´a, UNED. Paseo Senda del Rey 7, 20840, Madrid, Spain.
23
The Kimmel Center for
Archaeological Science, Weizmann Institute of Science, Rehovot 76100, Israel.
24
A
`rea de Prehisto
`ria, Universitat de Girona, pl. Ferrater Mora 1, 17071 Girona, Spain.
25
CNRS, UMR 5608, TRACES, Toulouse
Jean Jaure
`s University, Maison de la Recherche, 5 Alle
´es Antonio Machado, 31058 Toulouse, Cedex 9, France.
26
Department of Anthropology, Trent University, Life and Health Sciences Building Block C,
2140 East Bank Drive, Peterborough, Ontario K9J 7B8, Canada.
27
Dipartimento di Antichita
`, Filosofia e Storia, Universita
`di Genova, Via Balbi 2, Genova I-16126, Italy.
28
Ephoreia of Paleoanthropology of
Southern Greece, Ardittou 34B, Athens 11636, Greece.
29
Universita
`di Ferrara, Dipartimento di Studi Umanistici, Sezione di Scienze Preistoriche e Antropologiche, Corso Ercole I d’Este 32, I-44100 Ferrara,
Italy.
30
Service public de Wallonie, DGO4, Direction de l9Arche
´ologie, rue des Brigades d9Irlande, 1, B-5100 Jambes, Belgium.
31
Departamento de Historia, Universidad de Oviedo, c/Teniente Alfonso
Martı
´nez, s/n, 33011 Oviedo, Spain.
32
De
´partement d’Anthropologie, Universite
´de Montre
´al, C. P. 6128, Succursale Centre-ville, Montre
´al, Quebec H3T 1N8, Canada.
33
Service of Scientific Heritage, Royal
Belgian Institute of Natural Sciences, 1000 Brussels, Belgium.
34
UCD Earth Institute and School of Archaeology, University CollegeDublin, Belfield, Dublin 4, Ireland.
35
Department of Prehistory and Europe,
Franks House, The British Museum, London N1 5QJ, UK.
36
The Natural History Museum, Cromwell Road, London SW7 5BD, UK.
37
The Cantabria International Institute for Prehistoric Research (IIIPC),
University of Cantabria, Avda. Los Castros, s/n. 39005 Santander, Spain.
306 | NATURE | VOL 512 | 21 AUGUST 2014
Macmillan Publishers Limited. All rights reserved
©2014
that had previously supported late Neanderthal survival have been shown
to be marked underestimates (for example, Vindija
14
, Zafarraya
15
and
Mezmaiskaya
16
) and should be set to one side.
We performed extensive accelerator mass spectrometry (AMS) dat-
ing of critical late or final Mousterian archaeological horizons from 40
sites across Europe and the Mediterranean rim to explore the timing of
Neanderthal extinction(Fig. 1a and Supplementary Methods). We also
dated succeeding ‘transitional’ contexts, containing stone tool indus-
tries associated either with AMHs or with Neanderthals. These include
Uluzzian (distributed across peninsular Italy and southern Greece and
attributed to AMHs on the basis of associated AMH deciduous teeth
excavated in Cavallo Cave
5
) and Cha
ˆtelperronian (France and Canta-
brian Spain) layers, currently linked with Neanderthals on the basis of
skeletal and technological evidence, although the association is debated
17,18
.
Other transitional industries, such as the Szeletian and Bohunician of
central and eastern Europe have not been dated as part of this study,
nor have sites outside Europe, suchas in the far northern Arctic fringes
of Eurasia, where late Mousterian industries have been reported
19
.
We obtained 196 AMS radiocarbon measurements and used them to
build high-precision age models using Bayesian statisticson the OxCal
20
platform. This allows us to incorporate stratigraphic and other relative
age information, along with the calibrated likelihoods for each site. Prob-
ability distribution functions (PDFs) corresponding with the temporal
boundaries of the latest Mousterian occupations weregenerated (Fig. 1b
and Supplementary Methods).
The results show that the Mousterian end boundary PDFs all fall before
40,000 calibrated years (cal) BP (all probability ranges are expressed at
95.4%) (Fig. 1b). When placed into a single phase Bayesian model, the
PDFs result in an overall end boundary ranging from 41,030–39,260
cal BP (Fig. 1c and Supplementary Methods). This PDF represents the
age of the latest European Mousterian on the basis of our data.
The combined data suggest that the Mousterian ended at a very sim-
ilar time, across sites ranging from the Black Sea and the Near East, to
the Atlanticcoast (Fig. 1a, b). Southern Iberia has been held to represent
an exception to a wider European pattern
21
,withlatesurvivalofNean-
derthals previously argued at sites such as Gorham’s Cave, Gibraltar
22
.
We could not reproduce any of the late dates from sites in this region
15
(Supplementary Methods)and it is apparent that many previous deter-
minations underestimate the real age. It is unclear how long Neander-
thals persisted in southern Iberia
15
. More dating evidence is required
before we can determine whether Neanderthal presence was later here
than elsewhere in Europe.
Our data also reveal differences in the spatiotemporal distribution of
the latest Mousterian sites (Fig. 1b). The PDFs obtained were statistically
ordered and the results show that significant differences exist between
several late Mousterian contexts in different regions of Europe (Sup-
plementaryMethods). This may be attributed to the emergence of ‘tran-
sitional’ industries that replace the Mousterian between ,45,000–41,000
cal BP in some, but not all regions. At Fumane in Italy, for example, the
Mousterian is replaced by the Uluzzian at 44,800–43,950cal BP, while
39. Ksar Akil
40. Mezmaiskaya
38. Lakonis I
33. Geissenklösterle
27. Pin Hole
26. Hyaena Den
34. Fumane
32. Bombrini
25. Arcy-sur-Cure
22. La Quina
24. Les Cottés
19. Le Moustier
16. Romani
17. L'Arbreda
40,000
45,000
50,000
Modelled date (cal BP)
a
b
35. Castelcivita
Southern and
eastern Europe
8–15. NW Spain
Iberia
End of Mousterian
18. Pech de l'Azé
31. Mandrin
28. Spy
Western and northern Europe
23. St Césaire
250 km
Scale
12
3
4
5
8–15
7
616 17 18–21
23
24
28
27
26
25
32
31
30
29
33
34
35
36 37
40
38 39
22 0.001
0.0005
0
Probability density
c
42,000 41,000 40,000 39,000
Modelled date (cal BP)
End of Mousterian
68.2% probability
40,800 (68.2%) 40,000 BP
95.4% probability
41,030 (95.4%) 39,260 BP
Figure 1
|
Site locations and final boundary age
ranges for Mousterian and Neanderthal sites
a, Location of the 40 sites analysed and discussedin
this paper. 1: Gorham’s Cave; 2: Zafarraya; 3: El
Nin
˜o; 4: Sima de las Palomas; 5: El Salt; 6:
Quebrada; 7: Jarama VI; 8–15: La Vin
˜a, El Sidro
´n,
La Gu
¨elga, Esquilleu, Morı
´n, Arrillor, Labeko
Koba, Lezetxiki; 16: Abric Romanı
´; 17: L’Arbreda;
18–21: Pech de l’Aze
´, Le Moustier, La Ferrassie,
La Chappelle; 22: La Quina; 23: Saint-Ce
´saire;
24: Les Cotte
´s; 25: Arcy-sur-Cure; 26: Hyaena Den;
27: Pin Hole; 28: Spy; 29: Grotte Walou; 30: Ne
´ron;
31: Mandrin; 32: Bombrini/Mochi; 33:
Geissenklo¨sterle; 34: Fumane; 35: Castelcivita;
36: Oscurusciuto; 37: Cavallo; 38: Lakonis; 39: Ksar
Akil; 40: Mezmaiskaya. b, Bayesian PDFs for the
model boundaries of the final dated Mousterian
phases by site across Europe (generated using
OxCal4.2 software
20
and INTCAL13 (ref. 29)).
c, PDF for the latest Mousterian based on the
data in b.
LETTER RESEARCH
21 AUGUST 2014 | VOL 512 | NATURE | 307
Macmillan Publishers Limited. All rights reserved
©2014
at Mochi/Bombrini on the Italy–France border the Mousterian seems
to last longer—until 41,460–40,500 cal BP. In the latter region, the Auri-
gnacian arrives after a hiatus and no transitional complexes are evident.
Since both the Uluzzian and Aurignacian are linked to AMHs, this lends
support to the idea of a staggered replacement of Neanderthals in Italy
as they neared local extinction (Supplementary Methods). Other late
Mousterian contexts in sites in northern Spain, such as Abric Romanı
´
and L’Arbreda, are also considerably later than Fumane, suggesting that
the Mousterian ended at different times in some parts of Europe.
The temporal range of the ‘transitional’ technocomplexes was also
examined. With regard to the Cha
ˆtelperronian, it is apparent on stra-
tigraphic grounds thatthe Mousterian precedes it at all sites where both
occur. However, our results show that the Cha
ˆtelperronian at some sites
(for example, Arcy-sur-Cure) starts statistically significantly before the
end of the Mousterian at other sites in Europe such as Abric Romanı
´
and Geissenklo¨sterle (Germany). If Neanderthals were responsible for
both Mousterian and Cha
ˆtelperronian, the implication is that there was
considerable regional variation in their behaviour and adaptation stra-
tegies during this transition period. Assuming that the Cha
ˆtelperronian
is associated with Neanderthals, we combined the end boundaries for
both into a single-phaseBayesian model and obtained a final ‘Neander-
thal’ end PDF of 40,890–39,220 cal BP. The result is indistinguishable
from the final Mousterian PDF, showin g thatuncertainty over the author-
shipof the Cha
ˆtelperronian does not affect theage estimated for the last
Neanderthals; they did not survive after,41,000–39,000 cal BP (Fig. 2b).
By comparing the final Neanderthal PDF with those obtained for the
start of the Uluzzian at the Cavallo site
23
, we can quantify the temporal
overlap between Neanderthals and the earliest western European AMHs
(Fig. 2b). The difference is significant and ranges from 2,600 to 5,400
years at 95.4% probability. Coexistence has been linked previouslywith
the possibility of cultural transmission from AMHs to Neanderthals,
termed ‘acculturation’
24
, as a means of accounting forlate Neanderthal
technical and behavioural development. The early presence of AMHs
in Mediterranean Europe by ,45,000–43,000 cal BP (ref. 23) and the
35,00040,00045,00050,00055,000
60,000
Modelled date (cal BP)
a
b
Mousterian
Châtelperronian
Uluzzian
Uluzzian start
Uluzzian end
Châtelperronian end
Châtelperronian start
Mousterian end
Figure 2
|
Transitional site locations and Bayesian age ranges for the
start and end of the Cha
ˆtelperronian and Uluzzian technocomplexes.
a, Geographic distribution of Cha
ˆtelperronian (red), Uluzzian (green) and
Mousterian (blue) technocomplexes. Map is shown with sea level at 280 m
below the present day
1
. Dated ‘transitional’ industry site locations are shown.
Sea-level template map prepared by M. Deve
`s. b, Bayesian modelled PDFs
for the start and end boundaries of the Cha
ˆtelperronian and Uluzzian in
western Europe. The Mousterian end boundary (Fig. 1c) is shown for
comparison. The three end boundaries overlap, but the late Mousterian always
predates the two transitional industries stratigraphically where they co-occur.
45,000 cal BP 44,000 cal BP
43,000 cal BP 42,000 cal BP
40,000 cal BP
41,000 cal BP
Mousterian Uluzzian Châtelperronian
Figure 3
|
Time slices for western Europe
between 45,000 and 40,000 cal BP showing the
distribution of the Mousterian, Cha
ˆtelperronian
and Uluzzian modelled ages. The size of the dots
represents increasing and decreasing levels of the
95.4% probability ranges determined from the
duration (date range) of each industry, as
calculated by individual Bayesian site models
(Supplementary Methods). Dots with two colours
indicate overlapping date range probabilities for
two industries found at the same site.
RESEARCH LETTER
308 | NATURE | VOL 512 | 21 AUGUST 2014
Macmillan Publishers Limited. All rights reserved
©2014
potential overlapping time may have acted as a stimulus for putative
Neanderthal innovative and symbolic behaviourin the millennia before
their disappearance. When we compare the start and end boundary PDFs
for both Uluzzian and Cha
ˆtelperronian sites we observe that they are
very similar (Fig. 2b). This may provide further support for an accul-
turation model. Alternatively, this similarity in the start dates of the
two industries might be seen as reflecting an AMH authorship for both.
If this were the case, then the distribution of early modern humans
would be wider than expected.Since the physical evidence linking these
industries to differenthuman groups is scarce, these interpretationsare
potentially prone to change with new excavation data.
High-precision chronometric data and Bayesian modelling allows
us to map the spatiotemporal relationship between the three techno-
complexes during the period ,45,000–41,000 cal BP as a series of time
slices (Fig. 3 and Supplementary Methods). Since there is little to no robust
evidence for interstratification of the transitional industries within Mous-
terian archaeological layers, we concludethat the chronological overlap
observed musthave also involved a degree of spatial separation between
the two populations, regardless of whether Neanderthals were responsi-
ble for the Cha
ˆtelperronian or not. In turn, this suggests that the dispersal
of early AMHs was initially geographically circumscribed, proceeding
step-wise, with the Uluzzian first and the Aurignacian following a few
millennia later. The transitional industries, including those not analysed
here, may be broadly contemporaneous technocomplexes that remained
spatially distinct from one another. Rather than a rapid model of replace-
ment of autochthonous European Neanderthals by incoming AMHs,
our results support a morecomplex picture, one characterized by a bio-
logical and cultural mosaic that lasted for several thousand years.
METHODS SUMMARY
AMS radiocarbon dating was undertaken at the Oxford Radiocarbon Accelerator
Unit, University of Oxford. Collagen was extracted using the methods outlined
previously
11,25
. Shell samples were dated according to the protocol outlined previously
26
An acid–base oxidation/stepped combustion (ABOx-SC) method was used for
charcoal
13
. Radiocarbon ages are given as conventional ages BP as described previously
27
.
Corrections were made to bone collagen AMS determinations using a laboratory
pre-treatmentbackground subtraction
28
. Bones analysed rangefrom very well pre-
served (a maximum of 14.9wt% collagen) to poorly preserved (a minimum of ,1.0wt%
collagen). C:N atomicratios and otheranalyticalparameters weremeasured to deter-
mine the quality of the extracted collagen. The IntCal13 and Marine13 (ref. 29)
calibration curves and the OxCal4.2 (ref. 20) program were used in the calibration
and Bayesian age modelling. Supplementary Methods contains details of thearchae-
ologicalsites investigated, the samplesused, all determinationsand the full Bayesian
analysis.
Received 7 May; accepted 27 June 2014.
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Supplementary Information is available in the online version of the paper.
Acknowledgements The Natural Environment Research Council (NERC) funded this
work (NE/D014077/1). Additional funding was received from the Leverhulme Trust,
through the Ancient Human Occupation of Britain (AHOB) project, the NRCF (NERC
Radiocarbon Facility) programme, Keble College (Oxford) and the European Research
Council. We thank our many collaborators and their excavation teams, and all staff at
the Oxford Radiocarbon Accelerator Unit for their contribution to this work. Maps at
280 m below current sea level were produced by M. Deve
`s and A. Scheder Black.
Author Contributions T.H. and R.J. conceived the project. T.H. obtained funding and
directed the project. T.H., R.W., K.D., F.B., C.B.R. and A.Ma. performed pre-treatment
chemistry, AMS dating and Bayesian analysis using OxCal. T.H., R.W., K.D., L.B. and R.J.
sampled materials for AMS dating. T.H. and K.D. wrote the paper and all co-authors
contributed to the draft. K.D. and T.H. produced the figures and illustrations. R.J., L.B.,
M.C., A.A.,J.B., C.B.-R., C.Be.,C.Bo., P.B., M.C., N.J.C.,C.D., A.F., B.G., P.G.,A.G.-M., S.G., P.H.,
B.H., M.-J.I.-C., A.J., J.F.J.P., J.-M.M.-F., J.M., M.M., L.M., E.M., A.Mo., F.N., E.P., M.P., S.P.,
M.d.l.R., J.R.-S., A.R., D.S., P.S., L.S., J.S., N.S., A.V. and R.P. provided permits and
archaeological samples, expertise on site sequences and prior data for the modelling.
Author Information Reprints and permissions information is available at
www.nature.com/reprints. The authors declare no competing financial interests.
Readers are welcome to comment on the online version of the paper.
Correspondence and requests for materials should be addressed to
T.H. (thomas.higham@rlaha.ox.ac.uk).
LETTER RESEARCH
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