International Journal of Osteoarchaeology

Int. J. Osteoarchaeol. 14: 162–177 (2004)

DOI: 10.1002/oa.753

Carbon and Nitrogen Stable Isotopes as

Tracers of Change in Diet Breadth during
Middle and Upper Palaeolithic in Europe
D. DRUCKER* AND H. BOCHERENS
Institut des Sciences de l’Evolution, UMR 5554, Université Montpellier 2, Case Postale 064,
Place Eugène Bataillon, F-34095 Paris Cedex 05, France

ABSTRACT Carbon and nitrogen stable isotope ratios in fossil bone collagen have been used as evidence
for an increase of diet breadth between Middle Palaeolithic Neanderthals and Early Upper
Palaeolithic anatomically modern humans. In this paper, we revisit the rules of palaeodietary
reconstruction using collagen stable isotopes and reassess the possible isotopic signatures
of potential protein resources available to prehistoric humans. It appears that the interpreta-
tion of the human’s isotopic signature does not necessarily imply a significant proportion of
aquatic-derived protein in the diet neither for Neandertal nor for first anatomically modern
humans in Europe. Exploitation of aquatic ecosystems by humans needs to be supported by
further zooarchaeological evidence. Nevertheless, isotopic biogeochemistry of fossil human
collagen can be very useful in palaeodietary reconstructions provided that basic rules are
followed while selecting samples of coeval fauna, in order to establish the end members of
different food resources. Significant progress investigating the evolution of subsistence
strategies in fossil hominids is expected from a combination of zooarchaeological and
isotopic data. Copyright ß 2004 John Wiley & Sons, Ltd.

Key words: anatomically modern human; collagen; diet; Middle Palaeolithic; Neanderthal;
stable light isotopes; Upper Palaeolithic

Introduction modern human, and that they were only capable

The question of the replacement of Middle
Palaeolithic Neanderthals by Upper Palaeolithic
anatomically modern humans in Europe is still a
hotly debated issue (e.g. Demars & Hublin, 1989;
Vandermeersch, 1989; d’Errico et al., 1998;
Karavanic & Smith, 1998; Mellars, 1998; Zilhão
& d’Errico, 1999; Orschiedt & Weniger, 2002).
Numerous hypotheses based on subsistence stra-
tegies have been proposed to explain this episode
of European prehistory. One idea is that Middle
Palaeolithic Neanderthals were less sophisticated
hunters than Upper Palaeolithic anatomically
* Correspondence to: Institut de Science de l’Evolution, UMR 5554,
Université Montpellier 2, Case Postale 064, Place Eugène Bataillon,
F-34095 Paris Cedex 05, France.
e-mail: dorothee.drucker@ec.gc.ca
Copyright # 2004 John Wiley & Sons, Ltd.
of scavenging or of opportunistic hunting (e.g.
Binford, 1984, 1988). However, numerous
zooarchaeological data point to the existence of
specialized hunting of large herbivores by Nean-
derthals (e.g. Farizy & David, 1989, 1992; Marcy
et al., 1993; Gaudzinski, 1995, 1996; Gaudzinski &
Roebroeks, 2000), and indicate that hunting with
advanced planning was possible for Neanderthals
(e.g. Mellars, 1989; Burke, 2000). In addition,
recent functional analyses of stone tools from
Crimean sites suggest that both Middle Palaeo-
lithic and Upper Palaeolithic hominids used a
similarly wide range of resources and that late
Neanderthals had similar subsistence strategies to
anatomically modern humans (Hardy et al., 2001).
Carbon and nitrogen stable isotopes in fossil
bone collagen have been used during the last
Received 24 March 2003
Revised 29 August 2003
Accepted 21 October 2003
Stable Isotopes and Diet Breadth
decade to place Neanderthals within the trophic
web (e.g. Bocherens et al., 1991, 1999, 2001; Fizet
et al., 1995; Richards et al., 2000; Bocherens &
Drucker, 2003a). These works interpret the main
dietary resources of Neanderthals through com-
parisons of their isotopic compositions with
those of coeval plant-eating ungulates and
meat-eating carnivores. Isotopic results have
been obtained so far on specimens from France,
Belgium and Croatia, ranging in age from around
120,000 to 30,000 years BP. These studies point
out that the isotopic signatures of Neanderthal
collagen are similar to those of coeval carnivores,
although generally with slightly more positive
15N in Neanderthals than in carnivores. These
data strongly suggest the prevalence of a reliance
on the meat of large herbivores dwelling in open
environments. Collagen isotopic data have also
been gathered on Early Upper Palaeolithic ana-
tomically modern humans from Europe, and their
15N values appear more positive than those of
Neanderthals (Richards et al., 2001b). These
results led the authors (supra) to conclude that
large herbivore meat was not the only food
resource consumed by these anatomically mod-
ern humans, and that freshwater resources, which
typically exhibit more positive 15N values than
terrestrial herbivores, were contributing a signifi-
cant part to the diet. Unfortunately, almost no
isotopic data obtained on coeval fauna were
discussed in this paper.
Since the first study of isotopic palaeodietary
reconstruction of Upper Pleistocene European
humans by Bocherens et al. in 1991, the multi-
plication of isotopic investigations on the mam-
mal faunas of Upper Pleistocene Europe have
refined our knowledge of the variability of iso-
topic compositions of potential prey (e.g.
Bocherens et al., 1996, 1997; Drucker et al.,
2000; Iacumin et al., 2000; Bocherens, 2003).
Moreover, studies of modern mammals in con-
trolled laboratory conditions and in monitored
natural conditions, in combination with mathe-
matical mixing models (e.g. Phillips, 2001;
Phillips & Greg, 2001; Koch & Phillips, 2003),
allow a better quantification of the relationship
between the isotopic composition of a consumer
and that of its average diet (e.g. Bocherens &
Drucker, 2003b). Due to these improvements in
isotopic ecology, it is possible to attempt more
Copyright # 2004 John Wiley & Sons, Ltd.
163
detailed palaeodietary reconstruction for fossil
humans.
The present paper will reconsider the isotopic
data currently available for Neanderthal and
Early Upper Palaeolithic anatomically modern
humans in Europe during Marine Oxygen Iso-
topic Stage 3 (MOIS 3), between around 60,000
and 25,000 year Before Present (BP). We will
discuss the isotopic evidence in view of a possible
widening of dietary breadth at the Middle to
Upper Palaeolithic transition, as has been pro-
posed recently by Mike Richards and collabora-
tors (Richards et al., 2001b). The first part of this
paper will examine: (1) how the isotopic compo-
sition of food is recorded as isotopic composition
in collagen; (2) what the isotopic signatures of
mammal fauna associated with fossil humans are;
and (3) what kind of chronological variation is
expected for stable isotope signatures. We will
then reconsider the current hypothesis that
collagen carbon and nitrogen stable isotopes
indicate that Neanderthals were consuming
exclusively meat from large terrestrial herbivores
as their source of animal proteins, and that
anatomically modern humans expanded their
dietary breadth by including freshwater resources
in the Early Upper Palaeolithic.
Checking the rules of isotopic
palaeoecology in Europe during MOIS 3
How is the isotopic composition of food
recorded in collagen?
The carbon and nitrogen isotopic compositions
of collagen provide a proxy for the reconstruc-
tion of ancient trophic webs. They are especially
useful for deciphering the relationships between
predators and their potential prey. Indeed, feed-
ing experiments performed under controlled con-
ditions have shown that there is a quantitative
relationship between the carbon and nitrogen
isotopic composition of the tissues of a given
terrestrial mammal and that of its average diet
(e.g. DeNiro & Epstein, 1978, 1981; Ambrose &
Norr, 1993; Tieszen & Fagre, 1993; Roth &
Hobson, 2000; Jenkins et al., 2001). The differ-
ence between the isotopic signature of an animal
tissue and that of its average diet is subject to
Int. J. Osteoarchaeol. 14: 162–177 (2004)
164
some variation (e.g. Hare et al., 1991; Hilderbrand
et al., 1996; Hobson et al., 1996; Ambrose, 2000).
A review of published enrichment values in
experimental conditions yields a range of 3.7 to
6.0% for 13C values between diet and collagen,
and a range of 1.7 to 6.9% for 15N values (see
review in Bocherens & Mariotti, 2002). A recent
study using modern wild mammals from Bialo-
wieza Primeval Forest in Poland produced an
accurate range of variations for isotopic fractio-
nation in carbon and nitrogen between a predator
collagen and that of its prey (Bocherens &
Drucker, 2003b). These data, together with addi-
tional data from ancient terrestrial ecosystems,
have allowed to propose an enrichment of 0.8 to
1.3% for 13C values and an enrichment of 3 to
5% for 15N values between the collagen of a
predator and that of its average prey. Knowing
the carbon and nitrogen isotopic signatures of a
predator’s collagen, such enrichment values allow
us to calculate the expected 13C and 15N
collagen values of the average prey consumed
by a given predator, including Neanderthals and
prehistoric humans of modern type. A compar-
ison of the collagen isotopic signatures of poten-
tial prey available to the predator and that
deduced from the predator itself should lead to
quantitative estimates of the consumption of
different types of prey using mixing models or
at least it should allow the consumption of given
prey to be tested.
What are the isotopic signatures of mammal
fauna associated with fossil humans?
The main prey species found in Middle Palaeo-
lithic sites are large ungulates, such as the horse
(Equus sp.), bovines (Bos or Bison spp.), woolly
rhinoceros, (Coelodonta antiquitatis), woolly mam-
moth (Elephas primigenius), reindeer (Rangifer taran-
dus) and red deer (Cervus elaphus) (e.g. Patou, 1989;
Webb, 1989; Dibble & Rolland, 1992;
Baryshnikov & Hoffecker, 1994). A very diverse
assemblage of intermediate to large herbivores
was dwelling on the European continent during
MOIS 3 (e.g. Vereshchagin & Baryshnikov, 1982;
Guthrie, 1990). The vegetation reconstructed for
this period does not present large isotopic con-
trasts such as those observed in modern tropical
Copyright # 2004 John Wiley & Sons, Ltd.
D. Drucker and H. Bocherens
savannahs and forests, due to the lack of plants
using the C4 photosynthetic pathway. However,
some carbon isotopic variability has been evi-
denced in herbivores according to their taxon.
Mammoths exhibit the most negative 13C values
when compared to horse and woolly rhinoceros,
while bovines, and to a greater extent reindeer,
present more positive 13C values than all the
other ungulates (Bocherens et al., 1996, 1997;
Drucker et al., 2000; Iacumin et al., 2000;
Bocherens, 2003). This pattern is observed over
a large geographical area, from France to Alaska,
and is interpreted as reflecting dietary adaptation
of the different herbivorous taxa (supra). For
instance, reindeer was consuming large amounts
of 13C-enriched lichens, whereas mammoth,
horse and rhinoceros were mostly relying on
tall grass with 13C-depleted content (e.g.
Drucker et al., 2000; Bocherens, 2003). The
15N values of herbivore collagen also present
variations between co-occurring taxa (Bocherens
et al., 1996, 1997; Drucker et al., 2000; Iacumin
et al., 2000; Bocherens, 2003). The inter-specific
variations in herbivore 15N values reflect the
variations in plants such as grass and different
types of shrubs with symbiotic mycorhizes in
their roots (see detailed discussion in Bocherens,
2003). The consequence of this situation is that
different herbivores available to predators as prey
exhibit carbon and nitrogen isotopic signatures
that are sufficiently distinct for them to be
considered as different food resources in an
isotopic, palaeoecological study. This was the
case for the Neanderthal from Saint-Césaire
relative to the isotopic composition of potential
prey species, as documented by analyses per-
formed on bone samples from three contempor-
ary sites in the same area, i.e. Saint-Césaire, La
Berbie and Camiac (Table 1).
How much isotopic variation is
expected chronologically?
Variations of isotopic signatures in the collagen
of a given species through time have been docu-
mented in Europe, especially for 15N values
(Fizet et al., 1995; Iacumin et al., 1997; D. Drucker,
unpublished PhD dissertation, 2001; Drucker et al.,
2003b, in press; Richards & Hedges, 2003). For
Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth
Table 1. Summary of isotopic data measured on bone collagen from herbivore mammals from La Berbie,
Camiac, and layer Ejop sup of Saint-Césaire, all dated to around 35,000 BP (Guadelli, unpublished PhD
dissertation, 1987; Mercier et al., 1993; Madelaine, unpublished report, 1999)
Taxon n 13C
Reindeer 7
19.1
Bovine (Bos or Bison) 15
20.4
Horse 6
20.8
Rhinoceros 5
20.2
Mammoth 3
21.6
the area and period under consideration here, it is
not possible to provide a detailed isotopic curve
of bone collagen 15N values for a given species.
The isotopic variations prior to 40,000 years BP
are very unclear due to difficulties dating collagen
older than that age. Richards & Hedges (2003)
published a preliminary trend for four herbivore
species in northwestern Europe as a whole, which
suggests more positive 15N values around
30,000 years BP relative to samples of younger
age. For instance, 15N values increase up to
around 10% for bovine collagen by 30,000 years
BP, whereas they drop to 6% around 28,000 BP
(Figure 3 in Richards & Hedges, 2003). The case
for high 15N values in mammal herbivores
around 30,000 years BP is confirmed by the
isotopic signatures obtained on several taxa
from the site of Castanet in southwestern France,
where reindeer and horse 15N values range from
8.4 to 10.3% (Drucker, in press). In a previous
work, we suggested a relationship between the
15N values of terrestrial mammals and the rate of
nitrogen cycling in soils influenced by the inten-
sity of glacial conditions (Drucker et al., 2003a,
2003b). These patterns of variability seem to be
reliable for northern and western Europe, but not
for Mediterranean areas (Iacumin et al., 1997;
Richards & Hedges, 2003).
Quantitative estimate of the prey
consumed by Neanderthals
Four different sites of MOIS 3 age produced
isotopic signatures of Neanderthal collagen
(Figure 1). The range of isotopic signatures of
average prey are presented on the figure, using
the range of isotopic fractionations for 13C and
15N established by Bocherens & Drucker
Copyright # 2004 John Wiley & Sons, Ltd.
165
SD 15N SD
0.4 5.8 1.7
0.3 6.0 1.0
0.5 5.7 1.5
0.5 7.0 1.1
0.3 8.3 0.5
(2003b). These ranges fall close to the isotopic
signatures of potential herbivorous mammal prey,
when such values are available for comparison.
Globally, the 15N values of Neanderthals are
slightly more positive than those of coeval pre-
dators, such as wolves and hyaenas (Figure 1).
One difference between the meat consumed by
Neanderthals and that consumed by animal pre-
dators is cooking, which is usually performed by
Neanderthals but not by animal predators. It is
questionable whether cooking can lead to
changes in the isotopic signatures of meat prior
to its consumption by humans. Bonsall et al.
(1997) report that cooking has very little effect
on 15N values, but do not provide any actual
data. Cooking experiments conducted by
Katzenberg and colleagues (2000) demonstrate
small effect of heating on 13C values of vege-
tables (less than 1.2%) and meat (no more than
0.1%). We have performed a few basic experi-
ments on cooked meat and fish (D. Drucker,
unpublished PhD dissertation, 2001), The change
in 15N values range from
0.4 to þ0.2%
(Table 2), which is negligible when compared to
the variation observed between specimens of the
same species in a given site. Experiments using well
monitored cooking techniques based on ethnolo-
gical examples would be helpful to address this
issue more thoroughly. So far, there is no experi-
mental evidence for an influence of cooking on
15N values of meat consumed by humans.
In the case of Saint-Césaire, located in Char-
entes-Maritimes (France), it is possible to go
one step further thanks to the large dataset
of analysed potential prey. Indeed, isotopic
measurements have been carried out on herbivor-
ous mammals from the same layer as the Nean-
derthal specimen (layer Ejop sup in Saint-Césaire),
and on specimens of large mammals from two
Int. J. Osteoarchaeol. 14: 162–177 (2004)
166 D. Drucker and H. Bocherens

Figure 1. Collagen 13C and 15N values of Neanderthals dated of MOIS 3 (between around 45,000 and 30,000 years
BP), with coeval mammal fauna. Marillac, Saint-Césaire, Camiac and La Berbie are located in southwestern France
(Fizet et al., 1995; Drucker et al., 1999; Bocherens, unpublished data), Wallonia sites are located in Belgium
(Bocherens et al., 2001), and Vindija Cave is located in Croatia (two dated Neanderthals; Richards et al., 2000).
The ellipse stands for the range of the isotopic values expected for average prey collagen. Key for humans:
M ¼ Marillac; SC ¼ Scladina; Spy ¼ Spy; StC ¼ Saint-Césaire.

Table 2. Summary of the effect of different cooking treatments on fish and meat on 15N values (Drucker,
unpublished PhD thesis, 2001)

Sample Cooking
15N

treatment (15Ncooked-15Nraw)

Salmon flesh Roasted 0.2

Beef flesh Roasted 0.1
Roe deer bone red marrow Boiled
0.3
Roe deer bone red marrow Boiled 0.2
Roe deer bone red marrow Boiled
0.4

Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth
Figure 2. Application of the mixing model proposed by
Phillips & Koch (2002) to Neanderthals and hyaenas from
Saint-Césaire, Camiac and La Berbie. The triangle repre-
sents the possible isotopic values of mixtures of three
dietary poles (horse/bovine, reindeer, mammoth). The
rectangles stand for the possible isotopic values of
average prey consumed by Neanderthals and hyaenas,
using the range of isotopic fractionations presented by
Bocherens & Drucker (2003b).
additional sites from the same area, i.e. Camiac
and La Berbie, both roughly contemporary with
the Ejop sup layer of Saint-Césaire, dated to
around 36,000 BP ( J. L. Guadelli, unpuhlished
PhD dissertation, 1987; Mercier et al., 1993; S.
Madelaine, unpublished report). In this case, we
have used the mixing model presented by Phillips
& Koch (2002), but taking into account the
variability of isotopic fractionation for 13C and
15N values (Bocherens & Drucker, 2003b).
Using the average isotopic values for potential
prey (presented in Table 1), hyaena and Nean-
derthal, we calculate the ranges of percentages of
different prey compatible with the observed iso-
topic composition for Neanderthal and for hyae-
nas (Figure 2). This calculation is performed using
the spreadsheet, which is available at http://
www.epa.gov/wed.pages/models.htm (Phillips &
Koch, 2002), for the whole range of possible
values intercepting the triangle of potential prey
Copyright # 2004 John Wiley & Sons, Ltd.
167
and the rectangle of possible isotopic signatures
deduced from the isotopic signatures of preda-
tors. Considering three different prey, i.e. mam-
moth, reindeer and an average of bovine and
horse, whose isotopic signatures are relatively
close, it appears that the percentages of different
prey clearly differ between the hyaena and
Neanderthal samples. Results indicate that mam-
moth constitutes an obligate prey for Nean-
derthal but only an optional one for Hyaena
(with no more than 21%), whereas reindeer and
bovine/horse are obligate prey for hyaena and
only optional prey for Neanderthals (Figure 3).
Other choices of prey, for example Woolly
rhinoceros, would have led to different percen-
tages. The goal of this calculation is to illustrate
how different proportions of prey species could
explain the differences observed between the
isotopic signatures of Neanderthals and hyaenas
without invoking a difference in the composition
of prey species selected. The more positive 15N
values observed for Neanderthals relative to ani-
mal predators such as hyaena suggest that prey
with elevated 15N values, such as woolly mam-
moth and woolly rhinoceros, constituted a larger
part of the Neanderthal diet relative to smaller
ungulates such as horse or reindeer than they did
for carnivores such as hyaena. Zooarchaeological
evidence also points to the procurement of meat
from these large herbivores in Europe in some
Middle Palaeolithic sites (e.g. Auguste, 1995;
Auguste et al., 1998; Conard & Prindiville, 2000;
Weber, 2000; Moncel, 2001). When sufficient
isotopic data are available for the potential prey
of Neanderthals and for coeval animal predators,
the isotopic approach, using mixing models with
the proper fractionation factors, is thus able to
test different scenarios of prey consumption by
humans and animal predators, in view of the
zooarchaaeological evidence.
Do isotopic data indicate that
anatomically modern humans of Early
Upper Palaeolithic consumed
diversified dietary resources, such
as marine and freshwater food items?
Recent isotopic data published by Richards
et al. (2001b) for Early Upper Palaeolithic
Int. J. Osteoarchaeol. 14: 162–177 (2004)
168 D. Drucker and H. Bocherens

Figure 3. Range of proportion of prey (horse/bovine, reindeer, mammoth) consistent with the measured isotopic
signatures of Neanderthals and hyaenas in southwestern France around 35,000 years BP, using the mixing model
proposed by Phillips & Koch (2002) and the range of isotopic fractionations presented by Bocherens & Drucker
(2003b).

anatomically modern humans from different Eur-
opean sites appear to be generally different from
those measured on Neanderthals, especially with
respect to more positive 15N values. These 15N
values were compared to those of herbivores,
either coeval with Neanderthals or of Early
Upper Palaeolithic (Richards et al., 2001b). These
comparisons seemingly indicate that no herbi-
vore presents 15N values suitable for explaining
the isotopic values of humans as their predators.
Richards and colleagues (2001b) suggest addi-
tional dietary resources and report on a selection
of freshwater fish and fowl (identified in the
literature) whose 15N values are consistent
with the most positive 15N values exhibited by
Early Upper Palaeolithic anatomically modern
humans. This interpretation relies on three
assumptions: (1) the 15N-enrichment between
two successive trophic levels is only 3%; (2)
freshwater resources present significantly more
Copyright # 2004 John Wiley & Sons, Ltd.
positive 15N values than terrestrial herbivores;
and (3) some Early Upper Palaeolithic modern
humans exhibit 15N values as positive as those of
the Mesolithic population of the Iron Gates
(Balkans), where freshwater resource consump-
tion is clearly demonstrated by zooarchaeologi-
cal evidence (Bonsall et al., 1997).
As seen above, however, recent work has
shown that the 15N-enrichment between prey
and predator is not limited to 3%, but rather
ranges from 3 to 5% (Bocherens & Drucker,
2003b), which makes possible the consumption
of prey with less positive 15N values than are
estimated by Richards et al. (2001b).
The actual isotopic signatures of freshwater
resources available to Early Upper Palaeolithic
humans is difficult to assess. So far, no direct
isotopic measurements have been performed on
freshwater fish bones of Early Upper Palaeolithic
age, which occasionally occur (e.g. Cleyet-Merle
Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth 169

1990), and only a handful of Early Holocene
material has been investigated (Bonsall et al.,
1997). As a matter of fact, Richards and collea-
gues (2001b) used as reference a mixture of
published values for modern fish, mainly from
lakes, and isotopic values from Early Holocene
material. Unfortunately, most of the studied
modern freshwater ecosystems are located in
North America (e.g. Rau, 1980; Fry, 1991;
Hesslein et al., 1991; Beaudoin et al., 1999) and
have suffered from significant anthropic disrup-
tions (e.g. Vander Zanden et al., 1999). Hence,
the derived isotopic data are not necessarily
suitable as reference datasets for the prehistoric
period in Europe. Indeed, studies demonstrate
the high variability of stable isotope ratios for
freshwater fish since aquatic plants have access to
different sources of caron dioxide (CO2) and
fishes experience different habitat and trophic
level, even during their own lifetime (e.g.
Katzenberg & Weber, 1999).
This situation led us to perform new collagen
extractions and isotopic analyses on ancient
freshwater material. We carried out isotopic
analysis on fish and otter (Table 3) from two
French archaeological sites that yielded abundant
aquatic material: Pont d’Ambon (Dordogne,
13,000 to 9,500 years BP: Célérier, 1998) and
Noyen-sur-Seine (Seine-et-Marne, around
8,000 BP: Marinval-Vigne and Mordant, 1989).
Otter collagen isotopic signatures represent a
pure freshwater feeder and allow us to deduce the
carbon and nitrogen isotopic composition of its
prey. The calculation has been performed using
the isotopic fractionation between predator and
prey collagen proposed by Bocherens & Drucker
(2003b). The results of this calculation are pre-
sented in Table 4 with a review of the available
isotopic data obtained on aquatic resources from
temperate and peri-arctic environments in ancient
Europe. The range of 13C values is large, from

25.2 to
19.8% and the 15N values range
between 6.5 and 10.7%, with no clear pattern
relative to species, age and location.
Our reassessed 13C values of freshwater
resources are similar to those used by Richards
and colleagues. Obviously, the 13C enriched
human collagen is unlikely explained by a large
contribution of this 13C depleted food item. The
15N values presented in Table 4 are less positive
than those published by Richards and colleagues
(2001b), which ranged from 10.7 to 13.2%. The
selection performed by Richards et al. was
strongly biased towards lacustrine specimens,
which seem to present more positive 15N values
than riverine specimens, while the data presented
in this study are only for river specimens. This
new assessment of the isotopic values of fresh-
water resources shows that they are not necessa-
rily so 15N enriched compared to terrestrial
resources.
Reassessments of the isotopic signatures of
freshwater resources available to prehistoric
humans indicate that they represent a dietary
source with less positive 13C values and 15N
values than assumed by Richards et al. (2001b).
The addition of some marine resources, which
can occur in freshwater environments through

Table 3. New isotopic data on freshwater fish and otter bone collagen from two French archaeological sites;
Noyen-sur-Seine and Pont d’Ambon

N Species Site (Layer) Age Yield mg  g
1 % C %N C/N 13C 15N

NO7600 Eel (A. anguilla) Noyen-sur-Seine (9)  8,000 BP 40.7 14.5 3.3
23.8 8.3
NO3200 Otter (L. lutra) Noyen-sur-Seine (9)  8,000 BP 39.0 42.6 15.2 3.3
19.3 12.3
NO6500 Otter (L. lutra) Noyen-sur-Seine (9)  8,000 BP 103.7 41.2 15.1 3.2
24.2 10.7
NO6600 Otter (L. lutra) Noyen-sur-Seine (9)  8,000 BP 160 41.9 15.4 3.2
23.9 11.1
PAM5900 Cyprinide Pont d’Ambon (2)  9,500 BP 4.7 35.4 13.2 3.1
21.5 9.4
PAM6000 Pike (Esox lucius) Pont d’Ambon (2)  9,500 BP 10.6 36.2 13.6 3.1
22.2 9.5
PAM6200 Eel (A. anguilla) Pont d’Ambon (3)  10,000 BP 3.7 35.3 13.6 3.0
23.7 8.0
PAM6300 Cyprinide Pont d’Ambon (4)  12,500 BP 3.5 12.8 4.7 3.1
21.1 6.6
PAM6400 Eel (A. anguilla) Pont d’Ambon (4)  12,500 BP 2.8 36.3 13.8 3.1
20.8 8.5
PAM6600 Salmonide Pont d’Ambon (5)  13,000 BP 10.9 9.8 4.0 2.9
16.1 12.1

Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
170 D. Drucker and H. Bocherens
Table 4. Review of the available isotopic data obtained on aquatic resources from temperate and peri-arctic
environments in ancient Europe.  calculation based on the isotopic fractionation determined by Bocherens and
Drucker (2003b)

Species Location N Habitat 13C 15N Age Ref.

Pike Southwestern France 1 River
22.2 9.5  9,500 BP (1)

Cyprinide Southwestern France 1 River
21.5 9.4  9,500 BP (1)
Cyprinide Southwestern France 1 River
21.1 6.6  12,500 BP (1)
Eel Northern France 1 River
23.8 8.3  8,000 BP (1)
Unknown river dweller Danube 1 River
19.8 10.7 7,000
8,500 BP (2)

Otter’s food Northern France 1 River
20.3  0.3 8.3  1.0  8,000 BP (1)
Otter’s food Northern France 1 River
25.2  0.3 6.7  1.0  8,000 BP (1)
Otter’s food Northern France 1 River
24.9  0.3 7.1  1.0  8,000 BP (1)
Otter’s food Danube 1 River
20.2  0.3 6.5  1.0 7,000
8,500 BP (2)
Average  sd
22.2  1.9 8.1  1.4
Unknown anadromous Danube 1 River/Marine
15.7 12.9 7,000
8,500 BP (2)
Salmonide Southwestern France 1 River/Marine
16.1 12.1  13,000 BP (1)
Average  sd
15.9  0.2 12.5  0.4

migration of anadromous species, can raise the vant as potential food resources, even in the case
13C values of the mean diet. Anadromous fish, of continental human populations. Indeed, col-
such as salmon (e.g. Ben-David et al., 1997), and lagen carbon isotopic signatures have proven
some migrating birds (Hobson, 1999), are rele- salmon consumption for palaeoindians several

Figure 4. Collagen 13C and 15N values of Early Upper Palaeolithic anatomically modern humans with mammal fauna
of similar age (data from Ambrose, 1998; Iacumin et al., 2000; Drucker, in press). The ellipse stands for the range of the
isotopic values expected for average prey collagen. Key for humans are the following: K1 ¼ Kostenki 1; K18 ¼ Kostenki
18; M ¼ Mal’ta 1; S1, S2, S3 ¼ Sunghir 1, 2, 3; B ¼ Brno-Francouzska 2, DV ¼ Dolni Vestonice 35.

Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth 171

Figure 5. Changes in 15N values of horse, bovine, wolf, hyaena and human collagen at different periods between
around 45,000 years BP and 21,000 years BP (data from Iacumin et al., 2000; Richards, 2000; Richards et al., 20001b;
Drucker, in press). Comparison with 15N values in bovine, freshwater fish and humans from Iron Gates, around 7,000
years BP (data from Bonsall et al., 1997). Key for humans as given in Figures 1 and 4.

hundreds of kilometres from the coast in British
Columbia, Canada (Lovell et al., 1986). These
resources are 13C and 15N enriched relative to
terrestrial food resources (Table 4). A mixture of
Copyright # 2004 John Wiley & Sons, Ltd.
marine (anadromous or migratory) and riverine
resources could explain the isotopic signatures of
prehistoric humans, but such combinations
should be established using zooarchaeological
Int. J. Osteoarchaeol. 14: 162–177 (2004)
172
evidence in the studies sites, which is beyond the
scope of this paper.
To complete the dietary reconstructions of
modern human, we added the isotopic data of
terrestrial mammals. As an isotopic shift of 15N
values of terrestrial mammals collagen is observed
through time (Richards & Hedges, 2003; Drucker
et al., 2000, 2003b), we selected terrestrial mam-
mals remains from contemporaneous sites from
Europe (Figure 4). It appears that the 13C values
of terrestrial mammal collagen are more positive
than those of freshwater fish collagen. Taking
into account the isotopic difference in collagen
between a predator and its prey, the 13C values
of coeval fauna fit the expected 13C values of
averaged prey collagen, values deduced from
anatomically modern human isotopic signature
(Figure 4). The 15N of terrestrial mammals are
within a similar range in the case of the new
estimate for river resources, especially when
mammoth is considered (Figure 4).
Considering this updated estimate, obligate
implication of freshwater resources in human
diet is not so convincing. Although we do not
exclude any fish consumption, we consider that
contemporaneous terrestrial resources are suffi-
cient to explain the isotopic signature of anato-
mically modern humans. This conclusion is also
sound as far as Neanderthals are concerned.
The hypothesis of a strong trophic relation-
ship between terrestrial mammals and humans is
reinforced by the stability of their 15N differ-
ence (Figure 5). This stability is significant as 15N
amounts of terrestrial herbivores exhibit impor-
tant changes through time. In particular, a dra-
matic increase of the 15N values is found around
35,000–32,000 years BP for herbivores as well as
for terrestrial animal predators. In this context,
the high 15N value of the individual of Kostenki
1 (dated to 32,600  1100 BP OxA 7073) com-
pared to the Neanderthals, from Marillac, Wal-
lonia and southwestern France, is consistent with
the general isotopic shift observed in terrestrial
ecosystems. This case illustrates how a difference
of isotopic signature between humans can finally
lead to the same dietary interpretation. On the
contrary, the same 15N values of Kostenki 1 and
Iron Gates humans cannot result from the same
diet characteristics. Indeed, the mean 15N values
Copyright # 2004 John Wiley & Sons, Ltd.
D. Drucker and H. Bocherens
measured on terrestrial mammal collagen are as
different as about 4% between the two archae-
ological contexts. As a result, contemporaneous
terrestrial resources exhibit 15N values too low
for contributing alone to the isotopic signature of
the humans in Iron Gates, whereas, in they can
easily explain the 15N value measured on the
human of Kostenki.
Conclusions
The isotopic reconstruction of prehistoric human
diet raises several difficulties. First, the evaluation
of the isotopic enrichment linked to trophic
relationship provides a range of values rather
than an accurate figure. As a result, it enlarges
the possible sources of food, and more specifi-
cally the source of protein as far as collagen is
concerned. Second, the isotopic signature of
protein resources for human can be subject to
chronological evolution. Hence, it is sometimes
imperative to have access to the coeval fauna for
isotopic analysis in order to correctly evaluate the
signatures of protein resources. Lastly, consider-
ing zooarchaeological evidence is crucial when
isotopic study leads to equally probable scenar-
ios. When ideal conditions are reached (isotopic
analysis of human and coeval fauna selected
through zooarchaeological study), it proves
useful to apply a quantitative diet estimate to
decipher food sources reliance.
On the basis of isotopic data accumulated to
date, the following conclusions can be presented.
The current isotopic data obtained on Early
Upper Palaeolithic anatomically modern humans
can be interpreted as reflecting the consumption
of protein provided by meat of terrestrial herbi-
vores and do not necessarily require the addition
of significant amounts of freshwater fish. A similar
conclusion can be inferred for Neanderthals. This
interpretation, based on the isotopic tracking of
protein origin through collagen, does not pre-
clude some consumption of plant material since
this last dietary resource would provide much less
protein than meat for a similar dry weight con-
sumption. If confirmed, the similar importance of
exploitation of the terrestrial resources for Nean-
derthals and the first anatomically modern human
Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth
in Europe, leads to the possibility of a direct
dietary competition between both hominids.
The contribution of isotopic study to human
palaeodietary reconstruction has been certain.
There is no doubt that future investigations will
help to improve the precision and relevance of
the interpretations based on isotopic studies. In
addition to increasing the reliability of human
diet reconstruction, the establishment of chron-
ological fauna references will contribute to a
better knowledge of terrestrial environments in
the past.
Acknowledgements
Thanks are due to D. Billiou for technical assis-
tance during isotopic analyses. Freshwater faunal
material from Noyen-sur-Seine has been made
available by A. Bridault, M.-C. Marinval and J.-D.
Vigne, and from Pont d’Ambon has been made
available by G. Célérier and O. LeGall. We thank
J. Pelegrin for allowing isotopic analysis on
material from Castanet, and S. Madelaine and
J.-L. Guadelli for allowing isotopic analysis on
material from La Berbie and Camiac, respectively.
This paper was highly improved thanks to revi-
sion and comments from A. Burke and two
anonymous reviewers.
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