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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
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

of scavenging or of opportunistic hunting (e.g.
The question of the replacement of Middle Binford, 1984, 1988). However, numerous
Palaeolithic Neanderthals by Upper Palaeolithic zooarchaeological data point to the existence of
anatomically modern humans in Europe is still a specialized hunting of large herbivores by Nean-
hotly debated issue (e.g. Demars & Hublin, 1989; derthals (e.g. Farizy & David, 1989, 1992; Marcy
Vandermeersch, 1989; d’Errico et al., 1998; et al., 1993; Gaudzinski, 1995, 1996; Gaudzinski &
Karavanic & Smith, 1998; Mellars, 1998; Zilhão Roebroeks, 2000), and indicate that hunting with
& d’Errico, 1999; Orschiedt & Weniger, 2002). advanced planning was possible for Neanderthals
Numerous hypotheses based on subsistence stra- (e.g. Mellars, 1989; Burke, 2000). In addition,
tegies have been proposed to explain this episode recent functional analyses of stone tools from
of European prehistory. One idea is that Middle Crimean sites suggest that both Middle Palaeo-
Palaeolithic Neanderthals were less sophisticated lithic and Upper Palaeolithic hominids used a
hunters than Upper Palaeolithic anatomically similarly wide range of resources and that late
Neanderthals had similar subsistence strategies to
* Correspondence to: Institut de Science de l’Evolution, UMR 5554, anatomically modern humans (Hardy et al., 2001).
Université Montpellier 2, Case Postale 064, Place Eugène Bataillon,
F-34095 Paris Cedex 05, France. Carbon and nitrogen stable isotopes in fossil
e-mail: bone collagen have been used during the last
Copyright # 2004 John Wiley & Sons, Ltd. Received 24 March 2003
Revised 29 August 2003
Accepted 21 October 2003
Stable Isotopes and Diet Breadth 163

decade to place Neanderthals within the trophic detailed palaeodietary reconstruction for fossil
web (e.g. Bocherens et al., 1991, 1999, 2001; Fizet humans.
et al., 1995; Richards et al., 2000; Bocherens & The present paper will reconsider the isotopic
Drucker, 2003a). These works interpret the main data currently available for Neanderthal and
dietary resources of Neanderthals through com- Early Upper Palaeolithic anatomically modern
parisons of their isotopic compositions with humans in Europe during Marine Oxygen Iso-
those of coeval plant-eating ungulates and topic Stage 3 (MOIS 3), between around 60,000
meat-eating carnivores. Isotopic results have and 25,000 year Before Present (BP). We will
been obtained so far on specimens from France, discuss the isotopic evidence in view of a possible
Belgium and Croatia, ranging in age from around widening of dietary breadth at the Middle to
120,000 to 30,000 years BP. These studies point Upper Palaeolithic transition, as has been pro-
out that the isotopic signatures of Neanderthal posed recently by Mike Richards and collabora-
collagen are similar to those of coeval carnivores, tors (Richards et al., 2001b). The first part of this
although generally with slightly more positive paper will examine: (1) how the isotopic compo-
15N in Neanderthals than in carnivores. These sition of food is recorded as isotopic composition
data strongly suggest the prevalence of a reliance in collagen; (2) what the isotopic signatures of
on the meat of large herbivores dwelling in open mammal fauna associated with fossil humans are;
environments. Collagen isotopic data have also and (3) what kind of chronological variation is
been gathered on Early Upper Palaeolithic ana- expected for stable isotope signatures. We will
tomically modern humans from Europe, and their then reconsider the current hypothesis that
15N values appear more positive than those of collagen carbon and nitrogen stable isotopes
Neanderthals (Richards et al., 2001b). These indicate that Neanderthals were consuming
results led the authors (supra) to conclude that exclusively meat from large terrestrial herbivores
large herbivore meat was not the only food as their source of animal proteins, and that
resource consumed by these anatomically mod- anatomically modern humans expanded their
ern humans, and that freshwater resources, which dietary breadth by including freshwater resources
typically exhibit more positive 15N values than in the Early Upper Palaeolithic.
terrestrial herbivores, were contributing a signifi-
cant part to the diet. Unfortunately, almost no
isotopic data obtained on coeval fauna were Checking the rules of isotopic
discussed in this paper. palaeoecology in Europe during MOIS 3
Since the first study of isotopic palaeodietary
reconstruction of Upper Pleistocene European How is the isotopic composition of food
humans by Bocherens et al. in 1991, the multi- recorded in collagen?
plication of isotopic investigations on the mam-
mal faunas of Upper Pleistocene Europe have The carbon and nitrogen isotopic compositions
refined our knowledge of the variability of iso- of collagen provide a proxy for the reconstruc-
topic compositions of potential prey (e.g. tion of ancient trophic webs. They are especially
Bocherens et al., 1996, 1997; Drucker et al., useful for deciphering the relationships between
2000; Iacumin et al., 2000; Bocherens, 2003). predators and their potential prey. Indeed, feed-
Moreover, studies of modern mammals in con- ing experiments performed under controlled con-
trolled laboratory conditions and in monitored ditions have shown that there is a quantitative
natural conditions, in combination with mathe- relationship between the carbon and nitrogen
matical mixing models (e.g. Phillips, 2001; isotopic composition of the tissues of a given
Phillips & Greg, 2001; Koch & Phillips, 2003), terrestrial mammal and that of its average diet
allow a better quantification of the relationship (e.g. DeNiro & Epstein, 1978, 1981; Ambrose &
between the isotopic composition of a consumer Norr, 1993; Tieszen & Fagre, 1993; Roth &
and that of its average diet (e.g. Bocherens & Hobson, 2000; Jenkins et al., 2001). The differ-
Drucker, 2003b). Due to these improvements in ence between the isotopic signature of an animal
isotopic ecology, it is possible to attempt more tissue and that of its average diet is subject to
Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
164 D. Drucker and H. Bocherens

some variation (e.g. Hare et al., 1991; Hilderbrand savannahs and forests, due to the lack of plants
et al., 1996; Hobson et al., 1996; Ambrose, 2000). using the C4 photosynthetic pathway. However,
A review of published enrichment values in some carbon isotopic variability has been evi-
experimental conditions yields a range of 3.7 to denced in herbivores according to their taxon.
6.0% for 13C values between diet and collagen, Mammoths exhibit the most negative 13C values
and a range of 1.7 to 6.9% for 15N values (see when compared to horse and woolly rhinoceros,
review in Bocherens & Mariotti, 2002). A recent while bovines, and to a greater extent reindeer,
study using modern wild mammals from Bialo- present more positive 13C values than all the
wieza Primeval Forest in Poland produced an other ungulates (Bocherens et al., 1996, 1997;
accurate range of variations for isotopic fractio- Drucker et al., 2000; Iacumin et al., 2000;
nation in carbon and nitrogen between a predator Bocherens, 2003). This pattern is observed over
collagen and that of its prey (Bocherens & a large geographical area, from France to Alaska,
Drucker, 2003b). These data, together with addi- and is interpreted as reflecting dietary adaptation
tional data from ancient terrestrial ecosystems, of the different herbivorous taxa (supra). For
have allowed to propose an enrichment of 0.8 to instance, reindeer was consuming large amounts
1.3% for 13C values and an enrichment of 3 to of 13C-enriched lichens, whereas mammoth,
5% for 15N values between the collagen of a horse and rhinoceros were mostly relying on
predator and that of its average prey. Knowing tall grass with 13C-depleted content (e.g.
the carbon and nitrogen isotopic signatures of a Drucker et al., 2000; Bocherens, 2003). The
predator’s collagen, such enrichment values allow 15N values of herbivore collagen also present
us to calculate the expected 13C and 15N variations between co-occurring taxa (Bocherens
collagen values of the average prey consumed et al., 1996, 1997; Drucker et al., 2000; Iacumin
by a given predator, including Neanderthals and et al., 2000; Bocherens, 2003). The inter-specific
prehistoric humans of modern type. A compar- variations in herbivore 15N values reflect the
ison of the collagen isotopic signatures of poten- variations in plants such as grass and different
tial prey available to the predator and that types of shrubs with symbiotic mycorhizes in
deduced from the predator itself should lead to their roots (see detailed discussion in Bocherens,
quantitative estimates of the consumption of 2003). The consequence of this situation is that
different types of prey using mixing models or different herbivores available to predators as prey
at least it should allow the consumption of given exhibit carbon and nitrogen isotopic signatures
prey to be tested. that are sufficiently distinct for them to be
considered as different food resources in an
isotopic, palaeoecological study. This was the
What are the isotopic signatures of mammal case for the Neanderthal from Saint-Césaire
fauna associated with fossil humans? relative to the isotopic composition of potential
prey species, as documented by analyses per-
The main prey species found in Middle Palaeo- formed on bone samples from three contempor-
lithic sites are large ungulates, such as the horse ary sites in the same area, i.e. Saint-Césaire, La
(Equus sp.), bovines (Bos or Bison spp.), woolly Berbie and Camiac (Table 1).
rhinoceros, (Coelodonta antiquitatis), woolly mam-
moth (Elephas primigenius), reindeer (Rangifer taran-
dus) and red deer (Cervus elaphus) (e.g. Patou, 1989; How much isotopic variation is
Webb, 1989; Dibble & Rolland, 1992; expected chronologically?
Baryshnikov & Hoffecker, 1994). A very diverse
assemblage of intermediate to large herbivores Variations of isotopic signatures in the collagen
was dwelling on the European continent during of a given species through time have been docu-
MOIS 3 (e.g. Vereshchagin & Baryshnikov, 1982; mented in Europe, especially for 15N values
Guthrie, 1990). The vegetation reconstructed for (Fizet et al., 1995; Iacumin et al., 1997; D. Drucker,
this period does not present large isotopic con- unpublished PhD dissertation, 2001; Drucker et al.,
trasts such as those observed in modern tropical 2003b, in press; Richards & Hedges, 2003). For
Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth 165
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 SD 15N SD

Reindeer 7 19.1 0.4 5.8 1.7

Bovine (Bos or Bison) 15 20.4 0.3 6.0 1.0
Horse 6 20.8 0.5 5.7 1.5
Rhinoceros 5 20.2 0.5 7.0 1.1
Mammoth 3 21.6 0.3 8.3 0.5

the area and period under consideration here, it is (2003b). These ranges fall close to the isotopic
not possible to provide a detailed isotopic curve signatures of potential herbivorous mammal prey,
of bone collagen 15N values for a given species. when such values are available for comparison.
The isotopic variations prior to 40,000 years BP Globally, the 15N values of Neanderthals are
are very unclear due to difficulties dating collagen slightly more positive than those of coeval pre-
older than that age. Richards & Hedges (2003) dators, such as wolves and hyaenas (Figure 1).
published a preliminary trend for four herbivore One difference between the meat consumed by
species in northwestern Europe as a whole, which Neanderthals and that consumed by animal pre-
suggests more positive 15N values around dators is cooking, which is usually performed by
30,000 years BP relative to samples of younger Neanderthals but not by animal predators. It is
age. For instance, 15N values increase up to questionable whether cooking can lead to
around 10% for bovine collagen by 30,000 years changes in the isotopic signatures of meat prior
BP, whereas they drop to 6% around 28,000 BP to its consumption by humans. Bonsall et al.
(Figure 3 in Richards & Hedges, 2003). The case (1997) report that cooking has very little effect
for high 15N values in mammal herbivores on 15N values, but do not provide any actual
around 30,000 years BP is confirmed by the data. Cooking experiments conducted by
isotopic signatures obtained on several taxa Katzenberg and colleagues (2000) demonstrate
from the site of Castanet in southwestern France, small effect of heating on 13C values of vege-
where reindeer and horse 15N values range from tables (less than 1.2%) and meat (no more than
8.4 to 10.3% (Drucker, in press). In a previous 0.1%). We have performed a few basic experi-
work, we suggested a relationship between the ments on cooked meat and fish (D. Drucker,
15N values of terrestrial mammals and the rate of unpublished PhD dissertation, 2001), The change
nitrogen cycling in soils influenced by the inten- in 15N values range from 0.4 to þ0.2%
sity of glacial conditions (Drucker et al., 2003a, (Table 2), which is negligible when compared to
2003b). These patterns of variability seem to be the variation observed between specimens of the
reliable for northern and western Europe, but not same species in a given site. Experiments using well
for Mediterranean areas (Iacumin et al., 1997; monitored cooking techniques based on ethnolo-
Richards & Hedges, 2003). 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
Quantitative estimate of the prey 15N values of meat consumed by humans.
consumed by Neanderthals In the case of Saint-Césaire, located in Char-
entes-Maritimes (France), it is possible to go
Four different sites of MOIS 3 age produced one step further thanks to the large dataset
isotopic signatures of Neanderthal collagen of analysed potential prey. Indeed, isotopic
(Figure 1). The range of isotopic signatures of measurements have been carried out on herbivor-
average prey are presented on the figure, using ous mammals from the same layer as the Nean-
the range of isotopic fractionations for 13C and derthal specimen (layer Ejop sup in Saint-Césaire),
15N established by Bocherens & Drucker and on specimens of large mammals from two
Copyright # 2004 John Wiley & Sons, Ltd. 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 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-
Figure 2. Application of the mixing model proposed by
Phillips & Koch (2002) to Neanderthals and hyaenas from mal predators such as hyaena suggest that prey
Saint-Césaire, Camiac and La Berbie. The triangle repre- with elevated 15N values, such as woolly mam-
sents the possible isotopic values of mixtures of three moth and woolly rhinoceros, constituted a larger
dietary poles (horse/bovine, reindeer, mammoth). The
rectangles stand for the possible isotopic values of part of the Neanderthal diet relative to smaller
average prey consumed by Neanderthals and hyaenas, ungulates such as horse or reindeer than they did
using the range of isotopic fractionations presented by for carnivores such as hyaena. Zooarchaeological
Bocherens & Drucker (2003b).
evidence also points to the procurement of meat
from these large herbivores in Europe in some
additional sites from the same area, i.e. Camiac Middle Palaeolithic sites (e.g. Auguste, 1995;
and La Berbie, both roughly contemporary with Auguste et al., 1998; Conard & Prindiville, 2000;
the Ejop sup layer of Saint-Césaire, dated to Weber, 2000; Moncel, 2001). When sufficient
around 36,000 BP ( J. L. Guadelli, unpuhlished isotopic data are available for the potential prey
PhD dissertation, 1987; Mercier et al., 1993; S. of Neanderthals and for coeval animal predators,
Madelaine, unpublished report). In this case, we the isotopic approach, using mixing models with
have used the mixing model presented by Phillips the proper fractionation factors, is thus able to
& Koch (2002), but taking into account the test different scenarios of prey consumption by
variability of isotopic fractionation for 13C and humans and animal predators, in view of the
15N values (Bocherens & Drucker, 2003b). zooarchaaeological evidence.
Using the average isotopic values for potential
prey (presented in Table 1), hyaena and Nean-
derthal, we calculate the ranges of percentages of Do isotopic data indicate that
different prey compatible with the observed iso- anatomically modern humans of Early
topic composition for Neanderthal and for hyae- Upper Palaeolithic consumed
nas (Figure 2). This calculation is performed using diversified dietary resources, such
the spreadsheet, which is available at http:// as marine and freshwater food items? (Phillips &
Koch, 2002), for the whole range of possible Recent isotopic data published by Richards
values intercepting the triangle of potential prey et al. (2001b) for Early Upper Palaeolithic
Copyright # 2004 John Wiley & Sons, Ltd. 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

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

1990), and only a handful of Early Holocene the isotopic fractionation between predator and
material has been investigated (Bonsall et al., prey collagen proposed by Bocherens & Drucker
1997). As a matter of fact, Richards and collea- (2003b). The results of this calculation are pre-
gues (2001b) used as reference a mixture of sented in Table 4 with a review of the available
published values for modern fish, mainly from isotopic data obtained on aquatic resources from
lakes, and isotopic values from Early Holocene temperate and peri-arctic environments in ancient
material. Unfortunately, most of the studied Europe. The range of 13C values is large, from
modern freshwater ecosystems are located in 25.2 to 19.8% and the 15N values range
North America (e.g. Rau, 1980; Fry, 1991; between 6.5 and 10.7%, with no clear pattern
Hesslein et al., 1991; Beaudoin et al., 1999) and relative to species, age and location.
have suffered from significant anthropic disrup- Our reassessed 13C values of freshwater
tions (e.g. Vander Zanden et al., 1999). Hence, resources are similar to those used by Richards
the derived isotopic data are not necessarily and colleagues. Obviously, the 13C enriched
suitable as reference datasets for the prehistoric human collagen is unlikely explained by a large
period in Europe. Indeed, studies demonstrate contribution of this 13C depleted food item. The
the high variability of stable isotope ratios for 15N values presented in Table 4 are less positive
freshwater fish since aquatic plants have access to than those published by Richards and colleagues
different sources of caron dioxide (CO2) and (2001b), which ranged from 10.7 to 13.2%. The
fishes experience different habitat and trophic selection performed by Richards et al. was
level, even during their own lifetime (e.g. strongly biased towards lacustrine specimens,
Katzenberg & Weber, 1999). which seem to present more positive 15N values
This situation led us to perform new collagen than riverine specimens, while the data presented
extractions and isotopic analyses on ancient in this study are only for river specimens. This
freshwater material. We carried out isotopic new assessment of the isotopic values of fresh-
analysis on fish and otter (Table 3) from two water resources shows that they are not necessa-
French archaeological sites that yielded abundant rily so 15N enriched compared to terrestrial
aquatic material: Pont d’Ambon (Dordogne, resources.
13,000 to 9,500 years BP: Célérier, 1998) and Reassessments of the isotopic signatures of
Noyen-sur-Seine (Seine-et-Marne, around freshwater resources available to prehistoric
8,000 BP: Marinval-Vigne and Mordant, 1989). humans indicate that they represent a dietary
Otter collagen isotopic signatures represent a source with less positive 13C values and 15N
pure freshwater feeder and allow us to deduce the values than assumed by Richards et al. (2001b).
carbon and nitrogen isotopic composition of its The addition of some marine resources, which
prey. The calculation has been performed using 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  g1 % 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 7,0008,500 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 7,0008,500 BP (2)
Average  sd 22.2  1.9 8.1  1.4
Unknown anadromous Danube 1 River/Marine 15.7 12.9 7,0008,500 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 marine (anadromous or migratory) and riverine
Columbia, Canada (Lovell et al., 1986). These resources could explain the isotopic signatures of
resources are 13C and 15N enriched relative to prehistoric humans, but such combinations
terrestrial food resources (Table 4). A mixture of should be established using zooarchaeological
Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
172 D. Drucker and H. Bocherens

evidence in the studies sites, which is beyond the measured on terrestrial mammal collagen are as
scope of this paper. different as about 4% between the two archae-
To complete the dietary reconstructions of ological contexts. As a result, contemporaneous
modern human, we added the isotopic data of terrestrial resources exhibit 15N values too low
terrestrial mammals. As an isotopic shift of 15N for contributing alone to the isotopic signature of
values of terrestrial mammals collagen is observed the humans in Iron Gates, whereas, in they can
through time (Richards & Hedges, 2003; Drucker easily explain the 15N value measured on the
et al., 2000, 2003b), we selected terrestrial mam- human of Kostenki.
mals remains from contemporaneous sites from
Europe (Figure 4). It appears that the 13C values
of terrestrial mammal collagen are more positive Conclusions
than those of freshwater fish collagen. Taking
into account the isotopic difference in collagen The isotopic reconstruction of prehistoric human
between a predator and its prey, the 13C values diet raises several difficulties. First, the evaluation
of coeval fauna fit the expected 13C values of of the isotopic enrichment linked to trophic
averaged prey collagen, values deduced from relationship provides a range of values rather
anatomically modern human isotopic signature than an accurate figure. As a result, it enlarges
(Figure 4). The 15N of terrestrial mammals are the possible sources of food, and more specifi-
within a similar range in the case of the new cally the source of protein as far as collagen is
estimate for river resources, especially when concerned. Second, the isotopic signature of
mammoth is considered (Figure 4). protein resources for human can be subject to
Considering this updated estimate, obligate chronological evolution. Hence, it is sometimes
implication of freshwater resources in human imperative to have access to the coeval fauna for
diet is not so convincing. Although we do not isotopic analysis in order to correctly evaluate the
exclude any fish consumption, we consider that signatures of protein resources. Lastly, consider-
contemporaneous terrestrial resources are suffi- ing zooarchaeological evidence is crucial when
cient to explain the isotopic signature of anato- isotopic study leads to equally probable scenar-
mically modern humans. This conclusion is also ios. When ideal conditions are reached (isotopic
sound as far as Neanderthals are concerned. analysis of human and coeval fauna selected
The hypothesis of a strong trophic relation- through zooarchaeological study), it proves
ship between terrestrial mammals and humans is useful to apply a quantitative diet estimate to
reinforced by the stability of their 15N differ- decipher food sources reliance.
ence (Figure 5). This stability is significant as 15N On the basis of isotopic data accumulated to
amounts of terrestrial herbivores exhibit impor- date, the following conclusions can be presented.
tant changes through time. In particular, a dra- The current isotopic data obtained on Early
matic increase of the 15N values is found around Upper Palaeolithic anatomically modern humans
35,000–32,000 years BP for herbivores as well as can be interpreted as reflecting the consumption
for terrestrial animal predators. In this context, of protein provided by meat of terrestrial herbi-
the high 15N value of the individual of Kostenki vores and do not necessarily require the addition
1 (dated to 32,600  1100 BP OxA 7073) com- of significant amounts of freshwater fish. A similar
pared to the Neanderthals, from Marillac, Wal- conclusion can be inferred for Neanderthals. This
lonia and southwestern France, is consistent with interpretation, based on the isotopic tracking of
the general isotopic shift observed in terrestrial protein origin through collagen, does not pre-
ecosystems. This case illustrates how a difference clude some consumption of plant material since
of isotopic signature between humans can finally this last dietary resource would provide much less
lead to the same dietary interpretation. On the protein than meat for a similar dry weight con-
contrary, the same 15N values of Kostenki 1 and sumption. If confirmed, the similar importance of
Iron Gates humans cannot result from the same exploitation of the terrestrial resources for Nean-
diet characteristics. Indeed, the mean 15N values derthals and the first anatomically modern human

Copyright # 2004 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 14: 162–177 (2004)
Stable Isotopes and Diet Breadth 173

in Europe, leads to the possibility of a direct Vaast (Pas-de-Calais). Bulletin de la Société Préhistorique
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