International Journal of Osteoarchaeology
Int. J. Osteoarchaeol. 13: 46–53 (2003)
Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/oa.662
Trophic Level Isotopic Enrichment of
Carbon and Nitrogen in Bone Collagen:
Case Studies from Recent and Ancient
Terrestrial Ecosystems
H. BOCHERENS* AND D. DRUCKER
Laboratoire de Paléontologie, Institut des Sciences de l’Evolution, Université Montpellier 2,
Montpellier, France
ABSTRACT
Prey-predator collagen enrichment values for carbon and nitrogen isotopic compositions are
investigated. New enrichment values are given for the well-monitored ecosystem of Bialowieza
primeval forest (Poland) for lynx and wolf. The impact of using different approximations in
calculating such enrichment values is discussed. Several case studies of ancient vertebrate
communities from Upper Palaeolithic sites in southwestern France are presented to check
whether the enrichment values estimated for these past ecosystems are consistent with those
measured in well-monitored modern ecosystems. The use of ranges of values rather than
average ones is recommended, tentatively 0 to 2‰ for δ 13 C and 3 to 5‰ for δ 15 N. Copyright
 2003 John Wiley & Sons, Ltd.
Key words: collagen; carbon-13; nitrogen-15; mammals; trophic level
Introduction
The carbon and nitrogen isotopic compositions
of collagen provide a proxy to reconstruct ancient
trophic webs, and especially to decipher the relationships between predators and their potential
prey. Indeed, numerous studies performed under
controlled conditions have shown that there is a
quantitative relationship between the carbon and
nitrogen isotopic compositions 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;
Hilderbrand et al., 1996; Ambrose, 2000; Roth &
Hobson, 2000; Jenkins et al., 2001).
Mathematical models have been developed in
order to quantify the contribution of different
* Correspondence to: Laboratoire de Paléontologie, Institut des Sciences de l’Evolution, UMR 5455 du CNRS, Université Montpellier
2, case courrier 064, Place Eugène Bataillon, F-34095 Montpellier
cedex 05, France.
Copyright  2003 John Wiley & Sons, Ltd.
food resources in the diet of a given specimen,
using its stable isotopic composition (e.g.,
Schwarcz, 1991). The most recent progress with
these models has been to introduce the concentration of carbon and nitrogen in the food resources
instead of using linear mixing models, and to take
into account the uncertainty of the isotopic composition of the food resources (e.g., Phillips, 2001;
Phillips & Greg, 2001; Koch & Phillips, 2002;
Phillips & Koch, 2002). However, these newest
models still use the canonical value of 3‰ as the
value for the trophic enrichment of δ 15 N values.
Numerous studies have shown that this value is
variable in dietary experiments (e.g., Hare et al.,
1991; Hilderbrand et al., 1996; Hobson et al., 1996;
Ambrose, 2000), and this is also a key parameter that needs to be well constrained in order to
make the models even more reliable for dietary
and palaeodietary reconstructions. A review of
published enrichment values under experimental
conditions yields a range of 3.7 to 6.0‰ for δ 13 C
Accepted 25 September 2002
Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen
values between diet and collagen, and a range of
1.7 to 6.9‰ for δ 15 N values (Bocherens & Mariotti, 2002). Taking such a large range into account
in the models would lead to large uncertainties in
the quantifications of dietary resources.
In this paper, we evaluate the enrichment values
deduced from collagen isotopic compositions
of prey-predator pairs. Collagen presents the
advantage of averaging the isotopic composition
of the diet over long time periods. In the case of
predators, which consume mostly vertebrate prey,
the difference between the isotopic composition
of their collagen and that of their prey directly
reflects the isotopic enrichment linked to a trophic
step. Moreover, collagen can be preserved in
ancient bones, thus it opens the possibility to
check the presumed trophic link between prey
and predator in the past.
However, few studies have been published
on closely monitored modern faunas with welldefined terrestrial mammalian predators and their
possible prey in wild contexts (Table 1). Only
five cases meeting these criteria could be found,
and even if we missed a few, this is a low
number relative to the total number of trophic
isotopic enrichment studies performed to date.
The difference between the isotopic values of
prey and predator collagen range from 1.2 to
2‰ and from 2.4 to 4.8‰, for carbon and
nitrogen respectively. It is noteworthy that such
studies usually consider one species of prey as the
main prey and neglect the contributions of other
possible prey (e.g., Schwarcz, 1991; Szepanski
et al., 1999). This uncertainty may affect the actual
enrichment value in these studies.
Due to this small number of studies and
to these uncertainties regarding actual preypredator relationships, a detailed study has
47
been performed on the well-monitored large
mammals from the Bialowieza primeval forest in
Poland. These data will be used to discuss how
trophic enrichments can be calculated. Secondly,
case studies from Upper Palaeolithic sites in
southwestern France will be presented to verify
that predators from Late Pleistocene ecosystems
present enrichment values consistent with those
measured in modern ecosystems.
A case study in a well-monitored
modern ecosystem: Bialowieza
primeval forest
Bialowieza primeval forest is the last terrestrial
habitat in Europe that includes a suite of large wild
mammals and it is probably one of the most thoroughly studied ecosystems. In particular, data are
available on the relative contribution of each prey
species to each predatory species (Jedrzejewska
& Jedrzejewski, 1998), permitting a quantitative
estimation of the isotopic enrichment.
The studied bone material belongs to two
predator species, boreal lynx (Lynx lynx) and
wolf (Canis lupus) and their main prey, which
are ungulates such as red deer (Cervus elaphus),
roe deer (Capreolus capreolus), and wild boar (Sus
scrofa). The specimens died between 1959 and
1999, and the year of death has been recorded for
each specimen. During this 40-year period, the
δ 13 C value of atmospheric CO2 has shifted from
around −7.5‰ (Friedli et al., 1986) to −8.5‰
(extrapolating the exponential trend proposed by
Feng, 1998). Such a difference is not negligible
when calculating the difference between the
carbon isotopic composition of prey and predator
Table 1. Previously published isotopic enrichments between collagen of predators and their main prey in modern ecosystems
Site
South Africa (C3 )
Ontario (Canada)
Ontario (Canada)
Interior Alaska (USA)
East Africa
Predators (n)
Prey (n)
Lynx, jackal
Wolf (10)
Coyote (15)
Wolf (50)
Carnivorous mammals (15)
Hare, antelope
Deer (16)
Deer (19)
Caribou (41)
Herbivorous mammals (193)
13 C∗ 15 N∗
Predator—prey
∼2†
1.2
2.9
2.7
2.4
4.8
References
Van der Merwe (1989)
Schwarcz (1991)
Schwarcz (1991)
Szepanski et al. (1999)
Ambrose & DeNiro (1986)
∗ is isotopic enrichment between two taxa or tissues. 13 C
13
13
15
predator-prey = δ Cpredator − δ Cprey . Npredator-prey is
defined similarly.
† Value was not measured directly but was calculated using carnivore collagen-herbivore meat and herbivore collagen-herbivore meat .
Copyright  2003 John Wiley & Sons, Ltd.
Int. J. Osteoarchaeol. 13: 46–53 (2003)
48
H. Bocherens and D. Drucker
collagen. Consequently, it has been necessary to
set the δ 13 C values of each specimen to a similar
atmospheric δ 13 C value before calculating the
enrichment value between the carbon isotopic
composition of prey and predator collagen. A
correction factor for each specimen has been
designed using the formula presented by Feng
(1998) and modified in order to obtain a δ 13 C
value of −7‰ for atmospheric CO2 , which is the
average value for atmospheric CO2 during Upper
Pleistocene times (Leuenberger et al., 1992). The
modified correction formula is: 13 C = −7 −
(−6.429 − 0.0060e0.0217(t−1740) ), where t is years
AD. This correction ranges from 0.1‰ for
specimens killed in 1959 to 1.1‰ for specimens
killed in 1999. Taking into account this type of
correction will become more crucial in the future
studies since the isotopic shift of atmospheric
CO2 is due to increase.
We compare estimates produced by different
methods for calculating prey-predator isotopic
differences, including fairly crude methods typically used in studies of this sort (Tables 2
and 3). One estimate is based on a ‘virtual’
prey that has an average isotopic value with
an equal contribution of each ungulate species.
Another estimation is performed comparing collagen isotopic compositions of each predator and
that of its main prey. Finally, the most realistic
estimate is provided by a detailed calculation
Table 2. Calculation of average prey per cent biomass for wolves from faeces and isotopic enrichment values between years 1986
and 1996 in Bialowieza forest
Taxon (n)
Medium-sized mammals
Boar—Sus scrofa (4)
Red deer—Cervus elaphus (6)
Roe deer—Capreolus capreolus (5)
Cervids (80% red deer, 20% roe deer)*
Weighted average of ungulates
Wolf—Canis lupus (5)
wolf-red deer
wolf-1/3 each ungulate
wolf-weighted average of ungulates
% biomass in faeces % biomass in diet δ 13 C mean δ 13 C sd δ 15 N mean δ 15 N sd
1.5
14.7
16.5
3.1
62.3
1.5
14.7
66.3†
15.6†
−21.1
−23.1
−23.3
0.4
0.9
0.6
1.9
2.7
2.1
0.7
0.9
1.8
−22.8
−21.8
1.3
0.7
1.0
0.8
0.5
2.5
6.1
3.4
3.9
3.6
1.0
0.3
∗
Proportions of red deer and roe deer in unidentifiable cervid remains from wolf faeces have been deduced from the proportions
of each cervid species amongst carcasses of wolf kills during the same period. Data are from Jedrzejewski et al. (2000).
† % red deer and roe deer in diet is calculated by adding estimated % roe and red deer in unidentifiable cervid remains in faeces
to % roe and red deer in identifiable remains in faeces.
Table 3. Calculation of average prey per cent biomass for lynx from faeces and isotopic enrichment values between years 1986
and 1996 in Bialowieza forest
Taxon (n)
Boar—Sus scrofa (4)
Red deer—Cervus elaphus (5)
Roe deer—Capreolus capreolus (5)
Cervid (26% red deer, 74% roe deer)∗
Other (mostly hare)
Weighted average of ungulates
Lynx—Lynx lynx (4)
lynx-roe deer
lynx-1/3 each ungulate
lynx-weighted average of ungulates
% biomass in faeces
% biomass in diet
δ 13 C mean
δ 13 C sd
δ 15 N mean
δ 15 N sd
0.5
5.9
12.7
73.1
7.8
0.5
24.9†
66.8†
−21.1
−23.1
−23.3
0.4
0.9
0.6
1.9
2.7
2.1
0.7
0.9
1.8
−23.2
−22.1
1.2
0.4
1.1
0.7
0.3
2.3
6.3
4.2
4.1
4.0
1.5
0.4
7.8
∗
Proportions of red deer and roe deer in unidentifiable cervid remains from lynx faeces have been deduced from the proportions
of each cervid species amongst carcasses of lynx kills during the same period. Data from Jedrzejewski et al. (2000).
† % red deer and roe deer in diet is calculated by adding estimated % roe and red deer in unidentifiable cervid remains in faeces
to % roe and red deer in identifiable remains in faeces.
Copyright  2003 John Wiley & Sons, Ltd.
Int. J. Osteoarchaeol. 13: 46–53 (2003)
Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen
performed using the relative contribution of each
prey species to each predatory species, based on
ecological reports.
The ecological data show that for both predators, one prey species dominates the biomass of
the consumed prey (∼66%), i.e. red deer for
wolf and roe deer for lynx (Okarma et al., 1997;
Jedrzejewski et al., 2000). When the three main
ungulate species (boar, roe deer and red deer)
are considered, more than 90% of the diet of
each predator is taken into account (Table 2).
For estimates in which the three ungulate prey
species are considered to contribute equally to the
predator’s diet, the contribution of boar is highly
over-represented, especially for lynx, and the contribution of the main species is under-represented.
Estimates that consider only the main prey species
for each predator are more realistic ecologically,
and this is the method that is usually followed in
previously published work (e.g., Schwarcz, 1991;
Szepanski et al., 1999). Finally, the most accurate
analysis considers the contribution of each species
following the percentage in consumed biomass as
determined by ecological studies. The difference
between the estimates given by the first method
(one third of each ungulate) relative to the second
method (only main prey) is larger than between
the second method relative to the third (based on
the actual contribution of each prey). In the case
of nitrogen enrichment values of lynx, all three
approaches give very similar results, with a maximum difference of only 0.2‰, which is within
the range of analytical error. In conclusion, the
enrichment values obtained using the most precise approach are similar for wolf and lynx, 1.0
and 1.1‰ for δ 13 C and 3.6 and 4.0‰ for δ 15 N
respectively. In the case of a predator with a main
prey species that contributes more than 50% in
biomass with isotopic signatures relatively close
to those of other prey, the quantitative estimation
of enrichment values based on the main species is
a satisfactory approximation.
These results emphasize the importance of
using ranges of enrichment values rather than
an average figure deduced from a review of
the published data. In most cases, ecological
data as detailed as in the Bialowieza primeval
forest will not be available, especially for past
ecosystems. Thus using a relatively wide range of
isotopic enrichments will compensate for errors
Copyright  2003 John Wiley & Sons, Ltd.
49
linked to the uncertainties inherent to enrichment
calculations, even in modern ecosystems. The
problem is to define the extreme values of
the range of enrichment values. The commonly
quoted ranges for enrichment values of 0 to
2‰ for carbon and 3 to 5‰ for nitrogen seem
reasonable compared to the enrichment values
estimated in the present paper.
In the case of past ecosystems with no
analogues in modern environments, such as
those of the last glacial period (e.g., Guthrie,
1982), a first step before using this range of
values in modelling approaches is to verify that
such a range is consistent with the observed
data. We thus tried to investigate isotopic
enrichment between predators and their likely
prey for Upper Pleistocene western European
sites. In this context, most of the available faunal
remains are coming from archeological sites, in
which the main accumulation factor is human
activity. In such cases, comparing predator and
prey isotopic compositions is complicated by
two factors: (1) the possible bias between the
natural environment and the selection of animals
by humans, and (2) the fact that the relative
abundance of different prey species is not due
to the animal predator activity. Keeping these
complications in mind, we present some examples
of such studies in chosen sites from southwestern
France, dating from the Late Glacial Maximum.
Case studies from Upper Palaeolithic
sites in southwestern France
Three archeological sites, which range in age
from 19,000 to 16,000 BP, have yielded faunal
assemblages including predators and their likely
prey and have been the object of isotopic
investigations (Drucker, 2001). This context
is favourable to the application of isotopic
methodology, due to the good preservation of
bone collagen and to the occurrence of different
prey species that can be distinguished through
their carbon and nitrogen isotopic compositions,
such as reindeer versus horse (Fizet et al., 1995;
Drucker et al., 1999, 2000a). The chosen layers
are the Solutrean level from Les Jamblancs
(around 19,000 BP; Drucker et al., 2000b), the
Solutrean level from Combe-Saunière (around
Int. J. Osteoarchaeol. 13: 46–53 (2003)
50
H. Bocherens and D. Drucker
19,000 BP; Geneste & Plisson, 1986), and the
Middle Magdalenian layer from Saint-Germain
la Rivière (around 16,000 BP; Lenoir, 2000).
Samples from wolf and from the different ungulate
species have been selected in Les Jamblancs
and Saint-Germain-la-Rivière, while samples from
rodents (ground squirrel Citellus superciliosus) and
lagomorphs (hare Lepus timidus) have been sampled
from Combe Saunière 1 together with snowy
owl (Nyctea scandiaca). This last site offers the
opportunity to study a situation where small
mammals are the preferred prey. Indeed, modern
snowy owls consume mostly rodents, such as
lemmings, but also other kind of rodents and even
arctic hares (Paquin & David, 1993).
Collagen has been extracted from bone powders according to Bocherens et al. (1991). All
extracts have been checked for carbon and nitrogen content and C/N ratios in order to investigate
chemical purity. All extracts that contain less
than 10% nitrogen and C/N ratios outside a
range of 2.9–3.6 are not included in the discussion, since their isotopic composition may have
been shifted due to diagenetic alteration (DeNiro,
1985; Ambrose, 1990). Only results from adult
bones have been considered, since the nitrogen
isotopic composition of juvenile specimens can
be influenced by the consumption of milk from
their mother (e.g., Fogel et al., 1989; Hobson et al.,
1996). Moreover, teeth have been avoided systematically for herbivores (except horse) and as
much as possible for carnivores, since this tissue exhibits isotopic differences with bone of
the same individual that can interfere with the
trophic determinations (Bocherens et al., 1994,
1995; Bocherens & Mariotti, 1997).
Table 4. Estimates for isotopic enrichment between collagen
of wolf and its potential prey in the ancient ecosystem of Les
Jamblancs (Solutrean layer ∼19,000 BP). Data are from Drucker
et al. (2000b)
Taxon (n)
δ 13 C
mean
δ 13 C
sd
δ 15 N
mean
δ 15 N
sd
Horse—Equus sp. (4)
Reindeer—Rangifer tarandus (5)
Red Deer—Cervus elaphus (1)
Bovine—bos or bison (3)
Average herbivores
Wolf—Canis lupus (tooth) (1)
wolf-herbivores
−21.1
−19.6
−20.3
−19.9
−20.2
−18.9
1.3
0.2
0.1
2.4
3.9
2.6
4.7
3.4
8.9
5.5
0.9
1.1
0.1
Copyright  2003 John Wiley & Sons, Ltd.
0.4
Table 5. Estimates for isotopic enrichment between collagen of
wolf and its potential prey in the ancient ecosystem of SaintGermain-la-Rivière (Middle Magdalenian layer ∼16,000 BP).
Data are from Drucker (2001)
Taxon (n)
δ 13 C
mean
δ 13 C
sd
δ 15 N
mean
δ 15 N
sd
Horse—Equus sp. (3)
Saiga—Saiga tatarica (11)
Reindeer—Rangifer tarandus (3)
Bovine—bos or bison (3)
Average herbivores
Wolf—Canis lupus (1)
wolf-herbivores
−21.0
−19.6
19.1
−20.1
−19.9
−19
0.9
0.1
0.3
0.0
0.0
4.2
4.0
3.5
5.5
4.3
8.7
4.4
0.2
0.5
0.3
0.5
Table 6. Estimates for isotopic enrichment between collagen of
snowy owl and its potential prey in the ancient ecosystem of
Combe-Saunière I (Solutrean layer ∼19,000 BP). Data are from
Drucker (2001)
Taxon (n)
δ 13 C
mean
δ 13 C
sd
δ 15 N
mean
δ 15 N
sd
Hare—Lepus timidus (4)
Ground
squirrel—Citellus
superciliosus (5)
Average prey
Snowy owl—Nyctea
scandiaca (7)
owl-prey
−20.2
−20.9
0.4
0.4
2.3
1.9
0.7
0.9
−20.6
−19.8
0.2
2.1
5.1
0.6
0.8
3.0
The average isotopic signatures of the specimens are presented in Tables 4–6. Since modern
wolf feeds mainly on large ungulates (Mech,
1970), the calculation for average prey isotopic
signatures is performed considering an equal contribution of each ungulate species. The estimated
enrichment values are 0.3 and 0.9‰ for carbon and 5.5 and 4.4‰ for nitrogen in Les
Jamblancs and Saint-Germain-la-Rivière respectively (Tables 4 and 5). The 5.5‰ enrichment
value for nitrogen in Les Jamblancs is estimated
from collagen extracted from a tooth; this value
can be corrected using the enrichment observed
between dentine and bone δ 15 N values of modern individual wolf, which range from 1.6 to
2.1‰ (Bocherens, 1992, 2000). The estimated
15 N-enrichment value between this fossil wolf
and its potential prey is between 3.4 and 3.9‰.
In the case of snowy owl, the enrichment values are 0.8 and 3.0‰ for carbon and nitrogen
respectively (Table 6).
These examples show that the ranges of
enrichment values estimated from archeological
Int. J. Osteoarchaeol. 13: 46–53 (2003)
Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen
site faunas are consistent with those measured
in the studied modern ecosystems. This is
encouraging for the future use of modelling
approaches in Upper Pleistocene ecosystems
using this range of enrichment values.
Conclusions
Recent improvements in modelling approaches
have allowed significant progress in the dietary
reconstruction in modern ecosystems. No doubt
these approaches will provide very fruitful information on past ecosystems as well. However, one
factor that remains under-determined is the range
of variation in carbon and nitrogen enrichment
values between a predator and its average food.
Taking into account this additional uncertainty
in modelling approaches will decrease the precision of the obtained figures, which is frustrating
but unavoidable. Further work is thus necessary
in order to better understand if environmental or
physiological parameters can explain some of this
range. This point should progress when investigations involving experimentally designed trophic
situations and well-monitored ecosystems are performed on the species of interest for palaeodietary
reconstructions.
Acknowledgements
Most specimens have been kindly provided by
the Mammal Research Institute of Bialowieza
(E. Szuma), except for one red deer specimen,
provided by the Museum d’Histoire Naturelle
of Paris (M. Mashkour and E. Pellé). We thank
the Musée National de Préhistoire (Les Eyzies
de Tayac) and the Institut de Préhistoire et de
Géologie de Quaternaire (University Bordeaux 1)
for authorization to study ancient material. Many
thanks are due to Daniel Billiou for his assistance
in analysing the collagen at the Laboratoire
de Biogéochimie Isotopique (University Paris
6). The investigations of Upper Palaeolithic
faunas were financially supported by the PEH
programme of the CNRS. We are grateful to
Dr Paul Koch and two anonymous reviewers
for valuable comments on an earlier version of
this manuscript.
Copyright  2003 John Wiley & Sons, Ltd.
51
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