Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Bone Collagen: Case Studies from Recent and Ancient Terrestrial Ecosystems
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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 food resources in the diet of a given specimen,
using its stable isotopic composition (e.g.,
The carbon and nitrogen isotopic compositions Schwarcz, 1991). The most recent progress with
of collagen provide a proxy to reconstruct ancient these models has been to introduce the concentra-
trophic webs, and especially to decipher the rela- tion of carbon and nitrogen in the food resources
tionships between predators and their potential instead of using linear mixing models, and to take
prey. Indeed, numerous studies performed under into account the uncertainty of the isotopic com-
controlled conditions have shown that there is a position of the food resources (e.g., Phillips, 2001;
quantitative relationship between the carbon and Phillips & Greg, 2001; Koch & Phillips, 2002;
nitrogen isotopic compositions of the tissues of Phillips & Koch, 2002). However, these newest
a given terrestrial mammal and that of its aver- models still use the canonical value of 3‰ as the
age diet (e.g., DeNiro & Epstein, 1978, 1981; value for the trophic enrichment of δ 15 N values.
Ambrose & Norr, 1993; Tieszen & Fagre, 1993; Numerous studies have shown that this value is
Hilderbrand et al., 1996; Ambrose, 2000; Roth & variable in dietary experiments (e.g., Hare et al.,
Hobson, 2000; Jenkins et al., 2001). 1991; Hilderbrand et al., 1996; Hobson et al., 1996;
Mathematical models have been developed in Ambrose, 2000), and this is also a key parame-
order to quantify the contribution of different ter that needs to be well constrained in order to
make the models even more reliable for dietary
* Correspondence to: Laboratoire de Paléontologie, Institut des Sci-
and palaeodietary reconstructions. A review of
ences de l’Evolution, UMR 5455 du CNRS, Université Montpellier
2, case courrier 064, Place Eugène Bataillon, F-34095 Montpellier published enrichment values under experimental
cedex 05, France. conditions yields a range of 3.7 to 6.0‰ for δ 13 C
Copyright 2003 John Wiley & Sons, Ltd. Accepted 25 September 2002Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen 47
values between diet and collagen, and a range of been performed on the well-monitored large
1.7 to 6.9‰ for δ 15 N values (Bocherens & Mari- mammals from the Bialowieza primeval forest in
otti, 2002). Taking such a large range into account Poland. These data will be used to discuss how
in the models would lead to large uncertainties in trophic enrichments can be calculated. Secondly,
the quantifications of dietary resources. case studies from Upper Palaeolithic sites in
In this paper, we evaluate the enrichment values southwestern France will be presented to verify
deduced from collagen isotopic compositions that predators from Late Pleistocene ecosystems
of prey-predator pairs. Collagen presents the present enrichment values consistent with those
advantage of averaging the isotopic composition measured in modern ecosystems.
of the diet over long time periods. In the case of
predators, which consume mostly vertebrate prey,
the difference between the isotopic composition A case study in a well-monitored
of their collagen and that of their prey directly modern ecosystem: Bialowieza
reflects the isotopic enrichment linked to a trophic
step. Moreover, collagen can be preserved in primeval forest
ancient bones, thus it opens the possibility to
check the presumed trophic link between prey Bialowieza primeval forest is the last terrestrial
and predator in the past. habitat in Europe that includes a suite of large wild
However, few studies have been published mammals and it is probably one of the most thor-
on closely monitored modern faunas with well- oughly studied ecosystems. In particular, data are
defined terrestrial mammalian predators and their available on the relative contribution of each prey
possible prey in wild contexts (Table 1). Only species to each predatory species (Jedrzejewska
five cases meeting these criteria could be found, & Jedrzejewski, 1998), permitting a quantitative
and even if we missed a few, this is a low estimation of the isotopic enrichment.
number relative to the total number of trophic The studied bone material belongs to two
isotopic enrichment studies performed to date. predator species, boreal lynx (Lynx lynx) and
The difference between the isotopic values of wolf (Canis lupus) and their main prey, which
prey and predator collagen range from 1.2 to are ungulates such as red deer (Cervus elaphus),
2‰ and from 2.4 to 4.8‰, for carbon and roe deer (Capreolus capreolus), and wild boar (Sus
nitrogen respectively. It is noteworthy that such scrofa). The specimens died between 1959 and
studies usually consider one species of prey as the 1999, and the year of death has been recorded for
main prey and neglect the contributions of other each specimen. During this 40-year period, the
possible prey (e.g., Schwarcz, 1991; Szepanski δ 13 C value of atmospheric CO2 has shifted from
et al., 1999). This uncertainty may affect the actual around −7.5‰ (Friedli et al., 1986) to −8.5‰
enrichment value in these studies. (extrapolating the exponential trend proposed by
Due to this small number of studies and Feng, 1998). Such a difference is not negligible
to these uncertainties regarding actual prey- when calculating the difference between the
predator relationships, a detailed study has 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 Predators (n) Prey (n) 13 C∗ 15 N∗ References
Predator—prey
South Africa (C3 ) Lynx, jackal Hare, antelope ∼2† Van der Merwe (1989)
Ontario (Canada) Wolf (10) Deer (16) 2.9 Schwarcz (1991)
Ontario (Canada) Coyote (15) Deer (19) 2.7 Schwarcz (1991)
Interior Alaska (USA) Wolf (50) Caribou (41) 1.2 2.4 Szepanski et al. (1999)
East Africa Carnivorous mammals (15) Herbivorous mammals (193) 4.8 Ambrose & DeNiro (1986)
∗ is isotopic enrichment between two taxa or tissues. 13 C
predator-prey = δ Cpredator − δ Cprey . Npredator-prey is
13 13 15
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 killed in 1999. Taking into account this type of set the δ 13 C values of each specimen to a similar correction will become more crucial in the future atmospheric δ 13 C value before calculating the studies since the isotopic shift of atmospheric enrichment value between the carbon isotopic CO2 is due to increase. composition of prey and predator collagen. A We compare estimates produced by different correction factor for each specimen has been methods for calculating prey-predator isotopic designed using the formula presented by Feng differences, including fairly crude methods typ- (1998) and modified in order to obtain a δ 13 C ically used in studies of this sort (Tables 2 value of −7‰ for atmospheric CO2 , which is the and 3). One estimate is based on a ‘virtual’ average value for atmospheric CO2 during Upper prey that has an average isotopic value with Pleistocene times (Leuenberger et al., 1992). The an equal contribution of each ungulate species. modified correction formula is: 13 C = −7 − Another estimation is performed comparing col- (−6.429 − 0.0060e0.0217(t−1740) ), where t is years lagen isotopic compositions of each predator and AD. This correction ranges from 0.1‰ for that of its main prey. Finally, the most realistic specimens killed in 1959 to 1.1‰ for specimens 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) % biomass in faeces % biomass in diet δ 13 C mean δ 13 C sd δ 15 N mean δ 15 N sd Medium-sized mammals 1.5 1.5 Boar—Sus scrofa (4) 14.7 14.7 −21.1 0.4 1.9 0.7 Red deer—Cervus elaphus (6) 16.5 66.3† −23.1 0.9 2.7 0.9 Roe deer—Capreolus capreolus (5) 3.1 15.6† −23.3 0.6 2.1 1.8 Cervids (80% red deer, 20% roe deer)* 62.3 Weighted average of ungulates −22.8 0.8 2.5 1.0 Wolf—Canis lupus (5) −21.8 0.5 6.1 0.3 wolf-red deer 1.3 3.4 wolf-1/3 each ungulate 0.7 3.9 wolf-weighted average of ungulates 1.0 3.6 ∗ 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) % biomass in faeces % biomass in diet δ 13 C mean δ 13 C sd δ 15 N mean δ 15 N sd Boar—Sus scrofa (4) 0.5 0.5 −21.1 0.4 1.9 0.7 Red deer—Cervus elaphus (5) 5.9 24.9† −23.1 0.9 2.7 0.9 Roe deer—Capreolus capreolus (5) 12.7 66.8† −23.3 0.6 2.1 1.8 Cervid (26% red deer, 74% roe deer)∗ 73.1 Other (mostly hare) 7.8 7.8 Weighted average of ungulates −23.2 0.7 2.3 1.5 Lynx—Lynx lynx (4) −22.1 0.3 6.3 0.4 lynx-roe deer 1.2 4.2 lynx-1/3 each ungulate 0.4 4.1 lynx-weighted average of ungulates 1.1 4.0 ∗ 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 49 performed using the relative contribution of each linked to the uncertainties inherent to enrichment prey species to each predatory species, based on calculations, even in modern ecosystems. The ecological reports. problem is to define the extreme values of The ecological data show that for both preda- the range of enrichment values. The commonly tors, one prey species dominates the biomass of quoted ranges for enrichment values of 0 to the consumed prey (∼66%), i.e. red deer for 2‰ for carbon and 3 to 5‰ for nitrogen seem wolf and roe deer for lynx (Okarma et al., 1997; reasonable compared to the enrichment values Jedrzejewski et al., 2000). When the three main estimated in the present paper. ungulate species (boar, roe deer and red deer) In the case of past ecosystems with no are considered, more than 90% of the diet of analogues in modern environments, such as each predator is taken into account (Table 2). those of the last glacial period (e.g., Guthrie, For estimates in which the three ungulate prey 1982), a first step before using this range of species are considered to contribute equally to the values in modelling approaches is to verify that predator’s diet, the contribution of boar is highly such a range is consistent with the observed over-represented, especially for lynx, and the con- data. We thus tried to investigate isotopic tribution of the main species is under-represented. enrichment between predators and their likely Estimates that consider only the main prey species prey for Upper Pleistocene western European for each predator are more realistic ecologically, sites. In this context, most of the available faunal and this is the method that is usually followed in remains are coming from archeological sites, in previously published work (e.g., Schwarcz, 1991; which the main accumulation factor is human Szepanski et al., 1999). Finally, the most accurate activity. In such cases, comparing predator and analysis considers the contribution of each species prey isotopic compositions is complicated by following the percentage in consumed biomass as two factors: (1) the possible bias between the determined by ecological studies. The difference natural environment and the selection of animals between the estimates given by the first method by humans, and (2) the fact that the relative (one third of each ungulate) relative to the second abundance of different prey species is not due method (only main prey) is larger than between to the animal predator activity. Keeping these the second method relative to the third (based on complications in mind, we present some examples the actual contribution of each prey). In the case of such studies in chosen sites from southwestern of nitrogen enrichment values of lynx, all three France, dating from the Late Glacial Maximum. approaches give very similar results, with a max- imum difference of only 0.2‰, which is within the range of analytical error. In conclusion, the Case studies from Upper Palaeolithic enrichment values obtained using the most pre- sites in southwestern France cise 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 Three archeological sites, which range in age respectively. In the case of a predator with a main from 19,000 to 16,000 BP, have yielded faunal prey species that contributes more than 50% in assemblages including predators and their likely biomass with isotopic signatures relatively close prey and have been the object of isotopic to those of other prey, the quantitative estimation investigations (Drucker, 2001). This context of enrichment values based on the main species is is favourable to the application of isotopic a satisfactory approximation. methodology, due to the good preservation of These results emphasize the importance of bone collagen and to the occurrence of different using ranges of enrichment values rather than prey species that can be distinguished through an average figure deduced from a review of their carbon and nitrogen isotopic compositions, the published data. In most cases, ecological such as reindeer versus horse (Fizet et al., 1995; data as detailed as in the Bialowieza primeval Drucker et al., 1999, 2000a). The chosen layers forest will not be available, especially for past are the Solutrean level from Les Jamblancs ecosystems. Thus using a relatively wide range of (around 19,000 BP; Drucker et al., 2000b), the isotopic enrichments will compensate for errors Solutrean level from Combe-Saunière (around Copyright 2003 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 13: 46–53 (2003)
50 H. Bocherens and D. Drucker
19,000 BP; Geneste & Plisson, 1986), and the Table 5. Estimates for isotopic enrichment between collagen of
wolf and its potential prey in the ancient ecosystem of Saint-
Middle Magdalenian layer from Saint-Germain Germain-la-Rivière (Middle Magdalenian layer ∼16,000 BP).
la Rivière (around 16,000 BP; Lenoir, 2000). Data are from Drucker (2001)
Samples from wolf and from the different ungulate
species have been selected in Les Jamblancs Taxon (n) δ 13 C δ 13 C δ 15 N δ 15 N
mean sd mean sd
and Saint-Germain-la-Rivière, while samples from
rodents (ground squirrel Citellus superciliosus) and Horse—Equus sp. (3) −21.0 0.1 4.2 0.2
lagomorphs (hare Lepus timidus) have been sampled Saiga—Saiga tatarica (11) −19.6 0.3 4.0 0.5
Reindeer—Rangifer tarandus (3) 19.1 0.0 3.5 0.3
from Combe Saunière 1 together with snowy Bovine—bos or bison (3) −20.1 0.0 5.5 0.5
owl (Nyctea scandiaca). This last site offers the Average herbivores −19.9 4.3
opportunity to study a situation where small Wolf—Canis lupus (1) −19 8.7
wolf-herbivores 0.9 4.4
mammals are the preferred prey. Indeed, modern
snowy owls consume mostly rodents, such as
lemmings, but also other kind of rodents and even Table 6. Estimates for isotopic enrichment between collagen of
arctic hares (Paquin & David, 1993). snowy owl and its potential prey in the ancient ecosystem of
Combe-Saunière I (Solutrean layer ∼19,000 BP). Data are from
Collagen has been extracted from bone pow- Drucker (2001)
ders according to Bocherens et al. (1991). All
extracts have been checked for carbon and nitro- Taxon (n) δ 13 C δ 13 C δ 15 N δ 15 N
gen content and C/N ratios in order to investigate mean sd mean sd
chemical purity. All extracts that contain less Hare—Lepus timidus (4) −20.2 0.4 2.3 0.7
than 10% nitrogen and C/N ratios outside a Ground −20.9 0.4 1.9 0.9
range of 2.9–3.6 are not included in the discus- squirrel—Citellus
superciliosus (5)
sion, since their isotopic composition may have Average prey −20.6 2.1
been shifted due to diagenetic alteration (DeNiro, Snowy owl—Nyctea −19.8 0.2 5.1 0.6
1985; Ambrose, 1990). Only results from adult scandiaca (7)
owl-prey 0.8 3.0
bones have been considered, since the nitrogen
isotopic composition of juvenile specimens can
be influenced by the consumption of milk from The average isotopic signatures of the speci-
their mother (e.g., Fogel et al., 1989; Hobson et al., mens are presented in Tables 4–6. Since modern
1996). Moreover, teeth have been avoided sys- wolf feeds mainly on large ungulates (Mech,
tematically for herbivores (except horse) and as 1970), the calculation for average prey isotopic
much as possible for carnivores, since this tis- signatures is performed considering an equal con-
sue exhibits isotopic differences with bone of tribution of each ungulate species. The estimated
the same individual that can interfere with the enrichment values are 0.3 and 0.9‰ for car-
trophic determinations (Bocherens et al., 1994, bon and 5.5 and 4.4‰ for nitrogen in Les
1995; Bocherens & Mariotti, 1997). Jamblancs and Saint-Germain-la-Rivière respec-
tively (Tables 4 and 5). The 5.5‰ enrichment
Table 4. Estimates for isotopic enrichment between collagen
value for nitrogen in Les Jamblancs is estimated
of wolf and its potential prey in the ancient ecosystem of Les from collagen extracted from a tooth; this value
Jamblancs (Solutrean layer ∼19,000 BP). Data are from Drucker can be corrected using the enrichment observed
et al. (2000b) between dentine and bone δ 15 N values of mod-
Taxon (n) δ 13 C δ 13 C δ 15 N δ 15 N
ern individual wolf, which range from 1.6 to
mean sd mean sd 2.1‰ (Bocherens, 1992, 2000). The estimated
15 N-enrichment value between this fossil wolf
Horse—Equus sp. (4) −21.1 0.2 2.4 0.9 and its potential prey is between 3.4 and 3.9‰.
Reindeer—Rangifer tarandus (5) −19.6 0.1 3.9 1.1
Red Deer—Cervus elaphus (1) −20.3 2.6 In the case of snowy owl, the enrichment val-
Bovine—bos or bison (3) −19.9 0.1 4.7 0.4 ues are 0.8 and 3.0‰ for carbon and nitrogen
Average herbivores −20.2 3.4 respectively (Table 6).
Wolf—Canis lupus (tooth) (1) −18.9 8.9
wolf-herbivores 1.3 5.5 These examples show that the ranges of
enrichment values estimated from archeological
Copyright 2003 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 13: 46–53 (2003)Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen 51
site faunas are consistent with those measured References
in the studied modern ecosystems. This is
encouraging for the future use of modelling Ambrose SH. 1990. Preparation and characterization
approaches in Upper Pleistocene ecosystems of bone and tooth collagen for isotopic analysis.
using this range of enrichment values. Journal of Archaeological Science 17: 431–451.
Ambrose SH. 2000. Controlled diet and climate
experiments on nitrogen isotope ratios in rats.
Conclusions In Biogeochemical Approaches to Paleodietary Analysis,
Ambrose SH, Katzenberg MA (eds). Kluwer Aca-
demic/Plenum Publishers: New York; 243–259.
Recent improvements in modelling approaches
Ambrose SH, DeNiro MJ. 1986. The isotopic ecology
have allowed significant progress in the dietary of East African mammals. Oecologia 69: 395–406.
reconstruction in modern ecosystems. No doubt Ambrose SH, Norr L. 1993. Experimental evidence
these approaches will provide very fruitful infor- for the relationship of the carbon isotope ratios of
mation on past ecosystems as well. However, one whole diet and dietary protein to those of bone
factor that remains under-determined is the range collagen and carbonate. In Prehistoric Human Bone,
of variation in carbon and nitrogen enrichment Archaeology at the Molecular Level, Lambert J, Grupe G
values between a predator and its average food. (eds). Springer: Berlin; 1–37.
Taking into account this additional uncertainty Bocherens H. 1992. Biogéochimie isotopique (13 C,15 N,18 O)
in modelling approaches will decrease the preci- et Paléontologie des Vertébrés: Applications à l’étude des réseaux
sion of the obtained figures, which is frustrating trophiques révolus et des paléoenvironnements. Unpublished
but unavoidable. Further work is thus necessary Ph.D thesis. University Paris 6.
Bocherens H. 2000. Preservation of isotopic signals
in order to better understand if environmental or (13 C,15 N) in Pleistocene mammals. In Biogeochem-
physiological parameters can explain some of this ical Approaches to Paleodietary Analysis, Ambrose SH,
range. This point should progress when investiga- Katzenberg MA (eds.). Kluwer Academic/Plenum
tions involving experimentally designed trophic Publishers: New York; 65–88.
situations and well-monitored ecosystems are per- Bocherens H, Mariotti A. 1997. Comments on: Diet,
formed on the species of interest for palaeodietary physiology and ecology of fossil mammals as
reconstructions. inferred from stable carbon and nitrogen isotope
biochemistry: Implications for Pleistocene bears by
Bocherens et al.—Reply. Palaeogeography, Palaeoclima-
Acknowledgements tology, Palaeoecology 128: 362–364.
Bocherens H, Mariotti A. 2002. Paléoenvironnements
et paléoalimentations: biogéochimie isotopique des
Most specimens have been kindly provided by vertébrés. In Géologie de la Préhistoire, Miskovsky JC
the Mammal Research Institute of Bialowieza (ed.). GEOPRE, Presses Universitaires de Perpignan:
(E. Szuma), except for one red deer specimen, Perpignan, France; 1323–1344.
provided by the Museum d’Histoire Naturelle Bocherens H, Fizet M, Mariotti A, Lange-Badré B,
of Paris (M. Mashkour and E. Pellé). We thank Vandermeersch B, Borel JP, Bellon G. 1991. Isotopic
the Musée National de Préhistoire (Les Eyzies biogeochemistry (13 C,15 N) of fossil vertebrate col-
de Tayac) and the Institut de Préhistoire et de lagen: implications for the study of fossil food web
Géologie de Quaternaire (University Bordeaux 1) including Neandertal Man. Journal of Human Evolution
for authorization to study ancient material. Many 20: 481–492.
thanks are due to Daniel Billiou for his assistance Bocherens H, Fizet M, Mariotti A. 1994. Diet, physiol-
in analysing the collagen at the Laboratoire ogy and ecology of fossil mammals as inferred by sta-
ble carbon and nitrogen isotopes biogeochemistry:
de Biogéochimie Isotopique (University Paris
implications for Pleistocene bears. Palaeogeography,
6). The investigations of Upper Palaeolithic Palaeoclimatology, Palaeoecology 107: 213–225.
faunas were financially supported by the PEH Bocherens H, Fogel ML, Tuross N, Zeder M. 1995.
programme of the CNRS. We are grateful to Trophic structure and climatic information from
Dr Paul Koch and two anonymous reviewers isotopic signatures in a Pleistocene cave fauna of
for valuable comments on an earlier version of Southern England. Journal of Archaeological Science 22:
this manuscript. 327–340.
Copyright 2003 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 13: 46–53 (2003)52 H. Bocherens and D. Drucker DeNiro MJ. 1985. Postmortem preservation and alter- approche paléthnologique. Gallia Préhistoire 29: ation of in vivo bone collagen isotope ratios in 9–27. relation to palaeodietary reconstruction. Nature 317: Guthrie RD. 1982. Mammals of the mammoth 806–809. steppe as paleoenvironmental indicators. In Pale- DeNiro MJ, Epstein S. 1978. Influence of diet on the oecology of Beringia, Hopkins DM, Matthews JV Jr, distribution of carbon isotopes in animals. Geochimica Schweger CE, Young SB (eds.). Academic Press: et Cosmochimica Acta 42: 495–506. New York; 307–326. DeNiro MJ, Epstein S. 1981. Influence of diet on Hare PE, Fogel ML, Stafford TW Jr, Mitchell AD, the distribution of nitrogen isotopes in animals. Hoering TC. 1991. The isotopic composition of Geochimica et Cosmochimica Acta 45: 341–351. carbon and nitrogen in individual amino acids iso- Drucker D. 2001. Validation méthodologique de l’analyse lated from modern and fossil proteins. Journal of isotopique d’ossements fossiles et apport aux reconstitutions Archaeological Science 18: 277–292. paléoécologiques du Paléolithique Supérieur dans le Sud- Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Ouest de la France. Unpublished Ph.D. dissertation. Titus K, Servheen C. 1996. Use of stable isotopes to Université Paris 6. determine diets of living and extinct bears. Canadian Drucker D, Bocherens H, Mariotti A, Lévêque F, Van- Journal of Zoology 74: 2080–2088. dermeersch B, Guadelli JL. 1999. Conservation des Hobson KA, Schell DM, Renouf D, Noseworthy E. signatures isotopiques du collagène d’os et de dents 1996. Stable carbon and nitrogen isotopic frac- du Pléistocène Supérieur (Saint-Césaire, France): tionation between diet and tissue of captive seals: implications pour les reconstitutions des régimes ali- implications for dietary reconstructions involving mentaires des Néandertaliens. Bulletins et Mémoires de marine mammals. Canadian Journal of Fisheries and la Société d’Anthropologie de Paris 11: 289–305. Aquatic Sciences 53: 528–533. Drucker D, Bocherens H, Mariotti A. 2000a. Con- Jedrzejewska B, Jedrzejewski W. 1998. Predation in tribution de la biogéochimie isotopique à la vertebrate communities. The Bialowieza Primeval paléobiologie des grands mammifères pléistocènes Fores as a case study. Ecological studies, Springer 135: supérieurs: Application aux rennes et aux chevaux 1–450. du Pléistocène supérieur du Sud-Ouest de la France. Jedrzejewski W, Jedrzejewska B, Okarma H, Sch- Mémoire de la Société Préhistorique Française 28: 13–27. midt K, Zub K, Musiani M. 2000. Prey selection Drucker D, Bocherens H, Cleyet-Merle JJ, Made- and predation by wolves in Bialowieza primeval laine S, Mariotti A. 2000b. Implications paléoenviro- forest, Poland. Journal of Mammalogy 81: 197–212. nnementales de l’étude isotopique (13 C,15 N) de la Jenkins SG, Partridge ST, Stephenson TR, Farley SD, faune de grands mammifères des Jamblancs (Dor- Robbins CT. 2001. Nitrogen and carbon isotope dogne, France). Paléo 12: 29–53. fractionation between mothers, neonates, and nurs- Feng X. 1998. Long-term ci /ca response of trees in ing offspring. Oecologia 129: 336–341. western North America to atmospheric CO2 con- Koch PL, Phillips DL. 2002. Incorporating concentra- centration derived from carbon isotope chronolo- tion dependence in stable isotope mixing models: gies. Oecologia 117: 19–25. A reply to Robbins, Hilderbrand and Farley (2002). Fizet M, Mariotti A, Bocherens H, Lange-Badré B, Oecologia 133: 14–18. Vandermeersch B, Borel JP, Bellon G. 1995. Effect of Lenoir M. 2000. La fin des temps glaciaires dans les diet, physiology and climate on carbon and nitrogen basses vallées de la Dordogne et de la Garonne. isotopes of collagen in a late Pleistocene anthropic Mémoire de la Société Préhistorique française 28: 81–87. paleoecosystem (France, Charente, Marillac). Journal Leuenberger M, Siegenthaler U, Langway CC. 1992. of Archaeological Science 22: 67–79. Carbon isotope composition of atmospheric CO2 Fogel ML, Tuross N, Owsley DW. 1989. Nitrogen during the last ice age from an Antarctic ice core. isotope traces of human lactation in modern and Nature 357: 488–490. archeological populations. Annual Report of the Director Mech LD. 1970. The wolf, the ecology and behaviour of Geophysical Laboratory, Carnegie Institution 1988–1989: an endangered species. University of Minnesota Press, 111–117. Mineapolis. Friedli H, Lötscher H, Oeschger H, Siegenthaler U, Okarma H, Jedrzejewski W, Schmidt K, Kowasczyk R, Stauffer B. 1986. Ice core record of the 13 C/12 C ratio Jedrzejewska B. 1997. Predation of Eurasian lynx on of the atmospheric CO2 in the past two centuries. roe deer and red deer in Bialowieza Primeval Forest, Nature 324: 237–238. Poland. Acta Theriologica 42: 203–224. Geneste JM, Plisson H. 1986. Le Solutréen de la Paquin J, David N. 1993. Le harfang des neiges. Centre de grotte de Combe Saunière 1 (Dordogne). Première conservation de la faune ailée de Montréal. Copyright 2003 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 13: 46–53 (2003)
Trophic Level Isotopic Enrichment of Carbon and Nitrogen in Collagen 53 Phillips DL. 2001. Mixing models in analyses of diet Szepanski MM, Ben-David M, Van Ballenberghe V. using multiple isotopes: a critique. Oecologia 127: 1999. Assessment of anadromous salmon resources 166–170. in the diet of the Alexander Archipelago wolf using Phillips DL, Greg JW. 2001. Uncertainty in source stable isotope analysis. Oecologia 120: 327–335. partitioning using stable isotopes. Oecologia 127: Tieszen LL, Fagre T. 1993. Effect of diet quality 171–179. and composition on the isotopic composition of Phillips DL, Koch PL. 2002. Incorporating concentra- respiratory CO2 , bone collagen, bioapatite, and soft tion dependence in stable isotope mixing models. tissues. In Prehistoric Human Bone, Archaeology at the Oecologia 130: 114–125. Molecular Level, Lambert J, Grupe G (eds.). Springer: Roth JD, Hobson KA. 2000. Stable carbon and nitro- Berlin; 121–155. gen isotopic fractionation between diet and tissue of Van der Merwe NJ. 1989. Natural variation in 13 C captive red fox: implications for dietary reconstruc- concentration and its effect on environmental tion. Canadian Journal of Zoology 78: 848–852. reconstruction using 13 C/12 C ratios in animal bones. Schwarcz HP. 1991. Some theoretical aspects of In The chemistry of prehistoric human bone, Price TD isotope paleodiet studies. Journal of Archaeological (ed.). Cambridge University Press; Cambridge, UK; Science 18: 261–275. 105–125. Copyright 2003 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 13: 46–53 (2003)
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