- Email: [email protected]
Isotope evidence for paleodiet of late Upper Paleolithic humans in Great Britain: A response to Richards et al. (2005)
Journal of Human Evolution 51 (2006) 440e442
News and Views
Isotope evidence for paleodiet of late Upper Paleolithic humans in Great Britain: A response to Richards et al. (2005) Herve´ Bocherens a,b,*, Dorothe´e G. Drucker c a
Institut des Sciences de l’Evolution, UMR 5554, Universite´ Montpellier 2, Place E. Bataillon, F-34095 Montpellier cedex 05, France b Institute fu¨r Ur- und Fru¨hgeschichte und Archa¨ologie des Mittelalters, Abteilung A¨ltere Urgeschichte und Quartaˆro¨kologie, Schloss, Burgsteige 11, D-72070 Tu¨bingen, Germany c Maison de l’Arche´ologie et de l’Ethnologie, UMR 7041 ‘‘Arche´ologie Environmentale’’ 21 alle´e de l’Universite´, case 05, 92023 Nanterre Cedex, France Received 12 July 2005; accepted 2 December 2005
Keywords: Collagen; Diet; Great Britain; Isotopes; Upper Paleolithic
Measuring the stable-isotope composition of carbon and nitrogen in fossil bone collagen is a powerful approach to deciphering the diet of ancient people. It is especially useful for investigating human paleodiets during transitional periods of Paleolithic times in Europe, such as the Middle-to-UpperPaleolithic transition around 35,000 years ago, which corresponds to the replacement of Neandertals by anatomically modern humans (e.g., Richards et al., 2001; Drucker and Bocherens, 2004), and the Upper-Paleolithic-to-Epipaleolithic transition around 12,000 years ago, which occurred during the global warming at the end of the Pleistocene epoch (e.g., Richards et al., 2000, 2005; Drucker et al., 2005). Such transitions are often linked to changes in diet (e.g., Cachel, 1997; Richards et al., 2001), and any relevant information on paleodiet in these periods is crucial in order to test dietary hypotheses. In this context, the recently published paper by Richards et al. (2005) on the paleodiet of humans from the late Upper Paleolithic Kendrick’s Cave (Wales, United Kingdom) is a very welcome addition of new isotopic data. However, we consider this paper to be flawed due to methodological problems. We propose an alternative interpretation,
* Corresponding author. Institute fu¨r Ur- und Fru¨hgeschichte und Archa¨olo¨ ltere Urgeschichte und Quartaˆro¨kologie, gie des Mittelalters, Abteilung A Schloss, Burgsteige 11, D-72070 Tu¨bingen, Germany. Tel.: þ49 7071 297 8913; fax: þ49 7071 29 5714. E-mail addresses: [email protected], herve.bocherens@ uni-tuebingen.de (H. Bocherens), [email protected] (D.G. Drucker). 0047-2484/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2005.12.014
based on a more accurate definition of dietary end members, a correct reconstruction of the isotopic signature of the consumed proteins, and the use of linear mixing models. Although our new interpretation confirms that the human isotopic data cannot be explained by a fully terrestrial diet, it shows that seal consumption was not compulsory and could have been replaced by salmon or other marine fish, while freshwater fish was most likely an important resource. One of the methodological weaknesses of Richards and colleagues’ reasoning is the use of a herbivore end member with only two points from a large bovid and a roe deer (Richards et al., 2005). This is clearly insufficient in view of the isotopic variation of herbivore collagen during this period. Indeed, it has been demonstrated that there is variation in isotope values among herbivore species recovered from European sites within the relevant time period (e.g., Drucker and Ce´le´rier, 2001; Drucker et al., 2003; Richards and Hedges, 2003). This poor reference data set for the herbivore protein end point is a classical difficulty when dealing with sepulchral sites, where faunal remains are very rare. In such cases, it is necessary to extrapolate from other sites in the same geographic area and the same time period. Therefore, we used a more robust end member that includes isotopic data for horse, red deer, and large bovid measured by Richards et al. (2000) in Gough’s Cave, southern England, from the same time range as those measured in Kendrick’s Cave. We obtained a different end point, with d13C and d15N values being e20.2 0.8& and 2.1 1.0&, respectively. This new end point presents a less negative d13C value and
H. Bocherens, D.G. Drucker / Journal of Human Evolution 51 (2006) 440e442
a slightly less positive d15N value than the one chosen by Richards et al. (2005) to represent the terrestrial source of proteins. Another methodological weakness is the fact that, when Richards et al. reconstructed the isotopic signature of the protein fraction consumed by the humans, they used a trophic fractionation of 3e5& for d15N, but they did not take into account the 0.8e1.3& shift in d13C values. Such a shift in d13C values was determined for Upper Paleolithic ecosystems by Bocherens and Drucker (2003). If we plot this new end point for herbivore meat and apply the correct shift for the d13C values of a predator collagen relative to those of its prey, the rectangular area defined as the possible values of the average protein consumed by the human specimens does not intersect with the line joining the herbivore and the seal end members, even when the standard deviations for d15N values are taken into account (Fig. 1). This result means that some dietary sources are missing, especially those that would exhibit rather low d13C values and high d15N values in order to balance the isotopic signatures of seal. One possible dietary source with such isotopic features is woolly mammoth (Bocherens et al., 2005). However, the youngest mammoth remains are dated to ca. 12,700 BP in England (Coope and Lister, 1987), and, even if this species was still around Kendrick’s Cave when the studied humans lived, it is unlikely that mammoth were regularly preyed upon by humans (Smith, 1992). Since the north coast of Wales was still dry land between 13,000 and 20 Richards et al. mixing line
18 16 14
441
12,000 BP (Smith, 1992), it is reasonable to assume that freshwater fish was a possible source of proteins for prehistoric humans of this age in this area. Using the average carbon and nitrogen isotopic signatures of freshwater fish determined by Drucker and Bocherens (2004), a new plot can be presented (Fig. 2), and the linear mixing model for three sources from Phillips and Koch (2002) can tentatively be used. The graph shows that the area corresponding to the isotopic signature of the humans’ diet intersects the triangle formed by the aquatic resources (i.e., freshwater fish, salmon, and seal). Thus, it is not necessary to incorporate herbivore meat to explain the human isotopic values. The calculation of the proportion of food resources was performed using the spreadsheet available at http:// www.epa.gov/wed.pages/models.htm, not taking into account the slight differences in carbon and nitrogen concentrations between herbivore meat and aquatic resources. Indeed, the end members can only be estimated in the present case, and this approximation will not change the calculated proportions significantly. We obtained a rough estimate of the possible proportions for the four dietary resources, which range from 0 to 33% for herbivore meat, 27 to 69% for freshwater fish, 0 to 56% for salmon, and 0 to 34% for seal. No solution exists with only herbivore meat and freshwater fish. Some kind of marine food with more positive d13C values is necessary to explain the isotopic signatures in the mean diet of the humans from Kendrick’s Cave. One reason for Richards et al. (2005) to assume that seal was the only marine resource possibly consumed by Kendrick’s Cave humans with the use of only two end points, the herbivores from Kendrick’s cave and a marine one, is their high d15N value. Seals are top predators in the marine trophic web and exhibit among the highest d15N values of marine animals (Richards and Hedges, 1999). The addition of freshwater fish, which is inescapable with the new estimate for the herbivore end point and the shift of d13C values, makes
+3‰
12 15 δ N
18 +5‰
10
16 8
+1.3‰+0.8‰
14
6
12
4
15 δ N
herbivores seal
2
human 0 -22
-20
-18
-16
-14
-12
-10
δ13C
10 8
herbivores river fish
6
salmonid seal
4
human
Fig. 1. Average d13C and d15N values for bone collagen extracted from herbivores from southern England and Wales around 12,000 BP, and from humans from Kendrick’s Cave, as well as seals (data are from Richards and Hedges, 1999; Richards et al., 2000, 2005). The bars correspond to standard deviations for herbivores and seals. The rectangle corresponds to the possible range for the average isotopic signatures of the proteins consumed by the humans from Kendrick’s Cave, calculated using the fractionation ranges defined by Bocherens and Drucker (2003), and represented as equivalent collagen values. Also plotted are theoretical mixing lines between two resources, using the faunal data as end points, with their standard deviations.
human's diet
2 0 -22
-20
-18
-16
-14
-12
-10
δ13C Fig. 2. Average d13C and d15N values of bone collagen from different food resources. Also plotted are theoretical mixing lines between three resources, using the faunal data as end points. Additional data for fish are from Drucker and Bocherens (2004).
442
H. Bocherens, D.G. Drucker / Journal of Human Evolution 51 (2006) 440e442
possible the input of marine foods with lower d15N values than seal, such as fish. The intersection between the human food resource and the triangle of three food resources is still possible with d15N values of around 10& for the marine end point, a value that excludes shellfish, but that is exhibited by various types of marine fish (Richards and Hedges, 1999). The isotopic signatures of the humans from Kendrick’s Cave thus point to the consumption of a large proportion of freshwater fish, although no fish remains were mentioned in the excavation report (Richards et al., 2005). This is a classical occurrence for ancient excavations and does not mean that fish remains were absent from the site (Cleyet-Merle, 1990). Moreover, the burial context of the site makes it unlikely that all types of consumed animals were recovered (Richards et al., 2005). Fish could have been collected in the river running at the bottom of the Menai Strait, which was not yet invaded by the marine transgression that occurred after 9000 BP (Smith, 1992). The consumption of some kind of marine food is compulsory, but not necessarily in the form of seal. Marine fish is clearly acceptable, as well as salmon, an anadromous fish that brings inland a food resource with a marine signature (e.g., Bilby et al., 1996; Helfield and Naiman, 2002). Changing the nonterrestrial dietary component for the humans from Kendrick’s Cave from seal to freshwater fish and marine fish that could be anadromous salmon makes a large difference in the mobility pattern inferred by the paleodietary reconstruction. An increase in fish consumption at the end of the Upper Paleolithic and the beginning of Epipaleolithic has been suggested by zooarchaeological investigations (e.g., Le Gall, 1998). Burgeoning isotopic studies show a similar trend, such as this new interpretation of the data presented by Richards et al. (2005), but also in southwestern France during the same period (Drucker et al., 2005). The isotopic investigations of prehistoric humans need to be associated with thorough faunal studies, and the methodology of isotopic paleoecology must be carefully applied. In burial contexts with few faunal remains, the isotopic signatures of prehistoric humans will provide useful dietary trends, but it will be very difficult to infer the consumption of precise food resources in accurate proportions. References Bilby, R.E., Fransen, B.R., Bisson, P.A., 1996. Incorporation of nitrogen and carbon from spawning coho salmon into the trophic system of small streams: evidence from stable isotopes. Can. J. Fish. Aquat. Sci. 53, 164e173.
Bocherens, H., Drucker, D., 2003. Trophic level isotopic enrichments for carbon and nitrogen in collagen: case studies from recent and ancient terrestrial ecosystems. Int. J. Osteoarchaeol. 13, 46e53. Bocherens, H., Drucker, D., Billiou, D., Patou-Mathis, M., Vandermeersch, B., 2005. Isotopic evidence for diet and subsistence pattern of the SaintCe´saire I Neanderthal: review and use of a multi-source mixing model. J. Hum. Evol. 49, 71e87. Cachel, S., 1997. Dietary shifts and the European Upper Palaeolithic transition. Curr. Anthropol. 38, 579e603. Cleyet-Merle, J.-J., 1990. La pre´histoire de la peˆche. Editions Errance. Coope, G.R., Lister, A.M., 1987. Late-glacial mammoth skeletons from Condover, Shropshire, England. Nature 330, 472e474. Drucker, D., Bocherens, H., 2004. Carbon and nitrogen stable isotopes as tracers of diet breadth evolution during Middle and Upper Palaeolithic in Europe. Int. J. Osteoarchaeol. 14, 162e177. Drucker, D., Ce´le´rier, G., 2001. Teneurs en carbone-13 du collage`ne de grands mammife`res du site de Pont d’Ambon (Dordogne, France): Implications pour l’environnement et son exploitation au Tardiglaciaire dans le sudouest de la France. Paleo 13, 145e153. Drucker, D.G., Bocherens, H., Billiou, D., 2003. Evidence of shifting environmental conditions in southwestern France from 33,000 to 15,000 years ago derived from carbon-13 and nitrogen-15 natural abundances in collagen of large herbivores. Earth Planet. Sci. Lett. 216, 163e173. Drucker, D.G., Henry-Gambier, D., Lenoir, M., 2005. Alimentation humaine au cours du Magdale´nien en Gironde d’apre`s les teneurs en isotopes stables (13C, 15N) du collage`ne. Paleo 17, 57e72. Helfield, J.M., Naiman, R.J., 2002. Salmon and alder as nitrogen sources to riparian forests in a boreal Alaskan watershed. Oecologia 133, 573e582. Le Gall, O., 1998. Aperc¸u des peˆches maritimes pre´historiques en Europe occidentale. In: Camps, G. (Ed.), L’homme pre´historique et la mer, 120e congre`s CTHS, Aix-en-Provence, 23-26 oct. 1995. Editions du CTHS, Paris, pp. 377e386. Phillips, D.L., Koch, P.L., 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130, 114e125. Richards, M.P., Hedges, R.E.M., 1999. Stable isotope evidence for similarities in the types of marine foods used by late Mesolithic humans at sites along the Atlantic coast of Europe. J. Archaeol. Sci. 26, 717e722. Richards, M.P., Hedges, R.E.M., 2003. Variations in bone collagen d13C and d15N values of fauna from northwest Europe over the last 40,000 years. Palaeogeogr. Palaeoclimatol. Palaeoecol. 193, 261e267. Richards, M.P., Hedges, R.E.M., Jacoby, R., Currant, A., Stringer, C., 2000. Gough’s Cave and Sun Hole Cave human stable isotope values indicate a high animal protein diet in the British Upper Palaeolithic. J. Archaeol. Sci. 27, 1e3. Richards, M.P., Pettitt, P.B., Stiner, M.C., Trinkaus, E., 2001. Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proc. Natl. Acad. Sci. 98, 6528e6532. Richards, M.P., Jacoby, R., Cook, J., Pettitt, P.B., Stringer, C.B., 2005. Isotopic evidence for the intensive use of marine foods by late Upper Palaeolithic humans. J. Hum. Evol. 49, 390e394. Smith, C., 1992. Late Stone Age Hunters of the British Isles. Routledge, London.
News and Views
Isotope evidence for paleodiet of late Upper Paleolithic humans in Great Britain: A response to Richards et al. (2005) Herve´ Bocherens a,b,*, Dorothe´e G. Drucker c a
Institut des Sciences de l’Evolution, UMR 5554, Universite´ Montpellier 2, Place E. Bataillon, F-34095 Montpellier cedex 05, France b Institute fu¨r Ur- und Fru¨hgeschichte und Archa¨ologie des Mittelalters, Abteilung A¨ltere Urgeschichte und Quartaˆro¨kologie, Schloss, Burgsteige 11, D-72070 Tu¨bingen, Germany c Maison de l’Arche´ologie et de l’Ethnologie, UMR 7041 ‘‘Arche´ologie Environmentale’’ 21 alle´e de l’Universite´, case 05, 92023 Nanterre Cedex, France Received 12 July 2005; accepted 2 December 2005
Keywords: Collagen; Diet; Great Britain; Isotopes; Upper Paleolithic
Measuring the stable-isotope composition of carbon and nitrogen in fossil bone collagen is a powerful approach to deciphering the diet of ancient people. It is especially useful for investigating human paleodiets during transitional periods of Paleolithic times in Europe, such as the Middle-to-UpperPaleolithic transition around 35,000 years ago, which corresponds to the replacement of Neandertals by anatomically modern humans (e.g., Richards et al., 2001; Drucker and Bocherens, 2004), and the Upper-Paleolithic-to-Epipaleolithic transition around 12,000 years ago, which occurred during the global warming at the end of the Pleistocene epoch (e.g., Richards et al., 2000, 2005; Drucker et al., 2005). Such transitions are often linked to changes in diet (e.g., Cachel, 1997; Richards et al., 2001), and any relevant information on paleodiet in these periods is crucial in order to test dietary hypotheses. In this context, the recently published paper by Richards et al. (2005) on the paleodiet of humans from the late Upper Paleolithic Kendrick’s Cave (Wales, United Kingdom) is a very welcome addition of new isotopic data. However, we consider this paper to be flawed due to methodological problems. We propose an alternative interpretation,
* Corresponding author. Institute fu¨r Ur- und Fru¨hgeschichte und Archa¨olo¨ ltere Urgeschichte und Quartaˆro¨kologie, gie des Mittelalters, Abteilung A Schloss, Burgsteige 11, D-72070 Tu¨bingen, Germany. Tel.: þ49 7071 297 8913; fax: þ49 7071 29 5714. E-mail addresses: [email protected], herve.bocherens@ uni-tuebingen.de (H. Bocherens), [email protected] (D.G. Drucker). 0047-2484/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2005.12.014
based on a more accurate definition of dietary end members, a correct reconstruction of the isotopic signature of the consumed proteins, and the use of linear mixing models. Although our new interpretation confirms that the human isotopic data cannot be explained by a fully terrestrial diet, it shows that seal consumption was not compulsory and could have been replaced by salmon or other marine fish, while freshwater fish was most likely an important resource. One of the methodological weaknesses of Richards and colleagues’ reasoning is the use of a herbivore end member with only two points from a large bovid and a roe deer (Richards et al., 2005). This is clearly insufficient in view of the isotopic variation of herbivore collagen during this period. Indeed, it has been demonstrated that there is variation in isotope values among herbivore species recovered from European sites within the relevant time period (e.g., Drucker and Ce´le´rier, 2001; Drucker et al., 2003; Richards and Hedges, 2003). This poor reference data set for the herbivore protein end point is a classical difficulty when dealing with sepulchral sites, where faunal remains are very rare. In such cases, it is necessary to extrapolate from other sites in the same geographic area and the same time period. Therefore, we used a more robust end member that includes isotopic data for horse, red deer, and large bovid measured by Richards et al. (2000) in Gough’s Cave, southern England, from the same time range as those measured in Kendrick’s Cave. We obtained a different end point, with d13C and d15N values being e20.2 0.8& and 2.1 1.0&, respectively. This new end point presents a less negative d13C value and
H. Bocherens, D.G. Drucker / Journal of Human Evolution 51 (2006) 440e442
a slightly less positive d15N value than the one chosen by Richards et al. (2005) to represent the terrestrial source of proteins. Another methodological weakness is the fact that, when Richards et al. reconstructed the isotopic signature of the protein fraction consumed by the humans, they used a trophic fractionation of 3e5& for d15N, but they did not take into account the 0.8e1.3& shift in d13C values. Such a shift in d13C values was determined for Upper Paleolithic ecosystems by Bocherens and Drucker (2003). If we plot this new end point for herbivore meat and apply the correct shift for the d13C values of a predator collagen relative to those of its prey, the rectangular area defined as the possible values of the average protein consumed by the human specimens does not intersect with the line joining the herbivore and the seal end members, even when the standard deviations for d15N values are taken into account (Fig. 1). This result means that some dietary sources are missing, especially those that would exhibit rather low d13C values and high d15N values in order to balance the isotopic signatures of seal. One possible dietary source with such isotopic features is woolly mammoth (Bocherens et al., 2005). However, the youngest mammoth remains are dated to ca. 12,700 BP in England (Coope and Lister, 1987), and, even if this species was still around Kendrick’s Cave when the studied humans lived, it is unlikely that mammoth were regularly preyed upon by humans (Smith, 1992). Since the north coast of Wales was still dry land between 13,000 and 20 Richards et al. mixing line
18 16 14
441
12,000 BP (Smith, 1992), it is reasonable to assume that freshwater fish was a possible source of proteins for prehistoric humans of this age in this area. Using the average carbon and nitrogen isotopic signatures of freshwater fish determined by Drucker and Bocherens (2004), a new plot can be presented (Fig. 2), and the linear mixing model for three sources from Phillips and Koch (2002) can tentatively be used. The graph shows that the area corresponding to the isotopic signature of the humans’ diet intersects the triangle formed by the aquatic resources (i.e., freshwater fish, salmon, and seal). Thus, it is not necessary to incorporate herbivore meat to explain the human isotopic values. The calculation of the proportion of food resources was performed using the spreadsheet available at http:// www.epa.gov/wed.pages/models.htm, not taking into account the slight differences in carbon and nitrogen concentrations between herbivore meat and aquatic resources. Indeed, the end members can only be estimated in the present case, and this approximation will not change the calculated proportions significantly. We obtained a rough estimate of the possible proportions for the four dietary resources, which range from 0 to 33% for herbivore meat, 27 to 69% for freshwater fish, 0 to 56% for salmon, and 0 to 34% for seal. No solution exists with only herbivore meat and freshwater fish. Some kind of marine food with more positive d13C values is necessary to explain the isotopic signatures in the mean diet of the humans from Kendrick’s Cave. One reason for Richards et al. (2005) to assume that seal was the only marine resource possibly consumed by Kendrick’s Cave humans with the use of only two end points, the herbivores from Kendrick’s cave and a marine one, is their high d15N value. Seals are top predators in the marine trophic web and exhibit among the highest d15N values of marine animals (Richards and Hedges, 1999). The addition of freshwater fish, which is inescapable with the new estimate for the herbivore end point and the shift of d13C values, makes
+3‰
12 15 δ N
18 +5‰
10
16 8
+1.3‰+0.8‰
14
6
12
4
15 δ N
herbivores seal
2
human 0 -22
-20
-18
-16
-14
-12
-10
δ13C
10 8
herbivores river fish
6
salmonid seal
4
human
Fig. 1. Average d13C and d15N values for bone collagen extracted from herbivores from southern England and Wales around 12,000 BP, and from humans from Kendrick’s Cave, as well as seals (data are from Richards and Hedges, 1999; Richards et al., 2000, 2005). The bars correspond to standard deviations for herbivores and seals. The rectangle corresponds to the possible range for the average isotopic signatures of the proteins consumed by the humans from Kendrick’s Cave, calculated using the fractionation ranges defined by Bocherens and Drucker (2003), and represented as equivalent collagen values. Also plotted are theoretical mixing lines between two resources, using the faunal data as end points, with their standard deviations.
human's diet
2 0 -22
-20
-18
-16
-14
-12
-10
δ13C Fig. 2. Average d13C and d15N values of bone collagen from different food resources. Also plotted are theoretical mixing lines between three resources, using the faunal data as end points. Additional data for fish are from Drucker and Bocherens (2004).
442
H. Bocherens, D.G. Drucker / Journal of Human Evolution 51 (2006) 440e442
possible the input of marine foods with lower d15N values than seal, such as fish. The intersection between the human food resource and the triangle of three food resources is still possible with d15N values of around 10& for the marine end point, a value that excludes shellfish, but that is exhibited by various types of marine fish (Richards and Hedges, 1999). The isotopic signatures of the humans from Kendrick’s Cave thus point to the consumption of a large proportion of freshwater fish, although no fish remains were mentioned in the excavation report (Richards et al., 2005). This is a classical occurrence for ancient excavations and does not mean that fish remains were absent from the site (Cleyet-Merle, 1990). Moreover, the burial context of the site makes it unlikely that all types of consumed animals were recovered (Richards et al., 2005). Fish could have been collected in the river running at the bottom of the Menai Strait, which was not yet invaded by the marine transgression that occurred after 9000 BP (Smith, 1992). The consumption of some kind of marine food is compulsory, but not necessarily in the form of seal. Marine fish is clearly acceptable, as well as salmon, an anadromous fish that brings inland a food resource with a marine signature (e.g., Bilby et al., 1996; Helfield and Naiman, 2002). Changing the nonterrestrial dietary component for the humans from Kendrick’s Cave from seal to freshwater fish and marine fish that could be anadromous salmon makes a large difference in the mobility pattern inferred by the paleodietary reconstruction. An increase in fish consumption at the end of the Upper Paleolithic and the beginning of Epipaleolithic has been suggested by zooarchaeological investigations (e.g., Le Gall, 1998). Burgeoning isotopic studies show a similar trend, such as this new interpretation of the data presented by Richards et al. (2005), but also in southwestern France during the same period (Drucker et al., 2005). The isotopic investigations of prehistoric humans need to be associated with thorough faunal studies, and the methodology of isotopic paleoecology must be carefully applied. In burial contexts with few faunal remains, the isotopic signatures of prehistoric humans will provide useful dietary trends, but it will be very difficult to infer the consumption of precise food resources in accurate proportions. References Bilby, R.E., Fransen, B.R., Bisson, P.A., 1996. Incorporation of nitrogen and carbon from spawning coho salmon into the trophic system of small streams: evidence from stable isotopes. Can. J. Fish. Aquat. Sci. 53, 164e173.
Bocherens, H., Drucker, D., 2003. Trophic level isotopic enrichments for carbon and nitrogen in collagen: case studies from recent and ancient terrestrial ecosystems. Int. J. Osteoarchaeol. 13, 46e53. Bocherens, H., Drucker, D., Billiou, D., Patou-Mathis, M., Vandermeersch, B., 2005. Isotopic evidence for diet and subsistence pattern of the SaintCe´saire I Neanderthal: review and use of a multi-source mixing model. J. Hum. Evol. 49, 71e87. Cachel, S., 1997. Dietary shifts and the European Upper Palaeolithic transition. Curr. Anthropol. 38, 579e603. Cleyet-Merle, J.-J., 1990. La pre´histoire de la peˆche. Editions Errance. Coope, G.R., Lister, A.M., 1987. Late-glacial mammoth skeletons from Condover, Shropshire, England. Nature 330, 472e474. Drucker, D., Bocherens, H., 2004. Carbon and nitrogen stable isotopes as tracers of diet breadth evolution during Middle and Upper Palaeolithic in Europe. Int. J. Osteoarchaeol. 14, 162e177. Drucker, D., Ce´le´rier, G., 2001. Teneurs en carbone-13 du collage`ne de grands mammife`res du site de Pont d’Ambon (Dordogne, France): Implications pour l’environnement et son exploitation au Tardiglaciaire dans le sudouest de la France. Paleo 13, 145e153. Drucker, D.G., Bocherens, H., Billiou, D., 2003. Evidence of shifting environmental conditions in southwestern France from 33,000 to 15,000 years ago derived from carbon-13 and nitrogen-15 natural abundances in collagen of large herbivores. Earth Planet. Sci. Lett. 216, 163e173. Drucker, D.G., Henry-Gambier, D., Lenoir, M., 2005. Alimentation humaine au cours du Magdale´nien en Gironde d’apre`s les teneurs en isotopes stables (13C, 15N) du collage`ne. Paleo 17, 57e72. Helfield, J.M., Naiman, R.J., 2002. Salmon and alder as nitrogen sources to riparian forests in a boreal Alaskan watershed. Oecologia 133, 573e582. Le Gall, O., 1998. Aperc¸u des peˆches maritimes pre´historiques en Europe occidentale. In: Camps, G. (Ed.), L’homme pre´historique et la mer, 120e congre`s CTHS, Aix-en-Provence, 23-26 oct. 1995. Editions du CTHS, Paris, pp. 377e386. Phillips, D.L., Koch, P.L., 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130, 114e125. Richards, M.P., Hedges, R.E.M., 1999. Stable isotope evidence for similarities in the types of marine foods used by late Mesolithic humans at sites along the Atlantic coast of Europe. J. Archaeol. Sci. 26, 717e722. Richards, M.P., Hedges, R.E.M., 2003. Variations in bone collagen d13C and d15N values of fauna from northwest Europe over the last 40,000 years. Palaeogeogr. Palaeoclimatol. Palaeoecol. 193, 261e267. Richards, M.P., Hedges, R.E.M., Jacoby, R., Currant, A., Stringer, C., 2000. Gough’s Cave and Sun Hole Cave human stable isotope values indicate a high animal protein diet in the British Upper Palaeolithic. J. Archaeol. Sci. 27, 1e3. Richards, M.P., Pettitt, P.B., Stiner, M.C., Trinkaus, E., 2001. Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proc. Natl. Acad. Sci. 98, 6528e6532. Richards, M.P., Jacoby, R., Cook, J., Pettitt, P.B., Stringer, C.B., 2005. Isotopic evidence for the intensive use of marine foods by late Upper Palaeolithic humans. J. Hum. Evol. 49, 390e394. Smith, C., 1992. Late Stone Age Hunters of the British Isles. Routledge, London.