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Stable Isotopes Data ( 13C, 15N) from the Cave Bear (Ursus Spelaeus): a New Approach to Its Palaeoenvironment and Dormancy D

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Stable Isotopes Data ( 13C, 15N) from the Cave Bear (Ursus Spelaeus): a New Approach to Its Palaeoenvironment and Dormancy D doi 10.1098/rspb.2001.1639 Stable isotopes data ( 13C, 15N) from the cave bear (Ursus spelaeus): a new approach to its palaeoenvironment and dormancy D. Ferna¨ ndez-Mosquera*, M. Vila-Taboada and A. Grandal- d’Anglade Instituto Universitario de Xeolox|¨ a, Facultade de Ciencias, Universidade da Coru·a, E-15071, Spain Palaeoclimatic data that can be extracted from the isotopic signatures of d13C and d15N, which are found in fossil bone collagen, should be analysed according to the speci¢c metabolism of each species. Although Ursus spelaeus is an extinct species, its metabolism is assimilated to current, closely related species of bear. In this study, bone collagen isotopic signatures (d13C and d15N) of cave bears from Late Pleistocene Alpine sites were compared to those that have already been documented. The d13C signature did not seem to follow a systematic trend according to climatic conditions, probably as a consequence of the high variability present in the values of C3 plants, which were the basis of feeding. On the contrary, the d15N signature displayed higher values in sites corresponding to colder periods in which the d15N signature appeared to be dominated by the physiology of dormancy. Then, due to the reuse of urea in synthesizing amino acids, the d15N signature systematically increased along with dormancy duration. This was related to the length of winter and, in turn, depended on climate. Keywords: Ursus spelaeus; d13C; d15N; bone collagen; palaeoenvironment ; dormancy species are usually considered similar to those of the 1. INTRODUCTION American black bear (Ursus americanus) or the brown bear Carbon and nitrogen isotopic signatures, which are found (Ursus arctos). As with these bears, the cave bear would in fossil tissues (bone and dentine), have often been used retire to a refuge (usually a cave) when food was scarce, for reconstructing the features of palaeoclimate (Ambrose regardless of the amount of reserves accumulated as & De Niro 1989; Bocherens et al. 1994, 1996; Cormie & fat and become dormant (Nelson et al. 1998; Lide¨ n & Schwarcz 1994). The usual strategy followed in extracting AngerbjÎrn, 1999). palaeoclimatic data from the isotopic signatures of 13C Dormancy in bears is not real hibernation, although and 15N in fossil tissues is based on two di¡erent during this stage they do develop a particular metabolism approaches: (i) comparison between these signatures and whereby they do not feed, drink, defecate or urinate. those which are currently found in the same or other Metabolic waste, such as urea, the storage of which can related species under well-known climatic conditions, and be lethal, is almost entirely recycled, as will be explained (ii) comparison between di¡erent fossil species from the later. After dormancy, a bear will only have lost between same site, assuming they are contemporary. 15 and 25% of its body weight at the expense of a Both approaches have clear problems when applied to decrease in fat but not in protein or bone (Anderson extinct species. In the ¢rst case, extinct animals are 1992). Dormancy duration is variable. Periods of ¢ve to compared to current ones following purely phylogenetic seven months in cold regions (Rogers 1987) to cases criteria and, even if it is presumed that their metabolisms where there was no dormancy at all (Hellgren & were similar, the main isotopic signature conditioning, Vaughan 1987) have been documented in American black i.e. climate, is ignored. In the second case, it is presumed bears. In brown bears, variability is lower (Naves & that the climate where the life of the di¡erent species Palomero 1993). Clearly, permanence in bear dens is took place is the same, but comparison forces us to reject longer in those regions with longer winters (Johnson & physiological conditioning. Pelton 1980). The causes of cave bear death inside caves In order to be able to obtain results that allow for the were recently analysed by Stiner (1998) and were found creation of palaeoclimatic reconstruction, it is necessary, to have been disease, accident and starvation. in our opinion, to compare the isotopic signatures of The cave bear has a speci¢c tooth, skull and jaw individuals of the same species and age range from well- morphology, which is the principal reason why it is known geographical areas and, most importantly, use an thought to have followed a basically herbivorous regime accurate chronological framework. This is particularly (Kurte¨ n 1976). In recent years, di¡erent approaches have important in the case of extinct species, in which the been adopted in reconstructing this species’ diet through impossibility of having precise current referents forces us analysis of stable isotopes, usually 13C and 15N, preferably to assume more hypotheses than for extant species. in bone and dentine collagen and hydroxyapatite One of these species is the cave bear (Ursusdeningeri- spelaeus), (Bocherens et al. 1994, 1997; Ferna¨ ndez-Mosquera 1998; which is considered as having been endemic in Europe Nelson et al. 1998; Lide¨ n & AngerbjÎrn 1999; Vila- (Kurte¨ n 1976). The environment and metabolism of this Taboada et al. 1999). The results derived from these studies may be summed up in the following points. *Author for correspondence ([email protected]). (i) A preferably herbivorous diet based on C3 plants. Proc. R. Soc. Lond. B (2001) 268, 1159^1164 1159 © 2001 The Royal Society Received 14 December 2000 Accepted 19 February 2001 1160 D. Ferna¨ ndez-Mosquera and others Ursus spelaeus (¯13C, ¯15N) andpalaeoclimate Table 1. Isotopic data published so far of cave bear bone 10° 0° 20° collagen from European sites 0 300 600 km (The following references were used: Ferna¨ ndez-Mosquera (1998) for Eiro¨ s, Vila-Taboada et al. (1999) for Li·ares, Bocherens et al. (1994) for Alde© ne, Mialet and Olaskoa, 50° Bocherens et al. (1997) for Scladina-1, Bocherens et al. (1999) for Scladina-4 and Nelson et al. (1998) for Divje Babe.) ¯13C ¯15N age Sc site (%) (%) n (years BP) Sw Eiro¨ s 721.1 0.6 5.0 0.5 8 24 090 440 Gs § § § RK Hd Li·ares 721.0 0.3 3.0 0.4 20 35 220 1440 4 Hg § § 0° E Ll Alde© ne 720.8 0.4 3.1 1.5 3 5250 000 L Co PZ § § Mi DB Mialet 720.2 0.4 2.8 1.6 5 no data § § Al Olaskoa 720.5 2.7 1 ca. 10 000 Scladina-1 722.1 0.2 4.9 1.2 7 ca. 40 000 § § Scladina-4 723.2 0.3 3.6 0.6 4 120 000^130 000 § § Divje Babe 720.5 0.4 1.9 0.7 11 48 000 § § (ii) A marked lactation e¡ect that caused an increase in d15N values in the bone collagen of young individuals and in the dentine values of young and adult indivi- Figure 1. Geographical location of the cave bear sites studied duals, the latter of which maintained the lactation in this work. Sites with data published in this paper are signature due to non-renewal of dentine collagen represented by solid symbols and the initial numbers of after weaning. samples analysed appear in parentheses: Co, Conturines (iii) In some cases, there is a hint of a possible in£uence (three); Ll, Lieglloch (three); RK, Ramesch KnochenhÎhle of winter dormancy on their isotopic signatures (three); Gs, GamssulzenhÎhle (three); Hd, HerdengelhÎhle (Bocherens et al. 1997; Nelson et al. 1998; Lide¨ n & (six); Hg, Hartelsgraben (three); PZ, Potocka Zijalka (three); Sw, SchwabenreithhÎhle (three). Sites from the literature are AngerbjÎrn 1999). represented by hollow circles: L, Li·ares (Vila-Taboada et al. 1999); E, Eiro¨ s (Ferna¨ ndez-Mosquera 1998); Sc, Scladina This study was aimed at obtaining palaeoclimatic data (Bocherens et al. 1997, 1999); Olaskoa^Pyrenees^exact location 13 15 from d C and d N signatures found in the bone collagen unknown (Bocherens et al. 1994); Al, Alde© ne (Bocherens et al. of Ursus spelaeus from di¡erent Alpine sites and 1991, 1994); Mi, Mialet (Bocherens et al. 1994); DB, Divje proposing a comparison with data from other isotopically Babe (Nelson et al. 1998). well-described and well-documented sites. Using a comparison of data from adult individuals of the same in order to calculate the percentage of collagen in the bone. The species, we were able to evaluate how di¡erent climates carbon and nitrogen isotope compositions, percentage of carbon (geographical or chronological) in£uenced the same and nitrogen in collagen and the C:N atomic ratio were metabolism and, thus, delimit the responses of isotopic measured using an Elemental Analyser Carlo-Erba 1108 signatures to climatic conditions. The data from these connected to a Finnigan Mat Delta Plus mass spectrometer, sites, i.e. absolute age (if known), the average values of with analytic reproducibility better than 0.1% for carbon and d13C and d15N signatures and sample sizes, are shown in 0.2% for nitrogen. The results were referred to international table 1. Only data from adult individuals were included. standards, i.e. PDB (Pee Dee Bee limestone) and atmospheric The geographical locations of these sites are shown in N2, respectively. Isotopic ratios are presented using d notation, ¢gure 1. where d [(R /R )]71 1000, where R 15N/14N ˆ sample standard £ ˆ and 13C/12C. 2. MATERIAL AND METHODS 3. RESULTS AND DISCUSSION Palaeoclimatic data extraction from fossil collagen stable isotopes should be interpreted according to the location and Only 12 (none of them from GamssulzenhÎhle) out of conditions of each site. Even though all sites are in the Eastern the 27 initial samples yielded an atomic C:N ratio of Alps, a decision was taken to select samples that covered a wide collagen within the range 2.9^3.6, which is usually consid- range of altitudes (from 878 up to 2800 m above sea level ered as a criterion for proper preservation of the original (a.s.l.)) and ages (from 121 to 28 kiloyears before present (kyr isotopic composition (De Niro 1985).
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