Pleistocene bears in the Swabian Jura (Germany): Genetic replacement, ecological displacement, extinctions and survival

Quaternary International 245 (2011) 225e237

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Pleistocene bears in the Swabian Jura (Germany): Genetic replacement, ecological displacement, extinctions and survival Susanne C. Münzel a, *, Mathias Stiller b, c, Michael Hofreiter b, d, Alissa Mittnik a, Nicholas J. Conard a, Hervé Bocherens e a

Institute for Archaeological Sciences, University of Tübingen, Archaeozoology, Rümelinstr. 23, 72070 Tübingen Germany Research Group Molecular Ecology, MPI EVA, Deutscher Platz 6, D-04103 Leipzig, Germany Department of Biology, Pennsylvania State University, PA 16802, USA d Department of Biology, University of York, York, UK e Deparment of Geosciences, Palaeobiology (Biogeology), University of Tübingen, Hölderlinstr. 12, 72074 Tübingen, Germany b c

a r t i c l e i n f o

a b s t r a c t

Article history: Available online 22 April 2011

Palaeogenetic investigations in three geographically close caves (Hohle Fels, Geißenklösterle, and Sirgenstein) in the Ach Valley near Blaubeuren (Swabian Jura) document the sudden replacement of Ursus spelaeus by Ursus ingressus around 28,000 14C BP. New radiocarbon dates suggest an earlier immigration of Ursus ingressus and at least a partial coexistence with Ursus spelaeus some 4500 years before the ultimate replacement. These two genetic types of cave bears used the same caves for hibernation and had the same herbivorous diet, as shown by the stable isotope results. In contrast, sympatric brown bears (Ursus arctos) exhibited a clearly different ecology, as shown by the carnivorous pattern of their isotopic signatures, and probably did not use the caves as dens before the Last Glacial Maximum (LGM). Once established, the younger cave bear (Ursus ingressus) remained the only cave bear for only another circa 2000 years after the last appearance of the classical cave bear (Ursus spelaeus) in the Ach Valley and elsewhere. The final appearance of cave bear (sensu lato) is now dated to 25,560
130 BP, disproving a refuge area of this species in the Swabian Jura. After the extinction of cave bears (sensu lato), brown bears took over their cave dens and their nutritional niche as they shift to a diet dominated by plant food. Ó 2011 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction The Ach Valley, a tributary of the Danube, is located between Blaubeuren and Schelklingen on the Swabian Jura west of Ulm in Baden-Württemberg (SW-Germany). It provided numerous important cave sites, such as Grobe Grotte (Wagner, 1983; Weinstock, 1999), Brillenhöhle (Boessneck and von den Driesch, 1973; Riek, 1973), Geißenklösterle (Hahn, 1988; Münzel and Conard, 2004a), Sirgenstein (Schmidt, 1912; Koken, in Schmidt, 1912, 165e171), Hohle Fels (Conard and Bolus, 2008; Münzel and Conard, 2004b) and Kogelstein (Böttcher et al., 2000). Nearly all of these caves yielded large quantities of cave bear remains. The age profiles of their death assemblages revealed high percentages of cubs and juveniles and demonstrate that cave bears regularly hibernated in these caves (Münzel, 1997; Weinstock, 1999; Münzel and Conard, 2004b). The only exception is Kogelstein; this former

* Corresponding author. E-mail address: [email protected] (S.C. Münzel). 1040-6182/$ e see front matter Ó 2011 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2011.03.060

cave revealed very few bear remains. Instead, hyena bones are dominant including a high percentage of cubs, which led to the interpretation of it as a hyena den (Ziegler, in Böttcher et al., 2000, 64e77). Palaeogenetic investigation of the cave bears in three of these caves, namely Geißenklösterle, Hohle Fels, and Sirgenstein, have previously yielded positive results (Hofreiter et al., 2002); therefore the focus is on these cave sites in this study (Fig. 1). Archaeological research in the caves of the Ach Valley began in the 19th century. In the years 1870/71, Oscar Fraas (Fraas, 1872) and Theodor Hartmann started their work in the Hohle Fels, a cave near Schelklingen (Alb-Donau Kreis). Fraas’ research question at his time was whether extinct Diluvial mammals coexisted with humans. During the excavation of the main hall of Hohle Fels large quantities of cave bear remains were recovered and transported to the ‘Königliche Naturalienkabinett’ in Stuttgart, the former Natural History Museum. The high morphological variability of cave bears, that has been stated as one of their characteristics by Ehrenberg (1922), was already recognized by Fraas in his short notes about the findings of Hohle Fels (Fraas, 1872). Therein he distinguished three bear species, beside Ursus spelaeus, he mentioned Ursus

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S.C. Münzel et al. / Quaternary International 245 (2011) 225e237

Fig. 1. Geographical location of the cave sites in the Ach Valley: 1 Sirgenstein, 2 Hohle Fels, 3 Geißenklösterle.

priscus (?), an archaic type of bear, and Ursus tarandi (?) with arctoid traits, probably a brown bear. Unfortunately these remains cannot be inspected anymore, since almost all faunal remains were lost during World War II. Modern excavations at Geißenklösterle and Hohle Fels started in the 1970s and were conducted until 1996 by Joachim Hahn (Hahn, 1977, 2000). His research was continued by Nicholas Conard from 1997 until today (Conard and Malina, 2010). The stratigraphical sequences of these two sites are well dated (Conard and Bolus, 2008). These two caves in the Ach Valley are also well known for their earliest musical instruments (Hahn and Münzel, 1995; Conard et al., 2004, 2009) and their figurative art (Hahn, 1986; Floss, 2007), with the earliest female figurine recently found in the deepest Aurignacian layer of Hohle Fels (Conard, 2009). The high morphological variability of the European cave bears was and still is discussed by many researchers regarding phylogenetic, geographic and intra-population variability (e.g. Ehrenberg, 1922, 1929; Kurtén, 1976; Rabeder et al., 2000; Grandal-d’Anglade and López-González, 2005; Baryshnikov, 2006) and has raised questions about the genetic diversity of this species (Hofreiter et al., 2002; Orlando et al., 2002). Ancient DNA research became an important tool to better understand the phylogeny of cave bears (Hofreiter et al., 2002) and their relationship to brown bears (Loreille et al., 2001). In Central Europe two genetically distinct groups of cave bears have been recognized (Hofreiter et al., 2002), and quite recently a third group (Ursus “deningeri” kudarensis) was detected in the Caucasus (Baryshnikov, 2008; Knapp et al., 2009). After Rabeder and Hofreiter (2004) and Rabeder et al. (2004) the two European groups correspond to Ursus ingressus and Ursus spelaeus, of which the latter one can be further subdivided into Ursus s. spelaeus, the classical cave bear, found in Western Europe (Hofreiter, 2002, Fig. 18); Ursus s. eremus, found in Ramesch cave, the type site (Hofreiter, 2002) and recently in a few other caves (Münzel et al., 2010), and Ursus s. ladinicus, found in the entire Alpine region from West Préalpes to the Eastern Alps (Hofreiter, 2002; Münzel et al., 2010). Taken together they form the sister-group to Ursus ingressus, which is found in the eastern parts of the Alps and Eastern Europe, e.g. Slovenia, Croatia, Slovakia, Romania and

Ukraine (Hofreiter, 2002; Münzel et al., 2010). Ursus ingressus started its territorial expansion westwards probably around 60,000 years ago from Eastern Europe, but its origin is still unknown. These two main European groups (Ursus spelaeus and Ursus ingressus) form the sister-group of the Caucasus cave bears (Ursus “deningeri” kudarensis). For these three major groups species status is discussed (Hofreiter et al., 2004a; Knapp et al., 2009). Under this scenario, the three subgroups within Ursus spelaeus would represent different subspecies (Fig. 2). Interestingly all these fossil groups of cave bears show a less pronounced phylogeographic pattern based on their mtDNA than modern groups of brown bears (Taberlet and Bouvet, 1994), as they exhibit overlapping spatial distribution (Hofreiter et al., 2004b). However, considering the time depth of these fossils and the difficulties to date them accurately, a sharper phylogeographic pattern might be hidden. Moreover, recent ancient DNA studies on brown bears also showed that their phylogeographic pattern before

Fig. 2. Schematic cave bear tree.

S.C. Münzel et al. / Quaternary International 245 (2011) 225e237

the last glacial maximum and still in the early Holocene was less pronounced than it is today (Hofreiter et al., 2004b; Valdiosera et al., 2007, 2008). In fact, the pronounced phylogeographic pattern observed for modern brown bears may at least partially be an artifact of the human-driven population reduction that brown bears experienced during the last millennia. Two areas of overlapping group distribution are of special interest. The hot spot of the species debate focuses on two caves in the Austrian Alps less than 10 km apart, namely Ramesch and Gamssulzen caves (Rabeder and Hofreiter, 2004; Rabeder et al., 2004; Bocherens et al., 2011a). In these two caves two very different mtDNA groups, namely Ursus s. eremus and Ursus ingressus, were found (Hofreiter et al., 2004a): the small sized bears in Ramesch (named “hochalpine Kleinform” by Ehrenberg, 1929) and the large-sized bears in Gamssulzen cave. Both forms lived side by side of each other for at least 15,000 years without evidence for gene flow between the two sites. The other area of interest is the Ach Valley in the Swabian Jura. Palaeogenetic investigations at three neighboring caves, namely Geißenkösterle, Hohle Fels and Sirgenstein (Fig. 1), near Blaubeuren have again revealed two different mtDNA groups of cave bears. In these three caves the classical western European cave bear (Ursus s. spelaeus), was replaced by the eastern European cave bear (Ursus ingressus) (Hofreiter et al., 2007). This replacement was dated to around 28,000 14C BP, within the cultural layers of the Gravettian. The appearance of Ursus ingressus in the Ach Valley is the westernmost evidence of this group so far. This result raised the question whether climatic/environmental changes or human impact were responsible for the replacement during this time. Another question is whether these changes are correlated with changes in the diet of the respective bears.

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2.2. Methods for stable isotope analysis The collagen extraction was performed following Bocherens et al. (1997). The elemental and isotopic measurements were performed at the Geochemical unit of the Department of Geosciences at the University of Tübingen (Germany), using an elemental analyzer NC 2500 connected to a Thermo Quest Delta þ XL mass spectrometer. The isotopic ratios are expressed using the “d” (delta) value as follows: d13C ¼ [(13C/12C)sample/(13C/12C)reference e 1]  1000 (&) and d15N ¼ [(15N/14N)sample/(15N/14N)reference e 1]  1000 (&), with the international reference being V-PDB for d13C values and atmospheric nitrogen (AIR) for d15N values. Samples were calibrated to d13C values of USGS24 (d13C ¼ 16.00&) and to d15N values of IAEA 305A (d15N ¼ 39.80&). The reproducibility was
0.1& for d13C measurements and
0.2& for d15N measurements, based on multiple analysis of purified collagen from modern bones. The reliability of the isotopic signatures of the collagen extracts was addressed using their chemical composition. Only extracts with %C, %N, and C/N similar to those of collagen extracted from fresh bone should be considered reliable for isotopic measurements. Several studies have shown that collagen with atomic C/N ratios lower than 2.9 or higher than 3.6 are altered or contaminated, and should be discarded (DeNiro, 1985; Ambrose, 1990). Extracts with 2.9  C/N  3.6 and %N < 5% may also be problematic (Ambrose, 1990) and were also excluded from further palaeobiological interpretations. Non-parametric tests were performed to decipher significant differences in d13C and d15N values. The WilcoxoneKruskaleWallis test was applied on taxonomic groups that contained at least five samples using JMPÒ 8 software. The chi square and p-values are given with one degree of freedom (DF) in each case. Differences can be considered statistically significant for p < 0.01.

2. Material and methods 2.3. Methods for ancient DNA analysis 2.1. Material For the initial palaeogenetic study in the Ach Valley the dentine of fourteen 3rd upper and two lower 2nd incisors of cave bears from Geißenklösterle and Hohle Fels and of three lower 1st molars from Sirgenstein (Table 1) were sampled, sequenced and dated by Hofreiter et al. (2002, 2007 and suppl.). In order to get appropriate isotopic data for different mammals, bones were sampled in the second phase of the study. Due to metabolic differences in the tissues, tooth dentine reveals higher 15N values than bone and is therefore not directly comparable to the values observed in bones (Bocherens et al., 1994, 1997). Therefore, metapodials (Tables 1 and 2) of cave and brown bears were sampled as their compact and solid structure is an advantage for good molecular preservation essential for ancient DNA and isotope studies using collagen. Furthermore they provide the chance of having butchering marks, as evidence of human impact on this potential game species. Specimens were selected from all stratigraphic units, taking care to avoid metapodials from the same individual. While the isotopic analysis was conducted on all metapodials selected for this study (Table 2), the genetic analysis showed a few specimens to not have preserved aDNA. Radiocarbon dates were obtained from the majority of specimens, focusing especially on the Gravettien layers relevant for the replacement of U. spelaeus by U. ingressus, the extinction of all cave bears and their replacement by brown bears. A large skull was sampled from the uppermost Gravettian layer AH IIb in Hohle Fels (Fig. 3). So far, it is the only complete skull from the recent excavations. Thus, it was necessary to determine whether this skull corresponds genetically to the large-sized bear from Gamssulzen cave in Austria, cave site for the holotype of Ursus ingressus (Rabeder et al., 2004).

In addition to the sequences available from previous publications (Hofreiter et al., 2007; Münzel et al., 2007, 2008) 43 cave bears (40 metapodials, two maxillae and a skull) and two brown bear metapodials have been investigated in this study (Tables 1 and 2). Between 150 and 500 mg of powdered bone were used to extract DNA using a silica-based aDNA extraction protocol (Rohland et al., 2007). Both DNA extractions and PCR amplification setups were performed in a laboratory dedicated exclusively to ancient DNA work and physically separated from all post-PCR procedures. Primers CBL164 (3F) 5’-GCATATAAGCATGTACATATTATGC-30 and CBH221 (3R) 50 -CGGACTAAGTGAAATACATGCT-30 (originally published by Hofreiter et al., 2004b) were used to amplify a 103 base pairs (bp) fragment (56 bp excluding primers) of the mitochondrial control region. The amplification conditions were adopted from Hofreiter et al. (2004b) as well. Diagnostic nucleotide positions within the amplified region allowed first, to distinguish between brown bear and cave bears and second, distinguish between the three main groups of cave bears, namely Ursus spelaeus, Ursus ingressus and Ursus “deningeri“ kudarensis. To rule out any determination of erroneous sequences due to miscoding lesions in the ancient DNA, all amplifications were done in replicates. Furthermore, negative controls were performed at all steps to monitor possible contamination. Subsequently, all PCR products were either cloned using the TOPO TA cloning kit (Invitrogen) and Sanger sequenced as described in Stiller et al. (2010), or individually barcoded, pooled in equimolar ratios and then sequenced on the 454 FLX platform using the DMPS protocol (Stiller et al., 2009). The sequences were then sorted by individuals and PCR replicates (in case of the 454 data the “untag”-tool (http://bioinf.eva.mpg.de/pts/) was used to sort by barcode), aligned and a consensus sequence for

228

Table 1 Radiocarbon dates of Ursus spelaeus, Ursus ingressus and Ursus arctos, used in Fig. 6, calibrated after Reimer et al. (2009). Sites: GK ¼ Geißenklösterle; HF ¼ Hohle Fels; SI ¼ Sirgenstein; SCH ¼ Schussenquelle. Square/find #

Geol/arch layer

Taxon

Element

Genbank accession #

mtDNA -haplotype

14C-Lab

14C-date

sdþ

sd-

Reference 14C-date

GK SI GK GK GK SI HF GK GK GK HF GK HF GK

69/183 0/1 100/72 140/101 78/145 0/2 79/630 69/141/121 87/39 96/88 89/126 87/385 89/578

5/Ir I 4/6/Is 5/Ir I 3a/IIa 5c/Ir 5/Ir 5a/3b/IIb 5d/Ir 3b/IIb 12/IIa

U. U. U. U. U. U. U. U. U. U. U. U. U. U.

ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus ingressus

Maxilla, juvenile Lower M1 Metacarpal 1 Upper I3 Upper I3 Lower M1 Metacarpal 5 Maxilla, juvenile Upper I3 Lower I2 Complete skull Lower I2 Metatarsal 2 Metacarpal 4

FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733656 FR733657

ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_1 ingr_2

GrA-39687 OxA-12013 GrA-43836 Beta-143244 Beta-143243 OxA-12014 GrA-43923 GrA-39700 Beta-161019 Beta-161018 GrA-43702 Beta-161020 GrA-43914 GrA-43906

24,210 25,560 26,230 26,530 26740 26,980 27,090 27,180 27,240 27,340 27,420 27,870 28,330 32,000

100 130 140 120 120 130 130 130 200 180 150 190 140 220

100 130 140 120 120 130 130 130 200 180 150 190 140 200

Münzel et al., 2008 Hofreiter et al., 2007 this publication Hofreiter et al., 2007 Hofreiter et al., 2007 Hofreiter et al., 2007 this publication this publication Hofreiter et al., 2007 Hofreiter et al., 2007 this publication Hofreiter et al., 2007 this publication this publication

HF GK HF HF HF HF HF HF HF HF GK GK GK HF GK GK HF GK GK GK GK GK GK SI GK

89/413 58/55 29/856 86/4 78/1284 57/911 58/756 79/1839 78/338 58/112 0/112 67/211 36/129 67/1461 57/2370 15/195 58/2118 78/421 88/703 86/121 0/109 68/415 67/1270 0/3 110/445

3c/IIc 7/It 3c/IIc 1k/I 3c/IIc 3b/IIb 3c/IIc 3cf/IIcf 3a/IIa 3b/IIb 7-12/It-IIa 6/Is 10/Ic 3c/IIc 16/IIIa 11/IIn 3c/IIc 10/Ic 12/IIa 10/Ic 7/It 13/IIb 15/III I 15/III

U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U.

spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus

Metatarsal 2 Metatarsal 3 Upper I3 Upper I3 Upper I3 Upper I3 Upper I3 Metatarsal 2 Metatarsal 1 Upper I3 Metatarsal 4 Metatarsal 1 Metacarpal 1 Metatarsal 2 Upper I3 Upper I3 Metatarsal 2 Metatarsal 2 Upper I3 Metacarpal 1 Metatarsal 3 Upper I3 Metacarpal 5 Lower M1 Upper I3

FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733653 FR733654 FR733653 FR733654 FR733653 FR733653 FR733655 FR733654 FR733654 FR733655 FR733654 FR733654 FR733654 FR733654

spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_1 spel_2 spel_1 spel_2 spel_1 spel_1 spel_3 spel_2 spel_2 spel_3 spel_2 spel_2 spel_2 spel_2

GrA-43915 GrA-43841 Beta-161022 Beta-161021 Beta-156094 Beta-161023 Beta-156093 GrA-43913 GrA-43924 Beta-156092 GrA-43902 GrA-43838 GrA-43843 GrA-43912 Beta-156091 Beta-156088 GrA-43908 GrA-43842 Beta-143245 GrA-43837 GrA-43839 Beta-156089 GrA-43907 OxA-12015 Beta-156090

27,440 27,720 27,840 28,040 28,060 28,170 28,170 28,200 28,250 28,350 28,360 28,360 28,500 28,750 28,780 29,390 30,370 30,800 31,090 31,710 32,990 33,350 34,400 35,770 38,010

140 160 190 200 170 190 180 140 150 220 150 170 170 150 730 210 170 210 200 230 260 340 260 330 520

140 160 190 200 170 190 180 140 150 220 150 170 170 150 730 210 170 210 200 210 240 340 230 330 520

this publication this publication Hofreiter et al., 2007 Hofreiter et al., 2007 Hofreiter et al., 2007 Hofreiter et al., 2007 Hofreiter et al., 2007 this publication this publication Hofreiter et al., 2007 this publication this publication this publication this publication Hofreiter et al., 2007 Hofreiter et al., 2007 this publication this publication Hofreiter et al., 2007 this publication this publication Hofreiter et al., 2007 this publication Hofreiter et al., 2007 Hofreiter et al., 2007

HF HF HF HF HF GK GK GK GK

58/219 79/444 65/1049 77/195 79/2695 89/527 110/312 78/1495 78/1495

1br/I 3a/IIa 3c/IIc 3g/I-II 8/V 11/IIn 10/Ic 18/IV 18/IV

U. U. U. U. U. U. U. U. U.

arctos arctos arctos arctos arctos arctos arctos arctos arctos

Metacarpal 3 Lower M2 Metacarpal 1 Metacarpal 5 Metatarsal 1 Metatarsal 1 Metacarpal 5 Femur, juvenile Femur, juvenile

n.a. arct_1 n.a. n.a. n.a. arct_1 arct_1 n.a. n.a.

GrA-43918 Beta-171312 GrA-43922 GrA-43917 GrA-43919 GrA-43904 GrA-43901 OxA-19750 KIA-19556

13.170 14.600 27.850 28.330 29.830 30.320 30.560 36.000 37.780

50 60 130 140 170 190 180 500 520

50 60 130 140 170 190 180 500 490

this publication Münzel et al., 2007 this publication this publication this publication this publication this publication this publication Münzel et al., 2007

FR733658 FR733658

cal-2s

suppl suppl suppl suppl

suppl suppl suppl

suppl suppl suppl suppl suppl

suppl

suppl suppl

suppl

suppl suppl suppl

calþ2s

cal BP, med-2s

sd(2s)

Isotope sample #

Collagen content not reliable 29,757 30,819 30288 531 30,614 31,174 30894 280 30,941 31,271 31106 165 31,027 31,354 31190.5 163.5 31,111 31,487 31299 188 31,152 31,543 31347.5 195.5 31,183 31592 31387.5 204.5 31,145 31,756 31450.5 305.5 31,194 31,860 31527 333 31,254 31,912 31583 329 31,480 32,703 32091.5 611.5 31,976 33,184 32580 604 35,596 36,970 36283 687

TUB-91 TUB-38 TUB-01 TUB-27 TUB-26 TUB-39 TUB-85 TUB-55 TUB-25 TUB-23 TUB-96 TUB-24 TUB-70 TUB-16

31,272 31,407 31,462 31,577 31,617 31,689 31,702 31,805 31,858 31,851 31,996 31,964 32,103 32,642 31,578 33,415 34,627 34,776 35,042 35,327 36,829 36,997 38,715 40,218 41,784

31,920 32,439 32,668 32,909 32,889 33,056 33,042 33030 33,110 33304 33,225 33,249 33384 34,091 34,666 34,622 35,163 36,258 36,307 36,703 38,545 38,859 40,244 41,637 43,291

31596 31923 32065 32243 32253 32372.5 32372 32417.5 32484 32577.5 32610.5 32606.5 32743.5 33366.5 33122 34018.5 34895 35517 35674.5 36015 37687 37928 39479.5 40927.5 42537.5

324 516 603 666 636 683.5 670 612.5 626 726.5 614.5 642.5 640.5 724.5 1544 603.5 268 741 632.5 688 858 931 764.5 709.5 753.5

TUB-72 TUB-05 TUB-50 TUB-45 TUB-47 TUB-42 TUB-49 TUB-69 TUB-87 TUB-46 TUB-09 TUB-03 TUB-07 TUB-65 TUB-34 TUB-29 TUB-62 TUB-06 TUB-30 TUB-02 TUB-04 TUB-31 TUB-18 TUB-40 TUB-33

15,380 17,457 31,495 31,976 34,001 34,600 34,650 40,039 41,646

16,577 18,029 32,556 33,184 34,890 35,151 35,366 42,023 43,134

15978.5 17743 32025.5 32580 34445.5 34875.5 35008 41031 42390

598.5 286 530.5 604 444.5 275.5 358 992 744

TUB-82 n.a. TUB-84 TUB-81 TUB-83 TUB-14 TUB-08 TUB-53 TUB-53

S.C. Münzel et al. / Quaternary International 245 (2011) 225e237

Cave site

S.C. Münzel et al. / Quaternary International 245 (2011) 225e237

229

Table 2 Stable isotope results of d15N and d13C for Ursus spelaeus, Ursus ingressus and Ursus arctos, included in Fig. 7 (isotope values for the other species see Bocherens et al., 2011b, this volume) (Abbreviations for the cave sites see Table 1).

*

d13C

d15N

34.8 12.1 3.4 26.7 9.0 3.4 42.6 15.2 3.3 42.5 15.6 3.2 40.7 14.9 3.2 39.4 13.9 3.3 Average U. ingressus sd 39.1 14.1 3,2 35.4 13.1 3.2 41.6 14.3 3,4 39.3 13.9 3.3 33.3 11.5 3.4 41.6 14.2 3.4 39.3 14.6 3.1 34.4 11.8 3.4 25.0 8.5 3.4 39.3 13.8 3.3 44.1 14.6 3.5 34.0 12.0 3.3 30.8 11.0 3.3 33.4 11.5 3.4 34,5 12.7 3.2 36.9 13.0 3.3 39.7 15.1 3.1 40,9 14.2 3.4 43.7 15.4 3.3 41.9 15.1 3.2 41.3 15.3 3.1 42.7 15.5 3.2 43.2 15.4 3.3 43.2 15.7 3.2 42.8 14.9 3.4 39.6 15.6 3.0 39.9 14.5 3.2 41.9 14.7 3.3 42.9 15.3 3.3 40.8 14.8 3.2 41.6 15.1 3.2 41.6 15.0 3.2 Average U. spelaeus sd

21.0 20.9 21.1 20.9 20.6 21.3 21.0 0.2 20.8 20.8 21.0 20.3 20.8 20.3 21.0 21,2 20.7 20.6 21.1 20,7 20.8 21.2 20.8 20.8 21.1 21.3 20.8 21.1 21.0 21.1 20.7 21.1 20.7 20.8 21.2 20.6 20.4 20.8 20.9 21.2 20.9 0.3

4.0 1.1 3.9 3.7 2.8 4.0 3.3 1.0 1.7 2.9 3.4 2.5 1.8 3.0 2.8 2.0 2.7 2.3 2.3 2.3 3.0 3,1 2.8 3.0 4.2 4.8 3.8 2.7 3.6 3.5 4.2 4.2 4.4 3.2 4.3 4.0 2.9 3.9 3.1 4.1 3.2 0.8

41.6 16.4 3.0 36.9 14.0 3.1 41.8 15.1 3,2 43.3 15.6 3.2 41.9 15.1 3.2 42.8 15.2 3.3 U. spelaeus + U. spec. sd

20.8 21.5 20.7 21.2 20.9 20.5 20.9 0.3

0.0 4.0 3,2 2.9 4.9 2.0 3.2 1.0

86.4 36.5 14.2 3.0 130.8 29.1 9.5 3.6 90.0 42.6 15.3 3.3 93.9 42.1 15.1 3.3 51.3 38.5 13.7 3.3 118.3 42.4 14.9 3.3 Average U. arctos pre-LGM sd

19.5 19.3 19.1 19.3 19.4 19.4 19.3 0.1

8.3 9.1 10.5 7.3 8.1 9.6 8.8 1.1

3.4 120.5 40.6 15.0 3.2 Values: Bocherens et al., 2011b, this vol Values: Bocherens et al., 2011b, this vol Values: Bocherens et al., 2011b, this vol Average U. arctos post-LGM sd

19.3 18.7 20.6 20.3 19.7 0.8

4.0 4.7 3.3 2.8 3.7 0.7

Isotope sample #

Cave site

Square/ find #

Geol/arch layer

Taxon

mtDNA haplotype

Element

%N bone

Collagen yield

%C

TUB-01 TUB-16 TUB-55 TUB-70 TUB-85 TUB-96

GK GK GK HF HF HF

100/72 89/578 69/87/385 79/630 96/88

4/12/IIa 5c/Ir 3b/IIb 3a/IIa 3b/IIb

U. U. U. U. U. U.

ingressus ingressus ingressus ingressus ingressus ingressus

ingr_1 ingr_2 ingr_1 ingr_1 ingr_1 ingr_1

Metacarpal 1 Metacarpal 4 Maxilla, young Metatarsal 2 Metacarpal 5 Complete skull

1.0 2.8 2.5 3.6 3.0 1.1

42.7 61.5 62.1 104.9 84.8 30.0

TUB-02 TUB-03 TUB-04 TUB-05 TUB-06 TUB-07 TUB-09 TUB-10 TUB-11 TUB-12 TUB-13 TUB-15 TUB-17 TUB-18 TUB-19 TUB-20 TUB-21 TUB-22 TUB-61 TUB-62 TUB-63 TUB-64 TUB-65 TUB-66 TUB-68 TUB-69 TUB-71 TUB-72 TUB-87 TUB-88 TUB-89 TUB-90

GK GK GK GK GK GK GK GK GK GK GK GK GK GK GK GK GK GK HF HF HF HF HF HF HF HF HF HF HF HF HF HF

86/121 67/211 0/109 58/55 78/421 36/129 0/112 88/760 69/548 120/447 46/444 68/600 76/425 67/1270 100/300 110/461 36/625 36/663 26/261 58/2118 59/1530 59/1823 67/1461 68/2217 78/1951 79/1839 87/1467 89/413 78/338 59/1601 10/800 10/771

10/Ic 6/Is 7/It 7/It 10/Ic 10/Ic 7-12/It-IIa 12/IIa 13/IIb 12/IIa 13/IIb 15/III 12/IIa 15/III 15/III 15/III 17/18/IV 5wf/3c/IIc 3d/IId 6ab/IIIab 3c/IIc 3d/IId 3d/IId 3cf/IIcf 7/IV 3c/IIc 3a/IIa 1ek/I 1ek/I 1ek/I

U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U. U.

spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus spelaeus

spel_2 spel_1 spel_3 spel_1 spel_3 spel_2 spel_1 spel_3 spel_2 spel_3 spel_2 spel_2 spel_2 spel_2 spel_2 spel_2 spel_2 spel_2 spel_1 spel_1 spel_2 spel_2 spel_1 spel_2 spel_2 spel_1 spel_1 spel_1 spel_1 spel_2 spel_1 spel_2

Metacarpal 1 Metatarsal 1 Metatarsal 3 Metatarsal 3 Metatarsal 2 Metacarpal 1 Metatarsal 4 Metatarsal 3 Metatarsal 3 Metatarsal 4 Metatarsal 2 Metatarsal 4 Metatarsal 1 Metacarpal 5 Metatarsal 5 Metacarpal 1 Metatarsal 5 Metacarpal 5 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 1 Metatarsal 1 Metatarsal 5 Metacarpal 1

3.2 4.2 3.6 3.2 3.8 2.6 3.0 3.3 2.8 3.8 3.7 4.0 1.9 3.1 2.7 3.0 3.1 2.8 3.7 3.6 3.3 3.9 3.8 3.7 3.4 3.8 3.6 3.1 4.0 3.4 3.7 3.6

126.5 174.1 150.4 110.4 128.2 94.2 118.6 64.2 74.6 143.5 133.7 90.9 31.9 69.0 85.4 52.3 102.5 78.2 133.1 114.5 108.7 131.2 168.7 101.9 81.7 nd 89.1 46.9 109.8 74.3 105.2 102.9

TUB-52 TUB-54 TUB-59 TUB-60 TUB-67 TUB-86

HF GK HF HF HF HF

59/2256 56/1662 58/575 55/1287 75/131 69/333

9/VI 22/VIII 3b/IIb 3d/IId 3bl/IIb 3ad/IIa

U. U. U. U. U. U.

spec. spec. spec. spec. spec. spec.

n.a. n.a. no DNA no DNA no DNA no DNA

Metacarpal 2 Rib Metatarsal 2 Metatarsal 2 Metatarsal 2 Metatarsal 3

3.9 134.8 2.6 28.4 3.2 83.2 3.7 122.3 3.4 112.1 3.2 85.9 Average U. ingressus +

110/312 89/527 78/1495 77/195 79/2695 65/1049

10/Ic 11/IIn 18/IV 3g/I-II 8/V 3c/IIc

U. U. U. U. U. U.

arctos arctos arctos arctos arctos arctos

arct_1 arct_1 n.a. n.a. n.a. n.a.

Metacarpal 5 Metatarsal 1 Femur, juvenile Metacarpal 5 metatarsal 1 Metacarpal 1

3.8 3.8 3.2 3.6 3.4 3.8

1br/I

U. U. U. U.

arctos arctos arctos arctos

n.a. n.a. n.a. n.a.

Metacarpal 3 Mandible, right Mandible, left* Mandible, right*

Ursus arctos TUB-8 TUB-14 TUB-53 TUB-81 TUB-83 TUB-84

- pre-LGM GK GK GK HF HF HF

Ursus arctos TUB-82 TUB-56 SCH-8* SCH-9*

- post-LGM HF 58/219 Buttentalhöhle Schussenquelle Schussenquelle

Inv: 4815.1 Inv: 4815.2

Mandibles come from two different individuals.

%N

C/N

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Fig. 3. Complete Ursus ingressus skull (HF 96/88) from Hohle Fels.

each individual was called using the software BioEdit (Hall, 1999). No consistent nucleotide differences have been observed between PCR replicates of any of the individuals suggesting that miscoding lesions are not affecting the quality of the consensus sequences. The PCR product for the skull sample TUB-96 was directly converted into a Illumina multiplex library as described in Meyer

and Kircher (2010) carrying a specific p7 adapter with index sequence (50 ACCACCG 30 ) and was sequenced on the Illumina Genome Analyzer IIx platform using 2  76 þ 7 cycles on a sequencing lane together with other libraries according to the manufacturer’s instructions (FC-104-400x v4 sequencing chemistry and PE-203-4001 cluster generation kit v4). The raw reads

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were aligned to a PhiX 174 reference sequence to obtain a training data set for the base caller Ibis (Kircher et al., 2009). Raw sequences called by Ibis 1.1.1 were filtered for the index as described (Kircher et al., 2009). The paired-end reads were subjected to a fusion process (including removal of adapter sequences and adaptor dimers) requiring at least 11 nucleotides overlap between the two reads. In the overlapping sequence, quality scores were combined and the base with the highest base quality score was called. Only sequences merged in this way were used for further analysis. In total 6857 sequences with the right index sequence were observed and used as input for a custom iterative mapping assembler (Green et al., 2008). In total 4465 fragments were found to align to cave bear mtDNA. All fragments were used to create the 56 bp consensus sequence (excluding primers) for sample TUB-96. Based on the consensus sequences from Sanger, Roche/454 and Illumina sequencing, all individuals could be unambiguously identified as brown bears or one of the three groups of cave bears (namely Ursus spelaeus, Ursus ingressus and Ursus “deningeri“ kudarensis). 3. Results and discussion 3.1. Genetic replacement After the first series of dated samples, the genetic replacement of the cave bears in the Ach Valley seemed to happen suddenly around 28,000 14C BP (Hofreiter et al., 2007) resp. 32,000 cal BP (calibration of radiocarbon dates according to Reimer et al., 2009). The new radiocarbon dates however, show a different picture (Fig. 6, Table 1). There is evidence for the appearance of Ursus ingressus already 4000 years earlier, starting around 32,000 BP (resp. 36,000 cal BP), suggesting that the immigration of the new group might have occurred more gradually (Fig. 6). This conclusion is so far based on only one individual and will need to be further evaluated, e.g. by re-dating of this specimen. Even if the early occurrence of Ursus ingressus can be verified, it might just represent a single migrating individual. However, analyses of further individuals would be necessary to fully understand the process of immigration of U. ingressus into the Ach valley region. Independent of the details of this process, once established, Ursus ingressus remained the only genetic type of cave bear after the local extinction of Ursus spelaeus. Considering the earliest appearance of Ursus ingressus in Geißenklösterle at 32,000 þ 220e200 BP and the latest occurrence of Ursus spelaeus dated to 27,440
140 BP (GrA-43915) in the Hohle Fels (Table 1) there remains a time span of about 4500 years of possible cohabitation or occasionally overlapping ranges of the two genetic types in the Ach Valley. Disregarding the date of 24,210
100 BP for Ursus ingressus in Geißenklösterle, which is not reliable because of insufficient collagen content, then the latest occurrence of Ursus ingressus in the Ach Valley is dated to 25,560
130 BP in Sirgenstein (Table 1). Thus, Ursus ingressus survived Ursus spelaeus for another 2000 years. The date of 27,440
140 BP for the latest occurrence of the classical cave bear (Ursus s. spelaeus) in the Ach Valley seems to represent the demise of this group. The youngest date for Ursus spelaeus with known genetic provenience in Western Europe comes from Goyet in Belgium (27,440
160 BP, Germonpré, 2004) and is indistinguishable from the latest of the Swabian Jura. The reasons for the extinction of Ursus spelaeus are still unclear. Climatic and environmental changes are one possible explanation for the extinction of this group of cave bears. The composition of the large mammal fauna (Fig. 5; Münzel and Conard, 2004a) and the avifauna (Boessneck and von den Driesch, 1973; Krönneck, 2009) shows some changes that could be linked with a gradual climatic deterioration from the Aurignacian (35e30,000 BP) to the Gravettian (30e27,000 BP) layers. In the Gravettian layers of the

231

Ach Valley caves, namely Hohle Fels (Münzel and Conard, 2004b), Geißenklösterle (Münzel and Conard, 2004a) and Brillenhöhle (Boessneck and von den Driesch, 1973), the percentage (NISP%) of hare, Lepus sp. (Fig. 5) and ptarmigan, Lagopus sp. increases indicating a more open tundra-like landscape. Another indication for a richer and more diverse vegetation cover before the Gravettian period is the evidence of four cervid species in the Ach Valley, namely giant deer (Megaloceros giganteus), red deer (Cervus elaphus), reindeer (Rangifer tarandus) and roe deer (Capreolus capreolus) (Münzel and Conard, 2004a). These cervids could cover their different nutritional needs during the Aurignacian in contrast to the situation during the Gravettian with only reindeer and red deer being present. Furthermore there is evidence for saiga (Saiga tatarica) from the Gravettian layers of Brillenhöhle, which indicates cooler and dryer climatic conditions (Boessneck and von den Driesch, 1973). To better understand the apparent coexistence of these different ungulates, more stable isotopic work needs to be done in the Swabian Jura. This research should also address dietary preferences of ungulate species and habitat canopy since the ecological preferences during the Late Pleistocene varied (Drucker et al., 2005, 2008, 2010). The reconstruction of the population dynamics of bears using ancient mtDNA modelled by Stiller et al. (2010) provides strong evidence that the extinction of cave bears (sensu lato) was not only the effect of climatic deterioration associated with the coming LGM, but rather a withering away over the course of as much as 25,000 years, starting already 50,000 radiocarbon years ago. In contrast, the population size of their sister species the brown bear, remained more or less stable during this period (Stiller et al., 2010). This raises the question of how much each of the main groups contributed to the large scale ‘withering away’ and the ultimate extinction of cave bears (sensu lato). Although only based on a small sample size and a short overall time range, a trend toward decreasing genetic diversity can be observed looking at the number of Ursus spelaeus haplotypes from the Ach Valley (see Table 1: the occurrence of haplotypes spel_1, 2, 3 and ingr_1, 2). Another scenario of human hunters driving ‘spelaeus’ to extinction, which gave ‘ingressus’ the chance to transiently fill this niche in the Ach Valley, was proposed from archaeozoological side (SCM) and discussed in Hofreiter et al. (2007). Although cut marks are present on some of the metapodials under consideration, the sample size in this study is too small to draw any conclusions regarding the impact on the respective genetic group (3 metapodials with cut marks for U. spelaeus, 2 for U. arctos and none for U. ingressus). The lone occurrence of U. ingressus earlier than the final replacement of U. spelaeus by U. ingressus may weaken this scenario, but one could also suggest that increased hunting pressure could give exactly this picture. If the population size decreased over time, for species such as bears, an expected pattern might be an initial small scale migration and later a complete replacement as the local population went extinct and was replaced by incoming individuals, which soon after were also driven to extinction by human hunting pressure. This scenario also fits very well with the long-term population decline globally observed for cave bears (Stiller et al., 2010). Since the genetic information in the mitochondrial DNA does not influence the phenotype of a species, it cannot be certain that visual differences existed that hunters were able to recognize. While a metrical analysis of metapodials by Withalm (2001) showed some differences between the cave bears from Ramesch (Ursus s. eremus) and Gamssulzen cave, the type locality of Ursus ingressus, in the Austrian Alps, a biostatistical investigation of metapodials of the two bear taxa in the Ach Valley compared to Ursus ingressus from Gamssulzen cave revealed no significant metrical differences (Münzel and Athen, 2009). However, the recently found large skull

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from Hohle Fels (TUB-96) seemed to have a different morphology compared to cave bear skulls from other caves in the Swabian Jura. To date this is the only Ursus ingressus skull, for which both ancient DNA and isotope data have been obtained. Further work will need to be done in order to study the relationship between morphology, genetic proveniance and paleobiology of the cave bears in the Swabian Jura and elsewhere. Another question is which factors were responsible for the different population dynamics of brown and cave bears? Stiller et al. (2010) favours the idea of a competition for shelter, since both modern humans and Neanderthals would have been strong competitors for these caves and might have forced cave bears into

less suitable hibernation dens. However, hunting played an additional role and might have had considerable impact, not necessarily on a single genetic group, but on the cave bear population as a whole (Münzel et al., 2001; Münzel and Conard, 2004b). For cave bears it was fatal to prefer caves for hibernation. In these dens they were easy to locate in contrast to brown bears which at least nowadays favour dens in the open landscape, however natural caves are also reported by Heptner and Naumov (1974, 435e436). Furthermore, evidence for hunting of cave bears in the Ach Valley is given by numerous cut and impact marks on cave bear bones (Fig. 4), and in a thoracic vertebra from Hohle Fels with a projectile point still sticking in the bone (Münzel and Conard, 2004b, 881). The hunting

Fig. 4. Cave bear bones with cut marks from Hohle Fels. 1a, b) Metatarsal with cut marks from skinning; 2a, b) Canine of a young cave bear in its 2nd winter; 3a, b) Mandible fragment of a juvenile cave bear with cut marks; 4a, b) Dens of the 2nd cervical vertebra of a juvenile cave bear with cut mark caused by dismemberment of the head.

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233

Fig. 5. Faunal composition (%NISP) of the main cultural layers in Hohle Fels.

season for cave bears must have been winter during dormancy. Evidence for the hunting season is given by cave bear remains of known age with butchering marks (Figs. 4-2) and by the presence of fetal horse bones aged to the 6th to 7th month of pregnancy (Münzel and Conard, 2004b, 882, Fig. 13). This human impact for hunting of cave bears is much clearer and more pronounced for the Upper Palaeolithic layers, but it can be traced also for the Middle Palaeolithic layers (Münzel and Conard, 2004a), suggesting a long-term influence of hunting on cave bear populations. At present it is not possible to select which hypothesis is correct but further work is planed to test the plausibility of these scenarios. It is likely that different factors affected the population dynamics of cave bears between 32,000 and 26,000 years ago in the Swabian Jura. The authors agree with Barnosky et al. (2004) that human hunting is not solely responsible for the megafaunal extinction, rather a combination of several factors. In general the palaeobiology of the respective species should be taken more into consideration. The hunter’s knowledge about the behavior of its prey is essential for the hunting success. The coincidence of cut marks on the cave bear bones and the determination of a winter occupation of the Ach Valley caves show that the Palaeolithic hunters took advantage of the fact that cave bears hibernated in these caves. Certainly, it is not known how many cave bears hibernated in the Ach Valley, but if Palaeolithic hunters ambushed cave bears on a regular base, they can be considered an endangered species. The archaeological record of the Swabian Jura shows a much higher density of artefacts and all classes of cultural material in the Aurignacian and Gravettian relative to the Middle Palaeolithic. Neanderthals of the Middle Palaeolithic coexisted successfully with cave bears for several ten thousand years. The increased population densities of Aurignacian and Gravettian hunters and the increased evidence for killing and butchering of cave bears strongly suggest that modern humans contributed to the extinction of cave bears via over hunting and by competition with bears for denning space and other resources (Conard et al., 2006). Therefore, more regional and species specific studies are needed to determine the hunter/prey relationship before searching for global models of megafaunal extinction (Barnosky et al., 2004). 3.2. Dating the extinction of cave bears Until quite recently, the Swabian Jura was thought to be a refuge area in which cave bears survived the Last Glacial Maximum (LGM)

(Kurtén, 1976; Koenigswald, 1983; Münzel et al., 2007). This hypothesis was supported by cave bear remains in Magdalenian layers dating to 12e13,000 BP in several caves of the Ach Valley, such as Brillenhöhle (Boessneck and von den Driesch, 1973), Sirgenstein (Koken in Schmidt, 1912, 165e171), Geißenklösterle (Münzel and Conard, 2004a), and Hohle Fels (Münzel and Conard, 2004b). Furthermore a maxilla of a juvenile bear from Geißenklösterle had been dated to 13,230
130 BP (OxA-4854) (Münzel et al., 2007). This raised the question on the palaeogenetic status of this bear surviving the LGM, U. arctos, U. spelaeus or U. ingressus? The ancient DNA result was “ingressus”, but a second dating of this specimen turned out to be much older, namely 24,210
100 BP (GrA-39687) (Münzel et al., 2008). After testing the collagen content of this maxilla (GK 69/183, TUB-91) it appeared to be of insufficient quality to give reliable dates, with a C/N ratio of 2.4, well outside the acceptable range of 2.9e3.6 (DeNiro, 1985). Therefore a second “ingressus” sample (TUB-55) of the same layer was dated and gave an even older date, namely 27,180
130 BP (GrA-39700). These new dates are consistent with other European cave bear radiocarbon dates (Pacher and Stuart, 2009) and place the extinction of cave bear in South Germany well before the LGM. Thus, the idea of a post-glacial maximum refuge area for cave bears in the Swabian Jura can now be refuted. Nevertheless, there are some claims of post-LGM dates of cave bears in the French Jura and Massif Central (Argant et al., 2010), but these samples should be re-evaluated, as no DNA was retrieved. In view of the results of the re-dated cave bear specimen from Geißenklösterle, all claims of cave bears surviving the LGM should include (possibly even replicated) direct dating including detailed information on the chemical composition of collagen to verify the reliability of the date, as well as genetic analysis of the same particular bone to ensure the species status of the specimens in question. 3.3. Ecology of cave bear versus brown bear Interestingly during the whole stratigraphical sequence of the Ach Valley, brown bears (belonging to the western lineage) were sympatric with cave bears as confirmed by directly dated specimens from Hohle Fels and Geißenklösterle (Fig. 6). According to Kurtén (1976) brown bears may occur in caves of the Old World, but are never very common. Possibly they preferred shelters other than caves as extant brown bears do (Heptner and Naumov, 1974). Therefore it is not known whether these few pre-LGM brown bears

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Fig. 6. Radiocarbon dates of Ursus spelaeus, Ursus ingressus and Ursus arctos, calibrated after Reimer et al., 2009 (see Table 1).

from Hohle Fels and Geißenklösterle hibernated there or if they were brought in by human hunters. After the disappearance of cave bears the presence of brown bears in caves increased (Kurtén, 1976) and this coincides with a sudden expansion of brown bear lineages after the Last Glacial Maximum (Korsten et al., 2009). That Hohle Fels was used by brown bears in post-LGM times for denning can be demonstrated by a 2nd lower molar, dated to 14,600
60 BP (Table 1). The development of its root fits with bears in their second winter, indicating that this individual hibernated in Hohle Fels. Possibly the rareness of brown bears in caves before the extinction of cave bears results from the competition for winter shelters with both cave bears and humans. Dietary preferences of extant bears are as diverse as their tooth morphology, ranging from pure meat eaters, such as the polar bear Ursus maritimus, to bamboo consumers, such as the panda Ailuropoda melanoleuca (e.g. Christiansen, 2007). The dental morphology of bears is twofold. Systematically the large canines place bears into the lineage of the carnivores, while the large multicusps cheek teeth are of omnivorous character (Kurtén, 1976). The enlarged cave bear molars were always noticed as a sign of herbivorous diet, adapted to chew large amounts of plant food (e.g. Rabeder et al., 2000). Thus dietary preferences are partly reflected in the morphology of the teeth, although the variability of tooth size is not directly related to the diet actually consumed and therefore cannot be used with certainty to evaluate the food preference of a specific specimen. Microwear studies of tooth crowns are one approach to gain data of the texture of the diet (Rivals et al., 2010). Quite recently the omnivory of cave bears was postulated by means of microwear analysis of cave bear teeth from Belgium (Peigné et al., 2009), but this interpretation was refuted because of missing comparability in extant bears with similar food preferences (Bocherens, 2009a). Thus, microwear studies of the teeth should be combined with stable isotope studies of bone collagen since this approach is still the most powerful tool to address questions about diet and palaeobiology of extinct species. This is especially true in the case of testing for herbivory of an omnivorous species, since the addition of animal proteins would be readily recorded in the bone collagen isotopic signature, as animal foods contain much higher proportions of proteins than plant foods (Bocherens, 2009b). Data on the trophic system of the last glacial fauna in the Ach Valley were retrieved from the d15N and d13C values of cave bear,

brown bear, cave lion, horse, reindeer, and chamois (for isotopic data on cave and brown bear, see Table 2, for the other species see contribution Bocherens et al., 2011b). As already documented by previous studies on cave bears (e.g., Bocherens et al., 1994, 1997, 2006, 2007, 2011a; Fernandez-Mosquera, 1998) the isotopic values for d15N of cave bears are very low (Fig. 7) ranging even below those of grazers such as horse, reindeer and chamois, and demonstrating a vegetarian diet. Furthermore cave bears yielded the most negative d13C values of all herbivores. When cave bears belonging to both genetic types are considered separately, no statistically significant difference was found for d13C and d15N values (Chisquare ¼ 0.5805 and p ¼ 0.4461 for d13C values, Chisquare ¼ 0.1026 and p ¼ 0.7487 for d15N values). Therefore, the genetic change is not related to dietary change, since the isotopic compositions indicate that both cave bear taxa Ursus spelaeus and Ursus ingressus were in dietary competition in the Ach Valley. In contrast to cave bears, the d15N values of brown bears before the Last Glacial Maximum (pre-LGM) are as high as those of the

Fig. 7. Ach Valley fauna with isotopic data (isotope value for bears, see Table 2, for other fauna see Bocherens et al., 2011b).

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cave lions, showing a clearly carnivorous signature. While the d13C values of the four lion specimens (Fig. 7) vary considerably indicating an individualistic prey choice (Bocherens et al., 2011b), the brown bears’ carbon isotope values are more restricted making a focus on specific game plausible. The brown bear isotopic values are close to those of hyenas, a pattern also observed in Belgian caves of similar age (Bocherens et al., 2011b). This suggests a prey choice for pre-LGM brown bears including a mixture of any herbivorous species occurring in the surrounding environment. After the Last Glacial Maximum, d15N values of brown bears are as low as those of the extinct cave bears, but their carbon values are quite divers. The two brown bear individuals from Schussenquelle (Schuler, 1994), a Magdalenian open air reindeer hunting site close to Schussenried, show more negative d13C values than the brown bears from the two cave sites Hohle Fels and Buttentalhöhle (Hahn, 1995). However, both groups indicate a shift towards a herbivorous diet (Fig. 7). These low d15N values also demonstrate that in postLGM time the absence of competition with cave bears enables brown bears to occupy their nutritional niche. A similar mostly vegetarian diet was documented using carbon and nitrogen isotopic signatures of Late-glacial brown bears from the western Alps (Döppes et al., 2008). 4. Conclusions In the Ach Valley, there were two separate waves of extinctions for cave bear, which is well documented by dense series of radiocarbon-dated specimens; first, the extinction of Ursus spelaeus, and later on the extinction of Ursus ingressus, which survived Ursus spelaeus by about 2000 years. The Swabian Jura is the westernmost evidence of Ursus ingressus, and the latest evidence of its migration westwards is found here. Once established, Ursus ingressus remains the only genetic group of cave bear and the question remains open why one group disappears earlier than the other one. Climatic deterioration in the harsh environment of the Swabian Jura well before the LGM coincides with the onset of the genetic demise of cave bears. Intensified human occupation of the caves during the early Upper Palaeolithic as well as increased hunting contributed to the initial genetic replacement, and the final extinction of cave bears in this area. In post-LGM times brown bears took over the nutritional niche previously occupied by cave bears, as shown by the stable isotope results of brown bears before and after the LGM. Furthermore, they seem to have used the caves more often for dormancy after cave bears went extinct. The new data provided in this case study of the Ach Valley further supports the view of multiple coinciding factors including environmental change, intra- and inter-specific competition, and anthropogenic interference jointly leading to the final extinction of cave bears. Acknowledgments The project was supported by the German Research Foundation (DFG: CO 226/14-1), the Max Planck Society, the Heidelberg Academy of Sciences and Humanities and the Heidelberg Cement Company. We also thank Dorothée Drucker, Panagiotis Kritikakis, Maria Malina, Andrea Orendi, Bernd Steinhilber, H. Taubald and Christoph Wissing for technical support. The Alexander von Humboldt Foundation financially supported the stay of H. Bocherens in Tübingen to perform a large part of this research project. References Ambrose, S.H., 1990. Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science 17, 431e451.

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