Isotopic tracking of large carnivore palaeoecology in the mammoth steppe

Quaternary Science Reviews 117 (2015) 42e71

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Invited review

Isotopic tracking of large carnivore palaeoecology in the mammoth steppe
Bocherens a, b, * Herve a b

€t Tübingen, Fachbereich Geowissenschaften, Pala €obiologie (Biogeologie), Ho €lderlinstr. 12, 72074 Tübingen, Germany Universita €t Tübingen, Ho €lderlinstr. 12, 72074 Tübingen, Germany Senckenberg Research Center for Human Evolution and Palaeoenvironment (HEP), Universita

a r t i c l e i n f o

a b s t r a c t

Article history: Received 30 September 2014 Received in revised form 17 March 2015 Accepted 20 March 2015 Available online

Isotopic tracking of carnivore palaeoecology is a relatively new approach that yielded important results for the study of the non-analogue mammoth steppe biome. After describing the prerequisite to apply this approach and the possible complications, the main achievements will be described for extinct carnivore species such as scimitar-tooth cat Homotherium serum, cave lion Panthera spelaea, giant short-faced bear Arctodus simus, cave bear Ursus spelaeus s.l., as well as for ancient representatives of extant species such as brown bear Ursus arctos and wolf Canis lupus. Isotopic tracking showed that scimitar-tooth cats in Alaska were not specialist proboscidean predators but rather generalist consumers of other large herbivores. The majority of cave lions analysed so far were focused on reindeer, some individuals were specialized on cave bears, especially in contexts of competition with cave hyenas. Giant short-faced bears in Alaska were not pure herbivores and consumed meat from reindeer, muskoxen and possibly other predators, but may have still incorporated plant resources in their menu. In contrast, all cave bear populations studied so far for which a clear dietary reconstruction could be done were virtually pure herbivores, only a few cases are still unclear. Interestingly, brown bears used the opposite extreme of the dietary spectrum when competing with other large bears such as cave bears and giant short-faced bears, i.e. were more carnivorous in Europe and more herbivorous in Alaska. Finally wolves seem to have been outcompeted by hyenas but became dominant predators during the Lateglacial in Europe to the expense of the last cave lions. The results obtained through this approach are also relevant for improving conservation strategies of endangered extant large carnivores. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Mammoth steppe fauna Carnivores Carbon-13 Nitrogen-15 Palaeodiet Trophic web

1. Introduction Large mammalian carnivores are key components of modern terrestrial ecosystems. As apex consumers in the trophic webs, they play an important role in controlling the populations of herbivores they prey upon, and therefore have an indirect but important impact on vegetation density and structure. Changes in the diversity and abundance of large mammalian carnivores can lead to spectacular modifications of terrestrial ecosystems (e.g. Terborgh et al., 2001; Johnson et al., 2007; Ripple et al., 2010; Estes et al., 2011; Ripple and Beschta, 2012; Ritchie et al., 2012). In addition predators control the spatial distribution of carcasses that play an

€t * Universita Tübingen, Fachbereich Geowissenschaften, €lderlinstr. 12, 72074 Tübingen, Germany. (Biogeologie), Ho E-mail address: [email protected]. http://dx.doi.org/10.1016/j.quascirev.2015.03.018 0277-3791/© 2015 Elsevier Ltd. All rights reserved.

Pal€ aobiologie

important role in resource dynamics in terrestrial ecosystems (e.g. Bump et al., 2009). During the late Pleistocene, between around 50,000 and 12,000 years ago, the terrestrial ecosystems of the middle and high latitudes of the Northern hemisphere were populated by a rich and diverse guild of large mammalian carnivores including more species than the same areas during the Holocene since around 12,000 years ago (e.g. Markova and Puzachenko, 2007; Harington, 2011). It is very likely that these large carnivores were also playing a key role in the ecosystem functioning at this time (Ripple and van Valkenburgh, 2010). The abundance and diversity of large predators in late Pleistocene Eurasia must have led to high levels of intraguild competition between the different taxa (e.g. García and
s, 2007). In addition, these carnivores were potentially Virgo acting as competitors, mutualistic partners, predators or prey of prehistoric humans that lived and expanded into this geographic realm during this period (Stiner, 2004; Rodríguez et al., 2012; Espigares et al., 2013). Therefore understanding the trophic

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position of these late Pleistocene large carnivores is important for many aspects of the reconstruction of terrestrial ecosystems during this period. Moreover, the extant carnivore populations present in middle and high latitudes are only relict populations compared to their Pleistocene predecessors, with modified genetic structure and reduced or shifted ecological niche (e.g. Hofreiter, 2007; Hofreiter and Barnes, 2010). It is therefore also important to reconstruct the palaeobiology of these carnivores to provide background information of their fundamental ecological niche for conservation biology and to evaluate to what extent ecological flexibility was involved in the survival or extinction of different late Pleistocene predators. The diversity and abundance of large mammalian carnivores was much larger than nowadays in terrestrial ecosystems until around 12,000 years ago, especially in terrestrial environments of high and middle latitudes. During the colder than today episodes of the last 50,000 years, the non-glaciated part of this geographical area, ranging from North-western Spain in Europe to Northern Yukon in North America was the realm of the so-called “mammothsteppe”, a productive ecosystem dominated by herbaceous plants, large herbivores and their predators (e.g., Guthrie, 1968, 1990; Zimov et al., 2012). This biome was the largest terrestrial ecosystem on Earth during this period, but has no modern analogue today. In terms of large mammal diversity, this ecosystem was more similar to extant savannah than to boreal or arctic terrestrial ecosystems that occupy this area under cold conditions nowadays, especially regarding the large predators, with lions, hyenas and gregarious large canids (Vereshchagin and Baryshnikov, 1992). One major difference between modern savannah and ancient mammoth fauna is the occurrence of several extinct or still extant members of the ursid lineage, a carnivore family that includes predatory as well as omnivorous or even strongly vegetarian members (e.g. Stirling and Derocher, 1990). Therefore the carnivores present in the Mammoth steppe Fauna represent an important component of this non-analogue terrestrial ecosystem. These carnivores included predatory species that rely essentially on the meat (>70%) of other vertebrates, usually called hypercarnivores (Van Valkenburgh, 2007). In the mammoth steppe ecosystem, this category is represented by felids and hyaenids. In contrast, some taxa exhibit a broader dietary spectrum, where meat represents less than 30% of the average diet (hypocarnivores: Van Valkenburgh, 2007). Several members of this trophic group are among the bears. Finally, an intermediate category called mesocarnivores is represented by the canids, such as wolves (Van Valkenburgh, 2007). All these carnivores were not distributed homogenously in the mammoth steppe biome (Fig. 1). Some of them, such as cave lion, wolf and brown bear have been found over the whole territory of the mammoth steppe, from Spain to Alaska and Yukon (also called eastern Beringia), while others had a more restricted distribution, such as cave bear and cave hyena found essentially in Europe, with possible expansion into Siberia in the case of cave bear (Knapp et al., 2009; Boeskorov et al., 2012), while cave hyena was also present in southern and southeast Siberia (Baryshnikov, 1999), but both species were absent from eastern Beringia. This last region included, in contrast to Eurasia, the scimitar-tooth cat Homotherium serum as well as the giant short-faced bear Arctodus simus. Moreover the fossil record of some of these carnivore species stops significantly before the end of the Pleistocene (e.g., Guthrie, 2006; Stuart and Lister, 2007). For instance, cave hyenas became extirpated from northern Eurasia before the Last Glacial Maximum (Stuart and Lister, 2014), and cave bears were fully extinct around 25,000 years ago (Pacher and Stuart, 2009; Bocherens et al., 2014d). In Alaska, the youngest radiocarbon dates are not younger than 36,000 14C years BP for the scimitar-tooth cat Homotherium, and 20,000 14C years BP for the short-faced bear (Fox-Dobbs et al.,

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2008), even if this last bear species survived until the end of the Pleistocene in more southern regions of North America (e.g. Gillette and Madsen, 1992; Schubert, 2010; Fox-Dobbs et al., 2014). Therefore the carnivore assemblage was neither homogeneous through space nor through time within the mammoth steppe ecosystem. To complicate this situation even more, it is important to keep in mind that different types of prehistoric humans were also present in some areas at some times of the considered region, potentially competing and even actively hunting carnivores (e.g., Ripple and van Valkenburgh, 2010; Turner et al., 2013; Stuart and Lister, 2014). Neandertals were present in Europe and western Asia until around 40,000 years ago, then replaced by anatomically modern humans until around 35,000 years ago (e.g. Higham et al., 2014). Except in the most southern areas, the rest of Siberia was probably devoid of human populations until around 30,000 years ago, with a progressive expansion to the north and the east, finally reaching Alaska and Yukon shortly before or after the Last Glacial Maximum (e.g. Pitulko et al., 2004; Goebel et al., 2008). The aim of this paper is to reconstruct the actual paleodietary preferences of these carnivores, to place them into their trophic systems and investigate how they interacted with each other, as well as with other components of the ecosystem. Ultimately, this information will help to see how late Pleistocene carnivores of the mammoth steppe reacted to external and internal perturbation factors. For those species that survived until the present day, it will allow us to have a better idea of their fundamental niche, by accumulating more cases of their realized niche under various sets of circumstances. For this purpose, the present paper brings together a large body of published isotopic data with additional new values to examine carnivore palaeoecology across a large region and time period. 2. Paleodiet reconstruction with stable isotopes: “you are what you eat” Since the 1990s, stable isotopes in terrestrial teeth and bones have been providing palaeobiological information on dietary preferences of mammalian faunas from the Quaternary period (e.g. Bocherens et al., 1990, 1994a, 1994b, 1995a, 1996; Fizet et al., 1995; Matheus, 1995; reviews in Koch, 2007; Bocherens and Drucker, 2013). Indeed, the skeletal tissues of an animal incorporate chemical elements through its diet, which isotopic ratios may vary according to the consumed diet. This information is potentially preserved in molecules and minerals found in fossil teeth and bones and therefore can yield palaeoecological information. 2.1. Carbon and nitrogen stable isotopes Carbon and nitrogen are quantitatively the most important chemical elements provided by the diet of an animal, and not surprisingly the most commonly used pairs of isotopes for palaeodietary reconstructions are 13C/12C (for carbon) and 15N/14N (for nitrogen). The variations of isotopic abundances are measured using an isotopic ratio mass spectrometer and the results are expressed as relative abundances, known as “delta” (d) values, which are defined as follows: dEX ¼ [(ERsample  ERstandard)/ERsample]  1000 (‰), where EX stands for 13C or 15N, respectively. International reference standards have been established for d13C values (marine carbonate V-PDB) and for d15N values (atmospheric dinitrogen AIR). In theory, the d13C and d15N values measured for a given sample should be the same in any laboratory worldwide. A recent intercalibration campaign performed on the collagen of a well-preserved archaeological bone involved 21 laboratories in the USA and Germany evidenced some

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Fig. 1. Map of the study area, with distribution of the investigated carnivore species during MIS 2 and MIS 3 (60,000 to 14,000 years BP) (map background modified from www. geocities.jp). Note that the extension of glaciers has fluctuated during this period, that the actual distribution of the species may be larger than the study area, and that some species may not be present during the whole period in the represented areas (Data from Guthrie, 1990; Baryshnikov, 1999; Kahlke, 1999, 2013; Knapp et al., 2009). Although the scimitar cat
n et al., 2014) and if present, this Homotherium has been claimed to be present in the North Sea up to 28,000 years ago (Reumer et al., 2003), this evidence is still debated (Anto predator was very rare, therefore it is not shown as part of the late Pleistocene European carnivore assemblage.

small differences in the isotopic results but on average interpretatively insignificant (Pestle et al., 2014). Therefore it is reasonable to use isotopic dataset including data from different laboratories, as long as the reliability criteria of fossil collagen are met. 2.2. Reliability of fossil bone and tooth collagen for C and N stable isotope analysis When dealing with fossil material, it is necessary to measure the isotopic composition of an individual using purely material formed during the lifetime of this specimen and avoiding absolutely all altered or contaminated molecules. In the case of late Pleistocene mammals, the fraction of choice is collagen of skeletal tissues, bone and tooth dentine. Indeed, collagen is a very stable protein especially when embedded in the phosphatic mineral matrix of bone and dentine, and it can be easily characterized by its chemical composition that is very distinctive by comparison with possible contaminants, especially its carbon and nitrogen content as well as the atomic carbon on nitrogen ratio (%C, %N and C/N, respectively). Numerous studies have shown that only collagen with carbon and nitrogen content similar to those of collagen from fresh bone extracted using the same protocol had retained isotopic composition that does not differ significantly from its original values and therefore can be used for paleodietary reconstructions (e.g. DeNiro, 1985; Ambrose, 1990). According to these authors, the usual criteria for reliable collagen are atomic C/N ranging from 2.9 to 3.6 and N > 5%. In the rest of this paper, only isotopic data obtained on reliable collagen will be considered for palaeobiological reconstructions. Collagen survival rate in fossil bones and teeth decreases roughly with time elapsed since death and burial of the skeletal remains. The rate of decay is also dependant of physical factors such as temperature, humidity, and stability of the abiotic conditions in

the burial environment (e.g. Bocherens et al., 1997b; Holmes et al., 2005; Van Doorn et al., 2012). As general rules of thumb, it seems that bones from cave sites have better chances than bones from open air sites to preserve their collagen for long periods, while cold temperatures are favourable to collagen preservation. In cave sites located in areas with temperate climatic conditions, collagen is usually preserved until around 100,000 years ago (Bocherens et al., 1999), but some exceptional cases several times older have been documented (e.g. Jones et al., 2001; Drucker et al., 2014; Kuitems et al., in press). Besides, there is an increasing body of evidence that suggests that waterlogged burial deposits may also be favourable to long term collagen preservation (e.g. Bocherens et al., 1997b; Drucker et al., 2014; Kuitems et al., in press). 2.3. Trophic isotopic enrichments Numerous experimental studies have been performed to quantify the isotopic fractionation between a consumer and its food, in particular for mammalian carnivores (e.g. Hilderbrand et al., 1996; Roth and Hobson, 2000; Kurle, 2002; Zhao et al., 2006; Newsome et al., 2010; Kelly et al., 2012; Hobson and Quirk, 2014). Most of these studies analysed soft tissues, such as blood, hair or muscle, only a few studies include collagen (e.g. Hilderbrand et al., 1996; Hobson and Quirk, 2014). Some studies have documented some variation in the fractionation between food and an animal's tissues, depending on factors such as ontogenic age and protein content of the consumed food (e.g. Sponheimer et al., 2003; Robbins et al., 2010; Hobson and quirk, 2014). In the case of fossil material, there is no direct access to the food consumed by a given animal, and except in the very rare case of mummification, in which animal hair is available for isotopic studies (e.g. Bombin and Muehlenbachs, 1985; Iacumin et al., 2005; Kirillova et al., 2014), only bone collagen is available for isotopic analysis (e.g. Bocherens

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et al., 1994a, 1994b, 1996). Therefore using directly the estimates for isotopic fractionation between soft tissues and diet measured in modern specimens is not possible. Since only the bone collagen of the potential prey is available in the fossil sites, the most reasonable approach is to use reference fractionation data between the carbon and nitrogen isotopic values of bone collagen of predators and those of their prey (e.g. Bocherens and Drucker, 2003; Fox-Dobbs et al., 2007). A review of the published values of differences between d13C and d15N values of bone collagen of predators and those of their prey yields the following values (Fig. S1 and Table S1 in supplementary data). When only data from modern specimens are considered, the following relationships between the d13C values of predator collagen and that of their prey are obtained: d13Ccoll 13 15 15 predator ¼ d Ccoll prey þ 1.2 (±0.1) ‰ and d Ncoll predator ¼ d Ncoll þ 3.6 (±0.9) ‰ . When data from archaeological sites are taken prey into account, in which the prey is assumed from the archaeological context rather than actual prey, the differences in d13C and d15N values between bone collagen of predators and their estimated prey are only slightly different: 1.0 ± 0.3‰ and 4.2 ± 1.4‰, respectively. Finally, combining modern and archaeological data yields the following estimates for d13C and d15N differences between the predator collagen and that of its average prey: 1.1 ± 0.2‰ and 3.8 ± 1.1‰, respectively. Such estimates are still based on limited studies and should be improved in the future, but these results are sufficiently consistent to serve as a basis for paleodietary reconstructions. Previous studies used either single values for isotopic differences between carnivores and their prey (e.g. Fox-Dobbs et al., 2008), ranges of such estimates (e.g. Bocherens et al., 2005, 2013; Drucker and Henry-Gambier, 2005) or their average and standard-deviation values (e.g. Yeakel et al., 2013; Bocherens et al., 2015a). Using different estimates along this range may change the calculation of the proportion of prey by predators, it is therefore recommended to use ranges or average and standard-deviation of these estimates, rather than single values. 2.4. The “isotopic landscape” of the mammoth steppe for large carnivores 2.4.1. Distinguishing potential food resources with C and N stable isotopes in the mammoth steppe The use of carbon and nitrogen stable isotopic composition of late Pleistocene carnivores for dietary inferences is only meaningful if different food resources available to these carnivores can be distinguished through their d13C and d15N values. In the mammoth steppe context, it is possible to distinguish plant from meat, as well as to quantify the contribution of meat from different kinds of prey, and to identify the possible consumption of fish and other aquatic resources. 2.4.1.1. Plants versus meat. Nitrogen isotopic values are the isotopic tracer of choice for distinguishing plant from animal food. Indeed, at the basis of the trophic systems, plants provide food resources with generally the lowest d15N values that can be found in a given ecosystem. However, due to the preferential use of different nitrogen sources (e.g. N2, ammonium, nitrates) linked to various nitrogen acquisition strategies involving sometimes symbiotic associations with bacteria or fungi, a large range of d15N values can be found among plants, also in arctic and boreal contexts (e.g. Barnett, 1994; McLeman, 2006; Craine et al., 2009; Hobbie et al., 2009). The range of d15N values among plants can be as large as 12‰, therefore equivalent to around 3 times the isotopic fractionation of nitrogen between food and animal (Bocherens, 2009). Because of the general isotopic enrichment in nitrogen between a given food and its consumer, herbivores exhibit higher d15N values than the plants they eat (e.g. Darr and Hewitt, 2008; Halley et al.,

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2010). However, when the d15N values of some herbivores are compared to the d15N values of plants, there are cases where plants with high d15N values, such as graminoids and forbs, exhibit d15N values as high as those of herbivores feeding on plants with lower d15N values, such as shrubs, as it is illustrated for reindeer in McLeman (2006, figure 3.3). Even if bone collagen high d15N values do not mean necessarily carnivory, since some plants such as graminoids and forbs can be as high in 15N than the meat of herbivores feeding on shrubs and trees, the opposite situation, i.e. bone collagen with low d15N values, clearly indicates that very little if any animal food was consumed. 2.4.1.2. Different types of meat. In terrestrial ecosystems, it is expected that different herbivores exhibit different d13C and d15N values if they consume different types of plant food and if these plant foods present different carbon and nitrogen isotopic compositions. One very clear example of this phenomenon is the large difference in d13C values between grazers and browsers in areas where grass consumed by grazers use the C4 photosynthetic pathway (d13C ¼ 12‰), while woody plants that produce the leaves consumed by browsers use the C3 photosynthetic pathway (d13C ¼ 25‰). In such contexts, occurring in inter-tropical regions, it is easy to determine if a given predator consumes preferentially browsing or grazing prey, of a mixture of both (e.g. Ambrose and DeNiro, 1986; Koch et al., 1991; Codron et al., 2007; Yeakel et al., 2009). However, C4 plants need a warm growing season to provide a significant biomass and they are therefore virtually absent from cold regions today (e.g. Collatz et al., 1998). This was also the case in the mammoth steppe ecosystem, where all plants, grass as well as forbs and woody plants producing leaves, used the C3 photosynthetic pathway (Bocherens, 2003). Even in such a context, small but consistent variations in d13C values of C3 plants occurred under the influence of environmental or physiological factors. A review of such variations was presented by Bocherens (2003) and an updated version of the summary figure is given in supplementary information (Fig. S2). The most remarkable plant type that can be distinguished using d13C values is lichen, which presents systematically d13C values around 3‰ more positive than those of coeval vascular plants (e.g. Fizet et al., 1995; McLeman, 2006). Among vascular plants, the main differences in d13C values occur in relationship with the vegetation density. Even excluding the very negative d13C values of dense forest that were not present in the mammoth steppe, a range of around 2‰ can be expected among other plants depending on the density of the vegetation coverage (Fig. S2). Numerous isotopic investigations of plants from boreal and arctic contexts have documented predictable variations in d15N, according to the use of different pools of nitrogen through different mechanisms, some of them involving symbiotic organisms such as bacteria and fungi (e.g. Schulze et al., 1994; Michelsen et al., 1996; Hobbie et al., 2009). For instance, plants that obtain their nitrogen through a symbiosis with fungi associated to their roots (mycorrhizae) exhibit consistently and significantly lower d15N values than those incorporating nitrogen from the soil without such symbiosis (Fig. S3). These different nitrogen intake strategies are not randomly distributed among the plants available to herbivores, but in contrast correspond to functional groups relevant for dietary preferences, i.e. plants with low d15N values are essentially trees, deciduous and evergreen shrubs, while plants with high d15N values are graminoids (grass and sedges) and forbs. As a consequence, it is expected that browsers, feeding on leaves, will exhibit lower d15N values than grazers, feeding on graminoids (e.g. Bocherens et al., 2015b) (Fig. S3). In summary, due to these consistent differences in their d13C and d15N values, it is possible to recognize plant categories

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corresponding to the dietary preferences of large herbivores, such as grass and forbs, shrubs and trees, and lichens, and finally their respective consumers. Previous investigations based on tooth morphology, modern analogues and plants remains preserved in the mouth and stomach content of specimens from permafrost, as well as palaeogenetic investigations, have demonstrated dietary partitioning between grazers (mammoth, woolly rhinoceros and bison), mixed feeders (horse and muskoxen) and lichen feeders (caribou-reindeer) (e.g. Ukraintseva, 1993; Guthrie, 2001; Willerslev et al., 2014). However, investigations of dental wear patterns in different areas of the mammoth steppe have also documented some variation in this pattern for some ungulate species (Rivals et al., 2010). In this context, the pattern of distribution of d13C and d15N values among herbivorous large mammals appear remarkably consistent across the range of the mammoth steppe ecosystem, with a similar position of mammoth with high d15N values and rather low d13C values in Southwestern France, Belgium, Eastern Siberia and Alaska, while reindeer exhibits consistently d13C values higher than those of coeval species (Fig. 2). Horse present slightly lower d13C values than large bovines (Bos or Bison), and woolly rhinoceros is usually high in d15N values. Such a pattern can be interpreted as reflecting the consumption of lichen with less negative d13C values than other plants by reindeer, while mammoth was the most grazing species of this community and therefore exhibits the highest d15N values. Other herbivore species appear less stable in the isotopic values, probably reflecting more opportunistic dietary habits, such as muskox (Raghavan et al., 2014). Among the large bovines, potentially representing members of

bison and aurochs often difficult to distinguish osteologically, the scattering of the data may reflect to this taxonomic mixture, or more flexible dietary habits. Even among the more stable species, some local and chronologically restricted exception have been observed, such as unusually low d15N values on Lateglacial mammoths from Ukraine overlapping with local horse, which may correspond to an environmental change where mammoths could not find their preferred forage any more (Drucker et al., 2014b), or unusually high d15N values for some horse in southwestern Germany, overlapping with mammoth, and possibly reflecting a decline of mammoth populations and an ecological shift of horse to fill the gap (Drucker et al., 2015). In summary, the d13C and d15N values of bone collagen from large herbivores of the mammoth steppe exhibit a large range of variation, which is largely species dependent and consistent through space and time (Fig. 2). However, some environmental disturbances may lead to deviations for this basic pattern, such as shift of the baseline value of d15N values in a given ecosystem (e.g. Drucker et al., 2003; Richards and Hedges, 2003; Stevens and Hedges, 2004; Bocherens et al., 2014). It is therefore always preferable to obtain d13C and d15N values from the herbivores that formed the actual pool of prey for the investigated carnivores, whenever possible. 2.4.1.3. Fish and aquatic resources. Although feeding on fish or other aquatic resources is less common than feeding on terrestrial resources, such food resources are known to be consumed by modern carnivores, especially bears. For instance, modern populations of brown bears Ursus arctos and black bears Ursus

Fig. 2. d13C and d15N values in major herbivores from the mammoth steppe during the late Pleistocene in Alaska (data from Fox-Dobbs et al., 2008), Yakutia (data from Bocherens et al., 1996; Iacumin et al., 2010; Szpak et al., 2010), Southwestern France (data from Bocherens et al., 2005) and Belgium (data from Bocherens et al., 2011a).

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americanus living along rivers flowing into the Northern Pacific Ocean in Western North America and Eastern Siberia are notorious for their dietary use of spawning salmons (e.g. Kistchinski, 1972; Jacoby et al., 1999; Mowat and Heard, 2006). Other large carnivores can consume fish when available. Wolf populations from southeast Alaska are also exploiting spawning salmon when available (Kohira and Rexstad, 1997; Szepanski et al., 1999). Brown bears and wolves have been observed to scavenge whale carcass stranded on a beach in Alaska (Lewis and Lafferty, 2014). There is no observation of wild modern lion eating fish but other large felids such as panthers and jaguars are known to consume fish (Erlandson and Moss, 2001). Spotted hyenas have been observed to consume some fish in Africa (e.g. Kruuk, 1972; Di Silvestre et al., 2000). Therefore it is fully conceivable that fish and other aquatic resources, either marine (in coastal areas and around rivers where anadromous salmon could spawn) or freshwater, were part of the possible dietary resources for late Pleistocene carnivores. Carbon and nitrogen isotopic composition of freshwater and marine animal differ from those of terrestrial ones, and the isotopic differences between these dietary resources are reflected in the tissues of their consumers. Both exhibit typically higher d15N values due to longer food webs in aquatic ecosystems, while marine food resources present usually higher d13C values than terrestrial C3ecosystems. The case of freshwater ecosystem is more complicated, as the d13C values of freshwater fish are very variable, sometimes lower and other times higher than those of nearly terrestrial ecosystems (e.g., Dufour et al., 1999). The question of possible fish consumption has been addressed in a couple of cases involving late Pleistocene carnivores. A wolf from southwestern France with higher d13C and d15N values than expected for a terrestrial predator by comparison with coeval mammal fauna was interpreted as having consumed 15e45% anadromous salmon (Drucker and Henry-Gambier, 2005). In contrast, cave bears and cave lion that were found in a stratigraphic layer together with bones of large salmons from Kudaro 3 cave in the Caucasus Mountains did not consume these fish according to their d13C and d15N values, leaving ancient humans as the most likely accumulator of salmon bones (Bocherens et al., 2014c). For such studies, the addition of the stable isotopic composition of sulphur is quite helpful, since this element exhibits specific isotopic values in marine ecosystems, quite different from those of terrestrial and freshwater ecosystems (Petersen and Fry, 1987; Bocherens et al., 2014c). Sulphur isotopes could also help to evaluate the consumption of freshwater resources in some continental contexts, but the variability of sulphur isotopic composition in terrestrial resources in time and space makes this approach more complicated (Drucker, 2014). 2.5. Reconstructing ancient trophic systems To evaluate which prey were most consumed by a predator, the most simple approach is to plot the d13C and d15N values of this predator and those of the associated possible prey. Then it is possible to reconstruct the d13C and d15N values of the prey collagen using the differences between those values presented above. To cope with the uncertainties, it is recommended to use a range of values, or averages including standard-deviation, rather than absolute values. Once a range of d13C and d15N values of the possible prey is established, it should be compared to the actual isotopic values of coeval potential prey. An example of this approach is given in Fig. 3, where d13C and d15N values of a late Pleistocene cave hyena and coeval large herbivores such as horse, bovine (aurochs or bison), giant deer and reindeer, from a stratigraphic layer in a site from western France are presented (data from Richards et al., 2008b). The distribution of the isotopic values of the large

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herbivores shows clearly different values for reindeer on one hand, with higher d13C and d15N values, while the three other species cluster in one group, with horse slightly more negative in d13C values than the giant deer and bovine. The reconstructed isotopic values of the hyena prey collagen clearly overlap some of the samples of the latter group (bovine þ giant deer), so members of these two groups could well explain the isotopic values of the hyena by themselves. However it is also necessary to consider the possibility of mixture of prey that would ultimately produce a similar range of isotopic values. In the present case, adding horses would require to balance this with prey presenting high d13C and low d15N values, and they are not present here, while adding reindeer would require to add prey with low d13C values and very low d15N values, which correspond to none of the analysed prey species. Therefore, the conclusion of the original authors that reindeer was the most important prey of hyena (Richards et al., 2008b) appears to be totally unfounded, due to the failure to consider the known fractionation factors between the carbon and nitrogen isotopic abundances of a predator collagen and the collagen of its average prey. When these fractionation factors are taken into account, it appears that in fact large deer and bovine were the main prey of hyena in this context (Fig. 3). Other species could have been consumed, but in very small proportions since they did not impact on the isotopic values of this hyena. This basic approach linking a peculiar isotopic composition of a given predator with that of one given prey, taking into account the expected trophic enrichment, was used in other cases, as for instance in the late Pleistocene site of Marillac, where a high reliance of wolf on reindeer was suggested due to relatively high d13C values in both species (Fizet et al., 1995). A similar basic approach was also used to rule out significant consumption of mammoth meat by late Pleistocene predators in Siberia (Bocherens et al., 1996). This approach is useful when the reconstructed prey collagen isotopic values for a given predator correspond to an extreme value among those of the available prey. In such a case, the prey with extreme isotopic values has to be consumed in significant proportions since there is no possibility to mix other prey with different isotopic composition and obtain through this mixing average prey isotopic values in the range of the reconstructed prey bone collagen. In the context of the mammoth steppe, mammoth and reindeer consumption can be tested using this approach since these two types of prey have isotopic values at the extreme ranges of available prey. Such a basic approach is also still useful to evaluate niche partitioning and competition among predators. For such aspects, isotopic studies can rely on the comparison of the d13C and d15N values in different predator species. If the isotopic values overlap significantly, this could indicate dietary competition due to the use of the same resources, given the similar isotopic compositions among such carnivores. In contrast, if the values were significantly different among carnivores, this would indicate niche partitioning and avoidance of competition. For instance, such an approach was used to evaluate dietary competition and niche partitioning among modern carnivores by Warsen et al. (2014) among native carnivores bobcat (Lynx rufus), coyote (Canis latrans), grey fox (Urocyon cinereoargenteus), and red fox (Vulpes vulpes) in the Adirondack Park, NY, USA. Direct comparison of the isotopic values of individuals of one given predator species can also be informative about intra-specific dietary differences, for instance between escaped captive and wild wolf individuals in northeastern USA (Kays and Feranec, 2011), and has been used to check differences in the proportion of ungulate prey species consumed by different wolf packs in northern British Columbia, Canada (Milakovic and Parker, 2011). A similar approach was used to document niche partitioning among late Pleistocene carnivores, for instance between cave lions and cave hyenas in

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Fig. 3. a. Scatter-plot of d13C and d15N values of a cave hyena from layer 8 in the late Pleistocene site of Jonzac (Charente-Maritime, France: Richards et al., 2008b). The isotopic values of analysed herbivores from the same layer are also presented, as well as the range of reconstructed average prey d13C and d15N values. The three clusters defined in b are also presented. b. Results of a cluster analysis of the large mammals from Jonzac, layer 8 (data from Richards et al., 2008b), showing that the hyena Crocuta crocuta spelaea belongs to the same cluster as reindeer, but its prey plot together with large bovines and giant deer, as well as some horse, and are far away from reindeer.

southwestern Germany and Belgium (Bocherens et al., 2011a) and among large canids recognized as pleistocene wolf and Palaeolithic dogs in Moravia (Bocherens et al., 2015a). In a second step, the observed isotopic differences can be tentatively related to prey choice based on the isotopic values of the possible prey. To convert the isotopic values of predators into proportion of prey and therefore be able to reconstruct the fluxes of biomass from prey to predators, different approaches have been used. Today quantitative approaches based on mathematical models are available. These models were first developed for ecological studies and have been adapted for the special cases of palaeoecological studies (see reviews in Phillips, 2012; Hopkins III and Ferguson, 2013; Parnell et al., 2013). A first generation of models corresponds to basic mixing models that were progressively improved to incorporate uncertainties and differences in C and N concentrations (e.g. Phillips, 2001; Phillips and Cregg, 2001, 2003; Phillips and Koch, 2002; Phillips et al., 2005). Such models were used after some modifications for paleodietary reconstructions including Pleistocene predators (e.g. Drucker and Bocherens, 2004; Bocherens et al., 2005, 2013; Drucker and Henry-Gambier, 2005; Fox-Dobbs et al., 2008). More recently, Bayesian mixing models have become available and they have the advantage to estimate the probability distribution of mixing proportions and to account for uncertainties from various sources (Phillips, 2012). Examples of the results obtained using such models on late Pleistocene carnivores and their associated potential prey in Belgium are shown in Fig. 4. All methods yield similar results, indicating a high proportion of reindeer in the diet of cave lion while cave hyena may have consumed a mixture of all available prey in more or less equivalent proportions. The contributions calculated using the SIAR approach have however a higher resolution since the probability of the different proportions is also given, not just the possible range. Using such models, it is also possible to see if the consumption of some prey is correlated, positively (the increasing consumption of prey 1 has to be compensated by the increasing consumption of prey 2, this is the case when prey 1 and 2 have different isotopic values, located on either side of the values of the possible prey on the scatter-plot, for instance cave bear and reindeer, Fig. S4) or negatively (the increasing consumption of prey 1 has to be compensated by the decreasing consumption of prey 2, this is the case when both prey have similar isotopic values, for instance mammoth and woolly rhinoceros, mammoth and horse, horse and cave bear, and giant deer and reindeer, Fig. S4). It is also possible to

incorporate some non-isotopic data into the Bayesian model, for instance prey availability data (Yeakel et al., 2011). These Bayesian mixing models are widely used in ecology (e.g. Yeakel et al., 2009; Cherry et al., 2011; Killengreen et al., 2011; Milakovic and Parker, 2011; Savory et al., 2014), but their use in paleodietary reconstruction is still in its infancy (see for instance application of MixSIR (e.g. Yeakel et al., 2013) and SIAR (e.g. Bocherens et al., 2015a) to late Pleistocene carnivores). In all cases, a meaningful application of these mixing models requires a good knowledge of the spectrum of potential prey and their isotopic composition, since such models will always be able to produce results, even if they are not reflecting a realistic situation. Another limitation of SIAR Bayesian mixing models is the fact that prey with only one specimen cannot be incorporated in the calculation. To avoid this limitation, one can incorporate this single sample together with another prey with close isotopic values, and to treat this newly defined “prey” as taxonomically mixed, or to regroup prey on the basis of the isotopic values themselves, using a cluster analysis, instead of using average and standard-deviation of prey species (Bocherens et al., 2015a). These clusters based on individual isotopic values of prey may include only members of one prey species, sometimes all of the members of a prey species, or include a mixture of specimens from different prey species, while other specimens of the same species belong to other clusters. Since the isotopic values on which the clusters are based reflect some environmental parameters of the plants consumed by the herbivores, the consumption of prey from a given cluster indicate which habitat was preferentially exploited by a given predator, even if it is not possible to tell exactly which prey was preferentially consumed. The choice of the strategy for grouping prey and the type of mixing model to use will depend on the geographical scale (local, regional, global) and on the availability of isotopic data on potential prey (“isotopic landscape”). More details will be given on the specific situation of the mammoth steppe below. 2.6. Complicating factors 2.6.1. Environmental shifts of d13C and d15N values of terrestrial trophic webs Since isotopic fractionation between plants and their substrate for carbon and nitrogen changes according to environmental conditions, the d13C and d15N values of the same type of plant may vary across environmental gradients, and therefore an animal feeding

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Fig. 4. Left: Scatter-plot of d13C and d15N values of cave hyena, cave lion and the coeval large herbivores in late Pleistocene of Belgium (40 to 30 thousand years ago) (modified from Bocherens et al., 2013). Small symbols for mammoth and woolly rhinoceros stand for deciduous teeth, with higher d15N values due to suckling. The reconstructed prey isotopic values for cave lion point for obligatory consumption of reindeer, while cave hyena may consume a mixture of any prey available. Upper right: possible contribution of different prey species estimated using IsoSource (Bocherens et al., 2013). It appears clearly that cave lion needs to consume at least 25% reindeer, while cave hyena may consume a mixture of all prey, with possibly higher amounts of large bovine and woolly rhinoceros (note that some species such as giant deer and cave bear were not included in the calculation). Lower right: possible contribution of different prey species using SIAR (this work, this time including giant deer and cave bear as possible prey). The same pattern is obtained, with obligatory consumption of reindeer for cave lion, very little cave bear and mammoth are possible, while cave hyena may consume a mixture of any prey in more or less equivalent proportions.

on the same type of food may exhibit different d13C and d15N values accordingly. The main macro-ecological factors recognized to influence the d13C and d15N values of plants are temperature, aridity €rner et al., 1991; Amundson et al., 2003; Sah and altitude (e.g. Ko and Brumme, 2003; M€ annel et al., 2007; Craine et al., 2009; Zech et al., 2011). In general, d13C values of a given plant tend to increase with aridity and with altitude, while d15N values tend to increase with aridity and temperature, and decrease with altitude. The period between 50,000 and 12,000 years ago has witnessed numerous significant climatic fluctuations in northern Eurasia and northwestern North America (e.g. Anderson and Lozhkin, 2001; Barron and Pollard, 2002; Hubberten et al., 2004). Since climatic conditions, especially aridity and temperatures, have an impact on the d15N values of plants (Fig. S3; Amundson et al., 2003), it is not surprising that some changes in the d15N values of late Pleistocene herbivores have been observed. For instance, investigations of d15N values of late Pleistocene herbivores in Europe and eastern Beringia have documented fluctuations of d15N values caused by large global climatic changes, such as the Last Glacial Maximum followed by the first warming of the Lateglacial, between around 25,000 and 12,000 years ago. In Western Europe, this period corresponds to a decrease of d15N values in ungulates (e.g., Drucker et al., 2003; Stevens and

Hedges, 2004; Stevens et al., 2008), while an increase of d15N values in ungulates was observed in southern Italy and in eastern Beringia at the same time (Iacumin et al., 1997; Fox-Dobbs et al., 2008). This discrepancy of variations of d15N values at the basis of the trophic webs is due to the conflicting effects of decreasing temperature (leading to decreasing d15N values) and increasing aridity (leading to increasing d15N values). The effect of aridity seems to have been dominant in Italy and in eastern Beringia while, in contrast, the effect of decreasing temperature was stronger in western Europe. In addition to these fluctuations of d15N values that can be connected to large scale climatic changes during the late Pleistocene, more local and short-term variations have also been reported (Fizet et al., 1995; Richards et al., 2008b; Bocherens et al., 2014b). For instance, a clear short-term increase of d15N values in all large mammal species between 35 and 40 thousand years ago, with herbivorous and carnivorous species shifting their d15N values by around 3‰ by comparison with the older and younger stratigraphic layers of archaeological sites in southwestern France, while the d13C values were not changed (Bocherens et al., 2014b). This shows that the structure of the trophic webs were not modified, but an environmental factor, probably increasing aridity, led to a general

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increase of d15N values at the basis of the food webs that was reflected at each trophic level. If this general shift in d15N values had not been recognized and isotopic values of carnivores from this period had been compared to those of prey from younger or older time periods in this region, a dietary change such as fish consumption might have been concluded, while it did not happen. Therefore it is always necessary to check the isotopic values of possible prey as close as possible from the studied carnivores, to avoid such misinterpretations. The isotopic baseline of late Pleistocene ecosystems has not only shifted in time, but also in space. For instance, isotopic investigations of mammoths in eastern and western Beringia showed some significant differences in their d13C and d15N values, probably linked to different levels of aridity between Siberia and Alaska and Yukon (Szpak et al., 2010). A geographical gradient of d15N values in cervids was also recognized during the Lateglacial in Western Europe, with increasing d15N values when the distance from the ice caps of the Last Glacial Maximum increased (Drucker et al., 2011, 2012a). When such spatial gradients are recognized, the comparisons of d13C and d15N values of carnivores and their possible prey must take these isotopic variations into account. 2.6.2. Impact of varying nitrogen content in different food resources to evaluate animal food consumption by omnivores One potential dietary application of isotopic tracking is the use of d15N values to identify hypocarnivores from hypercarnivores among the late Pleistocene carnivores. The clear increase of d15N values at each trophic level should allow this type of application. However, the relationship between the proportion of meat versus plant food in the average diet and the d15N values of the consumer collagen is not linear, because nitrogen comes from the protein fraction of the diet and the protein content of meat is much higher than for plant (Phillips and Koch, 2002). Therefore, the consumption of only 50% meat will lead to a d15N value as high as that measured for a hypercarnivore (Fig. 5). This means that in the case of bears, individuals with d15N values in the range of coeval hypercarnivores have consumed a minimum of around 50% meat but may potentially have also consumed up to 50% plant food, therefore belong to mesocarnivores. In contrast, bears with d15N values as low as those of coeval herbivores cannot have consumed more than a few percent if any animal proteins and are therefore hypocarnivores, otherwise they would have immediately and very quickly increased their d15N values. This will have implications in the dietary reconstruction of omnivorous bears, for extinct species as well as extant ones, in the late Pleistocene. 2.6.3. Physiological effects During the life of a mammal, the nitrogen balance may be modified, which could lead to changes in the isotopic fractionation of nitrogen or in the source of nitrogen pools in the organism, and therefore to changes in the d15N values of an individual unrelated to a dietary change and that may interfere with paleodietary reconstructions. Some of these physiological effects, such as suckling and weaning, occur in all mammals while others, such as gestation, hibernation, starvation and water stress are limited to some species or to some individuals within a species. 2.6.3.1. Gestation, suckling and weaning. Pregnant mammal females need to deliver nitrogen to the growing foetus and therefore change their nitrogen balance compared to non-pregnant females and males of the same species. This situation leads to slightly lower d15N values in pregnant women (Fuller et al., 2004) but no similar studies were performed on animals. It is not clear if such an effect would be detectable in bone collagen, which averages several years of life of an individual, but it could show in incrementally growing

Fig. 5. Changes in d13C and d15N values of an omnivorous mammal with increasing proportion of meat versus plant food in its diet. The end-members for 100% plant food and 100% meat are the average d13C and d15N of cave bear and cave hyena in Scladina cave, layer 1A (Bocherens et al., 1997a), respectively. (a) is the expected variation if carbon and nitrogen content were the same in meat and plant food; (b) is the expected variation considering average carbon and nitrogen content in meat (C ¼ 51.5%; N ¼ 14%) and in plant food (C ¼ 44%; N ¼ 1%) (Phillips and Koch, 2002). This figure is modified from Bocherens (2009).

structures such as tusk dentine. In all mammals from birth to weaning, the diet is composed of milk from their mother instead of an adult diet, meaning that suckling mammals behave like predators of their own kind and exhibit an isotopic enrichment, especially in 15N compared to the adults of their population (e.g. Hobson and Sease, 1998; Jenkins et al., 2001; Dalerum et al., 2007; Fahy et al., 2014). Only a few mammalian species have been investigated for this effect, and some differences seem to exist among species (Jenkins et al., 2001), probably related to the use of storage tissues or normal food to synthesize milk (Dalerum et al., 2007). The intensity of this effect varies among species and is difficult to quantify. However, this is an important phenomenon to consider when dealing with bones of immature specimens, in which part of the collagen may still reflect the suckling 15N-enriched composition, as well as with deciduous teeth or the roots of some permanent teeth that formed at least partially during times of suckling and did not remodel afterwards (e.g. Bocherens et al., 1994; Fizet et al., 1995; Drucker et al., 2012b). In addition to the effects on the d15N values of the predator skeletal parts that could be enriched when taken from tissues during the early life of the individuals it should be noticed that the consumption of individual prey that retain their 15N-enriched suckling signal would also lead to higher than expected d15N values in the collagen of a given predator, compared to those evaluated using bone collagen d15N values of adult individuals of the same prey species. For instance, mammoths younger than 5 years may exhibit d15N values up to 3‰ higher than those of the coeval adults (e.g. Rountrey et al., 2007; Metcalfe et al., 2010; Bocherens et al., 2013). 2.6.3.2. Hibernation. Hibernation corresponds to a seasonal decrease of metabolic activity and food intake that coincides to the cold season in middle and high latitudes. This strategy to cope with

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seasonal food shortage is widely spread among extant ursids in temperate, boreal and arctic regions, and studies of fossil bear remains strongly suggest that it was also the case for extinct ursid
n, 1976; Stiner, 1998). During species such as cave bear (e.g. Kurte hibernation, bears do not feed so they have to rely on the nitrogen stored in their body tissues, and they do not urinate or defecate, so only recycling of nitrogen takes place for males and non-pregnant females, as well as some loss of nitrogen through pregnancy and lactating for pregnant females. At the same time, fat reserves provide carbon and a source of energy during hibernation. This dramatic physiological change has consequences on the stable isotopic composition of carbon and nitrogen of bear tissues, as documented on brown bears (Jenkins et al., 2001) and on female polar bears (Polischuk et al., 2001). The d13C values of bear blood decrease during hibernation, while the d15N values increase. The d15N values of skeletal muscle also increase at the beginning of hibernation but stay stable afterwards (Lohuis et al., 2007). Since these studies analysed d13C and d15N values in blood, it is not known to which extent these isotopic shifts will be recorded in bone collagen, since the turnover of bone collagen decreases but does not stop during this period of low metabolic activity (e.g. Donahue et al., 2006). This will be an important point to consider when discussing these effects on fossil bear bone collagen. It will be also important to consider this aspect when discussing the possible predation on cave bear cubs. 2.6.3.3. Starvation and water stress. Two additional cases of changes in the nitrogen balance are starvation and water stress. In the first case, a shortage of proteins in the ingested food can lead to the use of amino acids, and therefore nitrogen, from body tissues to compensation this shortage. Since an animal's tissues are 15Nenriched compared to its food, such a shift in nitrogen source could lead to an increase of d15N values in the tissues synthesized during such an event (Mekota et al., 2006). Such an effect was recorded in some tissues of some species, such as humans and some reptiles (e.g. Mekota et al., 2006; McCue and Pollock, 2008) but not in other species, such as cockroaches and salamanders (e.g. McCue, 2008; Milanovich and Maerz, 2013). Besides these varying effects of starvation, their possible impact on the d15N values of bone collagen necessitate that bone collagen would be synthesized during starvation periods, while in contrast bone synthesis is reduced or even stopped during starvation (e.g. Jha et al., 1968; Takagi, 2001). This means that any effect of starvation will probably not be visible on bone collagen. Water stress has also been suggested as a possible cause of enrichment in 15N of bone collagen independent of trophic level. Indeed the d15N values of bone collagen tend to increase with aridity for herbivores (e.g. Heaton et al., 1986; Sealy et al., 1987; €cke et al., 1997) and water recycling involves a change in the Gro excretion of urea, a molecule with low d15N values (e.g. Ambrose, 1991). More recent works have confirmed this trend but also showed that the increase in d15N values happens at the plant level and it is reflected in herbivores and carnivores through the normal 15 N-enrichment between consumers and their food rather than through an increase of the fractionation between diet and animals (e.g. Murphy and Bowman, 2006; Hartman, 2011). 2.6.4. Chronological resolution of skeletal tissues: implications for sampling bone and tooth Considering the possible isotopic variations that may occur during the lifetime of an individual, either through changes in its physiology or in its diet, it is very important to take into account which period of time is recorded in the fossil tissue being investigated, bone or tooth dentine. Bone collagen forms during the growth of the individual skeleton, but continues to remodel during

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the whole life, at different rates in different anatomical parts (Fig. 6). Collagen is synthesized in mammal bone during growth, but remodelling continues during adult life, and therefore adult bone collagen represents the average diet isotopic composition of several years before death in long-lived large mammals (e.g. Hindelang et al., 2002; Huja and Beck, 2007). Collagen can also be retrieved from the dentine of teeth, especially in roots. In this material, collagen will accumulate principally during tooth growth. Since carnivores have brachyodont teeth, except canines of some species, the growth stops early in life (Fig. 6), and takes place at a time when significant amounts of nutrients still come from suckling. As a consequence, the collagen extracted from dentine may still yield a 15N-enriched collagen by comparison with bone collagen of the same individual (Bocherens et al., 1994). Indeed, all d15N values measured on dentine collagen are higher than those measured on bone collagen of the same individual, in modern and fossil wolves, fossil hyenas, as well as modern and fossil bears (Table S2; Fig. S5). The average differences for wolf and hyena are 1.92 ± 0,19‰ and 1.08 ± 0.55‰, respectively, while the average difference for bears is 1.47 ± 0.92‰ for modern specimens and 1.94 ± 0.57‰ for fossil ones (Table S2). The difference in d13C values between dentine and bone collagen is not always positive but the average values for wolves, hyenas and modern bears are positive, ranging from 0.2 to 0.7‰ (Table S2). One exception is the case of the fossil cave bears, for which the difference is on average negative (0.43 ± 0.53‰) (Table S2). These isotopic differences are probably the result of dietary and/or physiological differences between the time of formation and collagen synthesis in both types of skeletal tissues. In any case, it means that bone should be preferred for collagen isotopic analysis over tooth dentine. In cases where teeth are the only pieces available for study, an adjustment of the d13C and d15N values measured on tooth dentine should be performed before comparing these isotopic values, using either differences established for the same species, or if they are not available taking the average calculated for all carnivore specimens so far, i.e. 0.29 ± 0.53‰ for d13C values and 1.41 ± 0.59‰ for d15N values (Table S2). This strategy was used when compiling isotopic data for late Pleistocene carnivores in the present study. The use of a tissue that integrates information during a long temporal scale, such as bone collagen, will not allow us to distinguish between a specialist population and a generalist population in which each individual feeds on various prey which average value coincides with that of the prey of the specialist population (Bearhop et al., 2004). Only using tissues integrating dietary information over short temporal scale, such as hair, could allow us to distinguish these two cases, but fossil hair of ancient carnivores are excessively rare and have not yet been studied for their isotopic signatures, except for one cave lion from the permafrost of northern Siberia (Kirillova et al., 2014). However, comparing isotopic results from individuals with clear biological differences, such as age or sex, could provide information about sexual ecological differences or change of diet through ontogeny. Fossil scats, also known as coprolites, are known for Pleisto
ndez cene carnivores (e.g. Horwitz and Goldberg, 1989; Ferna Rodríguez et al., 1995; Diedrich, 2010) and could potentially yield an isotopic signal related to the diet of its owner. Such a dietary information would be representative of a short period of the lifetime of the individual, a property that is exploited in modern carnivores to document seasonal changes in the diet (e.g. Keitt et al., 2002; Darimont et al., 2008; Seamster et al., 2014) and that should be considered in the interpretation of such data in fossil carnivores. Although such coprolites have been used as source of ancient DNA (e.g. Bon et al., 2012), their use as potential source of isotopic information on the consumed prey has not yet been attempted.

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Fig. 6. Summary of portion of life-time represented in collagen from different skeletal parts in cave bears (modified from Münzel et al., 2014).

3. Application to large carnivore palaeoecology in the mammoth steppe 3.1. Ursids Extant ursids include species with a wide range of dietary habits, ranging from fully or essentially herbivores, therefore clearly hypocarnivores, such as giant panda and spectacled bear, to purely carnivores, such as polar bear, with the majority of species such as brown bear, American black bear, Asiatic black bear being opportunistic and feeding on a variety of food items ranging as diverse as plants, insects, mammals and fish (e.g. Stirling and Derocher, 1990; Christiansen, 2007). As originally carnivores, all bears species, even the most herbivorous ones, have retained the ability to digest animal food and can eat it if available (Christiansen, 2007). Moreover, different populations or individuals of omnivorous bears can have very different dietary choices. The determination of food selection by extinct bear species or ancient members of extant opportunistic species is therefore an important question for palaeoecosystem reconstructions where the isotopic approach has provided very important results. 3.1.1. Cave bear (Ursus spelaeus s.l.) 3.1.1.1. Herbivores or omnivores?. Cave bear skull and tooth morphology has been suggested to reflect a more vegetarian diet
n, 1976), than modern brown bears (e.g., Ehrenberg, 1927; Kurte although more recent morphometric analyses conclude that the craniodental traits of cave bears reflect a similar level of omnivory than modern omnivorous bears (Figueirido et al., 2009). In such a case of uncertainty, carbon and nitrogen isotopes could certainly help. Since the fossil remains of cave bears are extremely abundant in cave deposits in Europe, to the point that they were exploited ze, 1994; Rabeder et al., industrially to produce fertilizers (e.g., Ge 2000; Neugebauer-Maresch, 2010), it does not come as a surprise that this species was the first extinct Pleistocene mammals to be investigated with stable isotopes (Bocherens et al., 1990, 1994). These first results, obtained on cave bears from southeastern France showed clearly that the d15N values of these bears were similar to those of coeval herbivores, such as horses or deer, and much lower that the d15N values of the coeval predators. A clear illustration of

this pattern is shown on Fig. 7, where d13C and d15N values of cave bears and coeval herbivorous and carnivorous species from southeastern France including Chauvet cave are presented (complete dataset on Table S3). This pattern observed in southeastern France and recognized already 20 years ago was fully confirmed by further studies of cave bears from Slovenia, Spain, Belgium, Luxembourg, Germany, Switzerland, Austria, Czech Republic and the northern Caucasus (e.g. Bocherens et al., 1997a, 2006, 2011a, 2011b, 2014c; Nelson et al., 1998; Vila Taboada et al., 1999; PatouMathis et al., 2005; Delsate et al., 2012; Pacher et al., 2012). At the same time, a second trend appeared, that showed large isotopic variations among bones of different age classes
ndez-Mosquera, 1998; Nelson et al., 1998; Pe
rez-Rama et al., (Ferna 2011) and between bones and teeth of adult individuals (Bocherens et al., 1994, 1997a, 2006). These isotopic variations can be explained by the changes in d13C and d15N experienced by the cave bear individuals during suckling and hibernation, combined with the different times of biosynthesis of bone and dentine in one given individual (Figs. S6 and S7). The pattern of d13C and d15N variations in cave bears mimics the observations made on blood plasma of captive bears, mothers and cubs (Jenkins et al., 2001). It is therefore clear that hibernation has an impact on the d13C and d15N values of some skeletal tissues in cave bear, at least the bones and deciduous teeth of very young cubs, as well as the teeth of adults. It is still questionable if bone collagen of adult individuals is also affected by this phenomenon, and if this d15N increase could be more pronounced if the hibernation is longer, as suggested by Fern
andezMosquera et al. (2001). An additional pattern is the absence of difference in d13C and 15 d N values between males and females, in sites where some adult individuals could be sexed and analysed for stable isotopes (Table S4; Fig. S8). This suggests that males and females had a similar hibernation behaviour, a feature typical of vegetarian extant bears, since among carnivorous bears, only females hibernate to give birth while males remain active during the winter and feed on carcasses (Stiner, 1998). Together with the fact that many cave bear hibernation caves include adults of both sexes, this is an indirect indication of herbivorous dietary habits for cave bears (Stiner, 1998). A new development in the palaeodietary reconstruction of cave bears using bone collagen stable isotopes was the publication of

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ne and Mialet), compared to those of herbivores (horse, Fig. 7. d13C and d15N values of bone collagen in cave bears from Chauvet cave and sites of similar age in the same region (Alde red deer, aurochs, ibex, hare) and carnivores (wolf, leopard) from the same region (data from Bocherens et al., 1994, 2006; Szmidt et al., 2010; Bon et al., 2011).

d15N data much higher than those measured so far for this species on bone material from one cave site in Romania (Richards et al., 2008a), with further similar data also from Romania published recently (Robu et al., 2013; Trinkaus and Richards, 2013). This led to the hypothesis that this cave bear population from the Carpathian Mountains had a more omnivorous diet than previously assumed, including meat and/or fish (Richards et al., 2008a). When all published isotopic data on European cave bears, corresponding to more than 530 measurements and more than 30 sites (Table S5 and Table S6), are represented on a map of Europe, it appears clearly that the Romanian cave bears with high d15N values are quite isolated (Fig. 8). All other analysed cave bears, from Spain to the Caucasus, exhibit d15N values in the range of coeval herbivores. Interestingly, these cave bears with low d15N values belong to all the recognized different genetic lineages, including representatives from U. spelaeus, Ursus ingressus and Ursus kudarensis (Knapp et al., 2009), while the Romanian cave bears belong to only one of these lineages, namely U. ingressus (Richards et al., 2008a). The most divergent group, U. kudarensis, diverged 270 to 800 thousand years ago from the other two groups, while U. spelaeus and U. ingressus divergence is estimated between 170 and 400 thousand years ago (Knapp et al., 2009). Since an overwhelming majority of these cave bears were definitely herbivores, it is conceivable that a shift from an omnivorous to a herbivorous diet occurred between the time when early cave bears diverged from the brown bear lineage, between 1.2 and 1.6 million years ago, and the time when U. kudarensis diverged from the rest of the cave bears, between 800

and 270 thousand years ago. The case of the Romanian cave bears with high d15N values makes the story more complicated than originally assumed if all cave bears were herbivorous, but the evolutionary implications for these bears depend on the dietary interpretation of these unusual isotopic values. If these cave bears with high d15N values were proven to be omnivores, this could mean that the herbivorous pattern seen in most cave bears was only an opportunistic use of part of the dietary spectrum, maybe in reaction to plant food availability and competition with other carnivores, or that these Romanian cave bears had to reverse from an originally herbivorous to an omnivorous diet due to local conditions making herbivory impossible. However, this omnivorous interpretation is far from demonstrated. In a further study including cave bear bone material from four cave sites in Romania, this hypothesis of omnivory for cave bears was supposedly supported by a comparison of the d13C and d15N values of cave bear bone collagen with the d13C and d15N values of hair from modern brown bears from Yellowstone National Park, USA (Robu et al., 2013). The Romanian cave bear d13C and d15N values were presented as overlapping on those of modern omnivorous brown bears, which was used as an indication of a similar diet, meaning an omnivorous diet for the Romanian cave bears (Robu et al., 2013). Unfortunately, this study suffered from several major flaws that makes its conclusions unfounded (Bocherens et al., 2014a). After taking into account the proper corrections, especially for the shifts in d13C values in atmospheric CO2 in recent times and for the different fractionation factors of

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Fig. 8. Map of Europe during MIS 3 (map background from ©RGZM/Grimm 2011. Since glacier extension and sea level correspond to the Last Glacial Maximum, they would have been fluctuating according to climatic changes during the Marine Isotopic Stage 3, between around 60 and 25 thousand years ago). The circles correspond to sites with analysed cave bears. Green circles stand for cave bears with d15N in the range of coeval herbivores, while yellow circles stand for cave bears with d15N in the range of coeval carnivores. The size of ne the circles depends on the number of specimens analysed in each site. The codes for the site numbers are as follows: 1. Cova Eiros, 2. Linares, 3. Olaskoa, 4. Font-de-Gaume, 5. Alde
le
tang, 10. Arcy-sur-Cure, 11. Goyet, 12. Scladina (layer 1A), 13. Mullerthal, 14. Rochedane, 15. Ba €renloch, 16. several cave, 6. Mialet cave, 7. Chauvet cave, 8. Balme-a-Collomb, 9. Pre re, Grotte des Plaints, Ba ^me aux Pirotas, Grotte de l'Ubena), 17. Drachenloch, 18. Wildenmanisloch, 19. Geissenklo €sterle, 20. sites in the Swiss Jura (Grotte Cracus, Grotte de la Toffie €hle, 22. Gamssulzen, 23. Ramesch, 24., Conturines, 25., Didje Babe, 26., Kulna (layer 7a), 27. Pestera cu Oase, 28. Cioclovina, 29. Muierii, 30. Hohle Fels, 21. Neue-Laubenstein-B€arenho Urs¸ilor, 31. Kudaro 3 (see Table S5 for summary of data and Table S6 for data new for this work).

carbon between hair keratin and bone collagen, it appears that the modern brown bears with low d15N values, the most herbivorous ones, indeed overlap wit the Romanian cave bears with low d15N values, while the modern brown bears with high d15N values are clear different from the Romanian cave bears with high d15N values (Bocherens et al., 2014a). Moreover, the cave bear specimens from Romania with high d15N value do not overlap with any other Pleistocene carnivores and do not overlap with Pleistocene brown bears with high d15N values (Fig. 9). In contrast, these Romanian cave bears overlap only with two types of Pleistocene herbivores, namely the woolly mammoths and the fallow deer from interglacial contexts, as well as with the isotopic values measured on tooth dentine of other cave bear populations (Fig. 9). Therefore the d13C and d15N values of these Romanian cave bears do not match an omnivorous or carnivorous diet in a terrestrial context. Only some freshwater fish may theoretical correspond to the observed values, but freshwater fish consumers typically exhibit very variable d13C values, which is not the case in Romania. Two interpretations remain plausible for the unusual Romanian cave bears. Instead of a carnivorous diet, these cave bears with high d15N may have recorded in their bone collagen the isotopic signature of hibernation (Grandal d'Anglade and Mosquera, 2008) that is usually restricted to tooth dentine and does not appear in the bone collagen of other European cave bears. Another possibility is that these bears still had a herbivorous diet, but that they relied on a different type of plant food than the other cave bear populations, more similar to that usually consumed by mammoths (probably dry grass: Bocherens, 2003) or to that consumed by fallow deer living in dense forests (plant food under a dense canopy, Bocherens et al., 1999). More work is needed to better understand the reasons for this unusual pattern. What is striking is to find caves so close from one another but with so different isotopic patterns between the cave bears that used these caves for hibernation. To decipher between physiology and diet as the main reason for the isotopic pattern, intra-individual variations would help: if dentine and bone exhibit the same isotopic differences as in other cave bear populations, a different diet is the cause of the pattern. If dentine and bone are isotopically similar, this would indicate that bone have recorded the same period of time than dentine, revealing a physiological cause for this pattern. Additionally, isotopic data on oxygen and sulphur could provide a better understanding of the climatic context and test for unconventional food for these bears,

as successfully performed in other cases (e.g. Bocherens et al., 2011b, 2014c; Münzel et al., 2014). 3.1.1.2. High-alpine cave bears. One ecological context where herbivorous cave bears were not expected is the high alpine domain, due to its challenging climatic conditions (Rabeder et al., 2000). When the first fossil evidence for cave bear was found in caves at altitudes higher than 2000 m, it was assumed that they were from interglacial warm periods, but the radiocarbon dating made on some of these bones demonstrated that they hibernated in these high caves during the colder period of the late Pleistocene, between around 60 and 30 thousand years ago (Rabeder et al., 2000). These cave bears present morphological differences compared to their lowland counterparts, some of them developing a body size reduction while others present changes in their dentition (Rabeder et al., 2008). Interestingly, these cave bears exhibit low nitrogen isotopic values, similar to those of coeval ungulates and clearly lower than those of predators when available (Fig. 10), and therefore indicating a herbivorous diet (e.g. Blant et al., 2010; Bocherens et al., 2011b; Pacher et al., 2012). These cave bears belong to the lineages U. spelaeus or U. ingressus (Bocherens et al., 2011b). One possibility is that these bears hibernated at high altitude, maybe to avoid predation from lowland carnivores, but spent the summer at lower altitude where plant food was more abundant than at the altitude of these caves. However, the pattern of variation of the d13C and d15N values among cave bear populations in different alpine caves suggest otherwise, i.e. the cave bears found in high altitude caves actually spent their active time more or less at the same altitude as where the caves they hibernated in were located. This conclusion can be reached when comparing the variations of d15N values in cave bear bones from alpine caves at different altitudes with those of coeval carnivores and modern alpine plants and herbivores (Fig. 11). In each case, the d15N values decrease with increasing altitude, a trend that is well recognized in modern plants and their consumers. This pattern in d15N values of cave alpine cave bears fits the expected values for cave bears feeding at altitudes similar to those of the caves they were found in, and also indicate a herbivorous diet, since their d15N values are around 5‰ lower than those of carnivores found at the same altitude (Fig. 11). Two cave bear populations from high altitude sites seem to diverge from this pattern. One is the cave bear population from the

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Fig. 9. Comparison of the d13C and d15N values of Romanian cave bears with other cave bears, Pleistocene brown bears, carnivores (wolves, lions, hyenas), mammoths and interglacial fallow deer.

Caucasus (Kudaro 3 cave) that belongs to the lineage U. kudarensis, where the d15N values are higher than expected for the altitude of the cave in comparison with cave bears from the European Alps. This could be due to a general climatic trend, with warmer temperatures in the Caucasus than in the Alps leading to higher

vegetation belts in the former region. Another exception is the case of Conturines cave, populated by cave bears of the lineage Ursus ladinicus and located on the southern side of the Alps in northern Italy, while all the other alpine sites are located on the western or northern side of the Alps. In this case as well, the d15N values of the

Fig. 10. d13C and d15N values of high-alpine cave bear populations from France, Switzerland, Germany and Austria, with coeval herbivores and carnivores (values in table S7). For €renloch and G. stands for the specimen from Gamssulzen. cave lions, B. stands for the specimen from Ba

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Fig. 11. Variations of d15N and d13C of cave bears and coeval predators according to site altitude. The green lines represent the trends observed for d15N and d13C values according to altitude in modern plants (dark green) and grazing herbivores (light green) in Bavaria (data from M€annel et al., 2007).

bears are clearly higher than expected if they had followed the same trend as the other alpine cave bears. This possibly reflects a Mediterranean influence on the southern side of the Alps, leading to differences in the altitudinal variation of the d15N values in northern Italy, or these cave bears may have spend their active time at altitudes lower than the cave where they used to hibernate. If the cave bears were herbivores and spent their summer in rather high altitudes, how could they find their forage? When looking at the variations of d13C values with increasing altitude, it is clear that the pattern of the cave bears is very different from the expectation when compared to modern plants and herbivores in a similar altitudinal range (Fig. 11). The d13C values of cave bears decrease rather than increasing with increasing altitude, while the carnivores remain more or less constant. This pattern could reflect ecological differences in the gradient of vegetation with altitude between the present time, where vegetation becomes denser when altitude decreases, while in the Pleistocene, the vegetation was open at all altitudes, and the decrease of d13C values with altitude might reflect the effect of low temperatures on the plants (Tieszen, 1991). A final aspect of the ecology of high-alpine cave bears that can be addressed with stable isotopic tracking is the type of predation they have been subject to. Based on the regular finds of cave lion bones in cave bear hibernation caves, bite marks on cave bear bones made by cave lions and the analogy with the antogonism between tigers and brown bears in Siberia, it has been suggested that cave lions were predators of cave bears (e.g. Rabeder et al., 2000; Diedrich, 2011b). The isotopic data available for high altitude sites confirm and refine this hypothesis. The wolf from B€ arenloch and the lion from Gamssulzen have d13C values indicative of predation of ungulates, not cave bears (Fig. 10). In contrast, the cave lion from B€ arenloch exhibits the expected d13C and d15N values for an individual consuming significant amounts of cave bear meat (Fig. 10). Not only is this pattern consistent with the hypothesis that cave lions were hunting cave bears, but it shows that this cave bear predation was performed by some cave lion individuals rather than others, since bone collagen averages the isotopic values of the prey consumed over many years. Therefore it appears that, even at high altitudes, cave bears were not immune against predation by cave lions, and this predation pressure may have been a reason for the choice of deep hibernation caves by cave bears (Diedrich, 2010).

3.1.1.3. Cave bear ecology and their extinction. An interesting aspect of cave bear ecology is the fact that two main different genetic lineages were present in Europe, U. spelaeus and U. ingressus, sometimes considered as different species (Rabeder et al., 2004). Although these bears seem to have been restricted to a herbivorous diet, the isotopic data show that they exhibited some ecological flexibility. In some cases, the two types of cave bear lived in close proximity during a significant amount of time, as in the Totes Gebirge Mountains in Austria (Hofreiter et al., 2004), while in other cases, one type seems to replace the other one through time, as in the Swabian Jura in southwestern Germany (Hofreiter et al., 2007; Münzel et al., 2011). Isotopic investigations helped to understand how they managed to coexist. In the Totes Gebirge (Austria), where populations of U. spelaeus and U. ingressus cave bears lived side by side for thousands of years, a clear difference is visible between the d13C and d15N values of these genetic types. Indeed, when represented as a cluster analysis, only one specimen of U. spelaeus falls in the cluster of U. ingressus, otherwise each type of bears is well separated from the other (Fig. 12). In both cases, brown bears U. arctos were also present and they exhibit different d13C and d15N values, indicative of an omnivorous diet (Münzel et al., 2011; Bocherens et al., 2011b). These different kinds of bears, when present together in a given ecological context, were clearly avoiding competition by partitioning the use of available resources. In both cases, brown bears were omnivores and cave bears herbivores. In the case of coexistence of two cave bear types, U. spelaeus and U. ingressus, both cave bear types were herbivores, but focused on different plant resources (Bocherens et al., 2011b). In contrast, where both types of cave bears follow each other as in the Swabian Jura, they use the same dietary niche (Münzel et al., 2011; Fig. 12). In addition, the cave bears from the Swabian Jura are morphologically not as different as in the Totes Gebirge, despite their genetic differences (Münzel et al., 2014). Therefore the cave bears may illustrate a case of ecological character displacement, where two closely related species exhibit morphological and ecological differences in the areas where their geographical distribution overlaps, but these differences are reduced or disappear were they occur alone (Brown and Wilson, 1956). This may well be the case for U. spelaeus and U. ingressus in Central Europe during the late Pleistocene. Clearly

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Fig. 12. Cluster analysis of d13C and d15N values of U. spelaeus, U. ingressus and U. arctos in a context of coexistence (Totes Gebirge) and succession (Swabian Jura).

the cave bear complex offers a very favourable material to test hypotheses of evolutionary ecology in a context of climate change and increasing anthropogenic pressure, thanks to the huge amount of fossil material with generally good biochemical preservation, that allows to perform isotopic and palaeogenetic investigations on the same specimens belonging to this taxon. Ultimately cave bear, an animal that was very abundant in the late Pleistocene of Europe, became extinct for reasons that are still unclear (e.g. Pacher and Stuart, 2009; Stiller et al., 2010). Although the palaeogenetic data suggest a long demographic decline that started up to 25,000 years before the final extinction (Stiller et al., 2010), so far the isotopic investigations on dated cave bears do no show any clear evidence for dietary change before its extinction (Bocherens et al., 2014d). This could indicate that some environmental changes happened so quickly that these bears did not have a chance to adapt, or that the extinction was not linked to a depletion of forage, but was related to competition with humans for hibernation caves or to direct predation by prehistoric human populations (e.g. Münzel and Conard, 2004; Stiller et al., 2010). 3.1.2. Giant short-faced bear (A. simus) This extinct bear species was one of the largest ursid ever to walk the Earth, with a body mass of 700 kg or more (Christiansen, 1999), out-weighted only by the giant short-faced bear from South American Arctotherium angustidens (Soibelzon and Schubert, 2011). As for

other extinct bears, the dietary ecology of this species has been heavily debated, with a reconstructed diet ranging from essentially herbivore, as suggested by its morphological similarity with the living Andean bear Tremarctos ornatus (e.g. Emslie and Czaplewski, 1985), to omnivore based on craniodental ecomorphology
n, 1967). (Figueirido et al., 2009) or largely carnivorous (Kurte The isotopic values published in Bocherens et al. (1995a), Matheus (1995), and Fox-Dobbs et al. (2008) were clearly in the range of coeval predators. These results were interpreted as reflecting a strongly carnivorous diet, in which meat acquisition may have been mainly performed through scavenging rather than active hunting (Matheus, 2003). The isotopic results published by Matheus (1995), combined with those from Fox-Dobbs et al. (2008), including a range of potential prey species such as mammoth, bison, horse and reindeer, allowed to estimate the relative contribution of these prey species in the meat consumption of shortfaced bears (Fig. 13). Using the mixing model Isosource, FoxDobbs et al. (2008) concluded that short-faced bears, showing relatively high d13C values, were specialized on reindeer. However, when isotopic data from Matheus (1995) are included, the shortfaced bear individuals with the highest d15N values could not eat only reindeer and they had to include prey with higher d15N values than the analysed reindeer. Recently published isotopic data for muskox in Yukon show that some individuals of this species had high d13C and d15N values (up to 7.7‰; Raghavan et al., 2014). Such

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Fig. 13. Short-faced bear collagen isotopic composition and reconstructed d13C and d15N values of their diet in Alaska and Yukon (~40e20,000 yr BP) (data from Matheus, 1995; Barnes et al., 2002; Fox-Dobbs et al., 2008).

ungulates could have been preyed upon by such short-faced bears to explain their high d13C and d15N values. Another possibility is the consumption of some meat from other carnivores, such as wolves or Homotherium, a possibility that would support the hypothesis of klepto-parasitism of short-faced bears upon coeval predators, chasing them from the carcasses of their prey (Matheus, 1995), while isotopic values suggest that some individuals may sometimes kill other predators and consumed them as well. The hypothesis that giant short-faced bears were specialized predators or scavengers has been challenged, based on ecomorphological investigations of this species (Figueirido et al., 2010). The high d13C and d15N values of A. simus prove that short-faced bears were not exclusively herbivores, but this does not mean that they did not also eat plant food. As explained previously, the relationship between the proportion of meat versus plant food and d15N values of the consumer collagen is not a linear one and bears with d13C and d15N values similar to those of carnivores may in fact have consumed up to 50% plant food (Fig. 5). Therefore an opportunistic foraging strategy including plant food up to 50% and meat of reindeer, muskox and possibly some predators, seems realistic, and consistent with the isotopic data and the conclusions of the ecomorphological studies. What the stable isotopic data can exclude as a dietary strategy for short-faced bears is a significant consumption of meat from horse and mammoth, as well as a purely vegetarian diet. This low consumption of mammoth and horse is surprising, since these two herbivore species have been evaluated to produce about 50% of the herbivore biomass in this ecosystem (Matheus, 2003). The pattern of prey partitioning among large carnivores in the mammoth steppe was probably also influenced by the ability of different predators to exploit differently different prey species, and the prey selection of the short-faced bear may have been limited by such

competition. So far no isotopic data from short-faced bears from lower latitudes are available, precluding an evaluation of the possibility that individuals of this species inhabiting areas richer in plant food might have been more herbivorous than their northern counterparts living in the mammoth steppe. In conclusion, the giant short-faced bear A. simus living in the easternmost part of the mammoth steppe ecosystem was a formidable creature that interacted with predatory carnivores as a competitor exploiting reindeer, possibly muskoxen, and taking his share on carcasses of large ungulates and their predators, but plant resources may have also been part of its dietary spectrum. 3.1.3. Brown bear (U. arctos) Brown bears were widespread across the whole range of the mammoth steppe during the late Pleistocene, although the fossil finds are much less frequent than for cave bears (e.g. Rabeder et al., 2000; Sabol, 2001). Considering the very wide ecological and dietary flexibility of the extant representatives of this species, it is expected that the fossil ones were also very variable in their ecology. Therefore isotopic tracking will be an essential tool to replace them in their respective trophic web, to evaluate which food items were consumed, how they competed with other large mammals including extinct species of bears, and to investigate the possible reasons for dietary changes across time and space for this species. Particularly interesting and well documented are two areas at both ends of the mammoth steppe ecosystem: eastern Beringia, where brown bears co-existed with the meat-eating giant short-faced bear until around 20,000 years ago, and Europe, where brown bears coexisted with essentially herbivore cave bears until around 24,000 years ago. In Alaska and Yukon, brown bears exhibit a shift of their isotopic values around the time of extirpation of the giant short-faced bear

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(Barnes et al., 2002; Fig. 14): the brown bears with dates older than 20,000 14C years BP, which coexisted with the giant short-faced bears, have virtually no overlap with this giant bear, all the d13C values are lower and most of the d15N values are lower for brown bears than for short-faced bears. In contrast, the brown bears with dates younger than 20,000 14C years BP, which lived after the extirpation of the giant short-faced bears, have generally higher d13C and d15N values than their older counterpart, and this isotopic range overlaps partly with the previous isotopic range of shortfaced bears. This isotopic shift can be interpreted as reflecting an increase of meat consumption after the extirpation of the mostly carnivorous giant short-faced bear. Such an ecological restriction of the smaller bear to a more vegetarian diet while a bigger bear species is more carnivore can be observed today between American black bear U. americanus and grizzly bear U. arctos horribilis (e.g. Belant et al., 2006), but this time with brown bear being the larger species and therefore dominant with access to the most proteinrich resources. In Europe, late Pleistocene brown bears contemporary to cave bears have been analysed from Belgium, Germany and the Czech Republic, together with coeval cave bears, as well as brown bears dating from the period after the extinction of cave bears, around 12,000 years ago (Fig. 14). The d13C values of brown bears are higher than those of cave bears, while the d15N values of most brown bears before 25,000 14C years ago are clearly higher than those of cave bears. In contrast, the younger brown bears have lower d15N values, in the former range of cave bears, and their d13C values tend to decrease. Some published data for more recent brown bears in the alpine region confirm that this trend continues into the early Holocene, with brown bears having d15N values in the range of coeval herbivores rather than higher, as it was the case for late Pleistocene € ppes et al., 2008). Once again, the disappearance of brown bears (Do a local very large bear seems to coincide with a significant dietary shift for brown bears. One possible interpretation is that the extinction of cave bears left a vacant niche for a mostly herbivorous large omnivore, and brown bears used it. However, an influence of

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the environmental change that occurred at roughly the same time, i.e. the beginning of the Holocene with warmer temperatures and more forested vegetation, may have also played a role in this dietary transition. The use of stable isotopic tracking could thus document two major dietary shifts for brown bears, in opposite directions, for two different areas of their distribution. Considering the contrasted ecological history of brown bears in northwestern North America and Europe, it is tempting to hypothesize that this different dietary history may have some implications on the current ecology of these brown bear populations (Fig. 15). For instance, as noted by Ward and Kynaston (p 84, 1995): “There are apparently some fundamental differences between the foods eaten by bears in North America and by those in Eurasia. Roots and other subterranean organs of plants are more important to North American bears, whereas ants are more commonly eaten in Eurasia.” The cause for this different dietary difference might be within the different environmental conditions nowadays on these two continents, but further isotopic investigations of ancient brown bears would allow to integrate the dietary history of different bear populations to better understand the food preferences of extant populations, with implications on their preservation. The isotopic data on fossil brown bears open the possibility that the dietary preferences of modern populations of this species may at least partially reflect a ghost of competition past. 3.2. Felids 3.2.1. Scimitar-tooth cat Homotherium This large machairodont felid was present in the easternmost part of the mammoth steppe ecosystem until 36,000 years ago (Fox-Dobbs et al., 2008). The remains of this species in Europe are too fragmentary to fully evaluate the occurrence of this species in the late Pleistocene, and no stable isotopes of these remains have been published, although collagen from a specimen found in the North Sea has been radiocarbon dated (Reumer et al., 2003). The post-cranial morphology of Homotherium led to the conclusion that

Fig. 14. Left. Changes in the d13C and d15N values of brown bears Ursus arctos before and after the extirpation of Short-faced bear in eastern Beringia. Data are from Matheus (1995), Barnes et al. (2002) and Fox-Dobbs et al. (2008). Right. Changes in the d13C and d15N values of brown bears Ursus arctos before and after the extinction of cave bears in Europe (Belgium, southwestern Germany, Czech Republic). Data are from Bocherens et al. (2011a, 2015a).

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Fig. 15. Summary of the isotopic/dietary shift of brown bears around the time of extinction of their ursid competitor, i.e. giant short-faced bears Arctodus simus in eastern Beringia (Alaska and Yukon) and cave bears Ursus spelaeus s.l. in Europe.

it was a cursorial predator, in contrast with other sabre-tooth cats that were probably ambush predators (e.g. Lewis, 1996, 2001; Galobart et al., 2003; Naples et al., 2011). The discovery of numerous mammoth remains in sites interpreted as a Homotherium dens led to the hypothesis of a dietary link between this big cat and proboscideans (e.g. Rawn-Schatzinger and Collin, 1981;
n Rawn-Schatzinger, 1987, 1992; Marean and Ehrhardt, 1995; Anto and Turner, 1997; Naples et al., 2011). Homotherium hunting juvenile proboscideans, such as mammoths in the context of the mammoth steppe, is a hypothesis that can be readily tested with stable isotopes of carbon and nitrogen, since mammoths present higher d15N values than all other herbivores that could be preyed on by Homotherium. Carbon and nitrogen isotopic data from eastern Beringia do not support the hypothesis that this morphologically specialized large cat was specialized in the hunting of proboscideans, woolly mammoth in this context. Most individuals of Homotherium presented by Fox-Dobbs et al. (2008) present d15N values in the same range than the mammoths and relatively scattered. Once the difference between d13C and d15N values of prey and predators is taken into account, the prey values of different individuals end up among reindeer, bison and horse and barely overlap with the lowest d15N values of mammoths (Fig. 16). Using a Bayesian mixing model, Yeakel et al. (2013) concluded that, on average for all values of specimens of the species, Homotherium consumed more yak (Bos mutus) than other herbivores, but included reindeer and bison, with less amounts of muskox, mammoth and horse. The scattering of the isotopic data of Homotherium individuals excludes the possibility that this species of carnivore was specialized on one specific prey (Fox-Dobbs et al., 2008). Since bone collagen reflects an average of many years for a large carnivore, individuals which isotopic values of prey fall at one end of the isotopic spectrum of prey (such as reindeer or horse) would have to consume essentially this prey and almost no other to endup with such isotopic compositions. This suggests that many individuals probably consumed a mixture of prey species but some individuals were more focused on a type of prey during their adult life. With the data available, it is not possible to know if this reflects a lack of other prey during this period, or a choice among different prey that were available but not consumed. In any case, this shows that scimitar cats were able to hunt different ungulates, including reindeer, horse, bison and most probably mammoth as well, but none of the analysed individual was a specialist mammoth eater. The scattering of the individual data also points to a rather individualistic behaviour and is not consistent with a social predator, contradicting some hypothesis on the behaviour of sabre-tooth cats. A final conclusion about Homotherium palaeobiology is that, in view of this rather flexible and non-specialized predatory behaviour, the reason for the disappearance of this species from the fossil record around 36,000

years ago is not easy to relate to known ecological changes around this period in eastern Beringia. 3.2.2. Cave lion Cave lions were present on the whole geographic expansion of the mammoth steppe biome. This large felid was on average 10% larger than extant African lions (Rabeder et al., 2000), and palaeogenetic investigations have shown that they belong to a distinct genetic lineage (Barnett et al., 2009). Due to its close relationship with extant lions that hunt preferentially zebras and antelopes in African savannah, a prey choice focused on horses and bisons has been assumed for cave lions, consistent with some occasional discoveries of trophic interactions between cave lions and bison (Guthrie, 1968, 1990; Turner, 2009; Stuart and Lister, 2011). In view of the large range of prey choice and habitats known for extant lion populations (e.g., Hopcraft et al., 2005; Patterson, 2007), and the contrast between the ecological conditions experienced by cave lions in the mammoth steppe compared to extant lions in intertropical environments, it is difficult to predict how cave lions could behave trophically in the late Pleistocene (Bocherens et al., 2011a). Here again, stable isotopic tracking of the dietary ecology of this large carnivore has proven helpful to sort out its palaeoecology. The recently published isotopic data for cave lions in western Europe have revealed a pattern with a scattering of individual data indicative of an individualistic behaviour in contrast with the social hunting of most extant lion populations, and a focus on two very different types of prey species, reindeer or cave bears, especially when cave hyenas were around (Bocherens et al., 2011a). The example of the mammoth steppe in Belgium around 30,000 years ago is a good illustration of this pattern (Fig. 17). Four lion individuals exhibit quite different d13C and d15N values that can be translated into contributions of different prey species using SIAR Bayesian model. One typical isotopic position of cave lions, also found in the southwestern Germany and the Moravian Plain, is a high d13C value that is higher than most other coeval carnivores (Bocherens et al., 2011a, 2015a). For such a lion, SIAR results indicate clearly a predominance of reindeer in its diet, other deer were also consumed, but most other prey were very limited (Fig. 17). In contrast, other individual cave lions have low d13C values, and the SIAR results for such an individual indicate a high amount of cave bears, some horse and mammoth, and very few deer and rhinoceros (Fig. 17). One other individual, with relatively low d15N values, gave through SIAR a dietary evaluation dominated by cave bears and deer, but low in other prey (Fig. 17). Finally, one cave lion individual is surprisingly similar to cave hyenas, and SIAR results indicate similar a diet than hyena, i.e. a mixture of almost all prey available (Fig. 17). This individual is actually directly dated to a time younger than the extirpation of cave hyenas in the region, and this type of diet for cave lions could be a consequence of the disappearance of its main competitor (Bocherens et al., 2011a). These

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Fig. 16. Scimitar-toothed cat Homotherium collagen isotopic composition and prey selection in Alaska and Yukon (~40e20,000 yr BP) (data from Matheus, 1995; Barnes et al., 2002; Fox-Dobbs et al., 2008).

results clearly indicate a solitary hunting behaviour of cave lions in Europe at least, with a selection of prey at the margins of the range of herbivores regularly consumed by cave hyenas. In Siberia, in the absence of cave hyena, the d13C values of cave lion were more negative than for European individuals (Fig. 18). This could reflect either a shift of prey selection, less focused on reindeer and more on prey with lower d13C values such as bison (Kirillova et al., 2014). However, detailed reconstruction of the trophic web is still pending more isotopic data on different prey species in Siberia. For mammoths, the only species with enough data for a valid comparison, the d13C values are lower in Siberia than in Europe, leaving open the possibility that cave lions had a similar diet than in Europe if all herbivorous species had d13C values lower than their equivalent in Europe. Before their final extinction from Europe, cave lions were still focused on reindeer as their main prey (Bocherens et al., 2011a; Yeakel et al., 2013). The same conclusion is suggested by the high d13C values (18.2‰) measured for a Lateglacial cave lion from northern Spain (Stuart and Lister, 2011). A similar pattern is visible in eastern Beringia (Fig. 19) (Fox-Dobbs et al., 2008; Yeakel et al., 2013). In Europe, Lateglacial wolves seem to have outcompeted cave lions from access to other prey species based on the isotopic values of these wolves at the center of the carnivore range, maybe using the advantage of collective hunting even if individual body size of wolves was smaller than for lions (Bocherens et al., 2011a). The implications of the currently available isotopic data on cave lions in the mammoth steppe ecosystem are important. First of all, the scattering of the isotopic values among cave lion individuals, at least in pre-LGM Europe, indicate a solitary behaviour for this species, in agreement with arguments based on the poor development of mane in this species (Guthrie, 1990). In terms of

competition and niche partitioning with other large carnivores of the mammoth steppe, cave lions seem to be at a disadvantage and seem to have been dominant predators only in areas where the climatic conditions were too cold for other large carnivores, such as hyena that were absent in high altitude and northern Siberia, or after hyenas were extirpated. Indeed, when co-existing with other large carnivores with a collective social structure, such as cave hyenas in Europe before 25,000 years ago or wolves after 15,000 years ago, cave lions seem to have limited their prey choice to those not taken by these other predators, essentially reindeer, as well as cave bears as long as they were around. Interestingly, there is no isotopic evidence so far that the last cave lions in western Europe shifted their prey selection on species more adapted to forested conditions, such as red deer and roe deer, with the warming trend of the Lateglacial. This is surprising since cave lions were present in Europe during the Last Interglacial period (e.g., Bona, 2006; Diedrich, 2011b), but the last cave lions had suffered a loss of genetic diversity (Barnett et al., 2009), which might have led to a more limited ability to adapt to environmental change. The youngest fossil record of cave lion seems to coincide with the extirpation of reindeer in western Europe, but there is no evidence for cave lions surviving longer in northern Europe, where reindeer shifted their geographic distribution in the Holocene (Sommer et al., 2014). 3.3. Canids Wolf (Canis lupus) is the most widespread large predator in Eurasia and North America nowadays, even if the geographic distribution of this species has shrunk due to its active extermination by humans. This distribution covers a large range of climatic conditions from arctic tundra to temperate forests and steppes,

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Fig. 17. Scatter-plot of d13C and d15N values of cave lions in the late Pleistocene of Belgium, 40 to 25 thousand years ago, compared to coeval herbivores and carnivores (modified from Bocherens et al., 2011a), with the evaluation of the contribution of prey species using SIAR Bayesian model for 4 lion individuals and the average of cave hyenas.

showing that this species is not limited by climate (e.g. Mech, 1970). This species was also an ubiquitous representative of the mammoth steppe carnivore guild, but in contrast with the current situation where competition with other predators is limited but the main factor limiting their distribution is anthropogenic, wolves had many potential competitors in the mammoth steppe. Modern wolves are hypercarnivores, living in packs and feeding preferentially on ungulates, especially cervids, but can shift on smaller prey if needed (e.g., Mech, 1970; Flower and Schreve, 2014). 3.3.1. Diversity of Pleistocene wolves Pleistocene wolves were morphologically and genetically more diverse than the modern ones. The body size of Pleistocene wolves has changed since the first occurrence of the species around 300,000 years ago, with usually being smaller during interglacial periods, while the late Pleistocene wolves coeval with the mammoth steppe were larger than the modern ones (Flower and Schreve, 2014). Moreover the proportions of different parts of teeth and cranial features showed differences between modern wolves and their Pleistocene counterparts (e.g. Leonard et al., 2007;


et al., 2012; Flower and Schreve, 2014). Such morphoGermonpre logical features have been tentatively related to dietary differences (e.g. Leonard et al., 2007; Flower and Schreve, 2014). In addition, some large canids from upper Palaeolithic sites in Belgium, Czech Republic and southern Siberia have shown morphological differences compared to coeval and modern wolves and are more similar
et al., 2009, 2012, 2015; Ovodov to archaic dogs (e.g. Germonpre et al., 2011). These peculiar large canids have been considered to be early domesticated wolves, therefore Palaeolithic dogs (e.g.
et al., 2009, 2012, 2015). This interpretation has been Germonpre questioned by others who interpret at least some of these large canids as a specialized morph of wolf, more adapted to scavenge the carcasses of very large herbivores, such as mammoths, as well as bisons and horses (Crockford and Kuzmin, 2012). Not only were Pleistocene wolf morphologically diverse and different from modern wolf, they were also genetically different. A palaeogenetic investigation showed that late Pleistocene wolves from eastern Beringia belong to a now extinct genetic type that is not ancestral to modern wolf in this region (Leonard et al., 2007). There is also some evidence for loss of genetic diversity among

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Fig. 18. Comparison of histogrammes of d13C values in cave lions in Europe and Eastern Siberia, with those of cave hyenas in Europe (data in Table S8). A significant shift of d13C values in direction of the range of cave hyenas is visible for cave lions from Siberia.

European Pleistocene large canids (Thalmann et al., 2013). In this context, stable isotopic tracking could be used to test hypotheses related to possible dietary differences among morphological or genetic types of large canids in the mammoth steppe context. 3.3.2. Pleistocene wolves in the late pleistocene carnivore guild The first dietary hypothesis to be tested is the consumption of large prey by extinct Alaskan wolf ecomorph, whose cranial morphology with short and broad muzzle as well as large carnassial suggests the possibility to generate large bite forces, possibly

reflecting an adaptation for killing and consuming large and for scavenging (Leonard et al., 2007). When the d13C and d15N of these wolves are used to reconstruct the isotopic values of their average prey and compared to the isotopic values of large herbivores in the same area, the wolf prey values overlap with those of herbivores except mammoth, i.e. horse, bison and reindeer (Leonard et al., 2007). When compared to the isotopic values of other predators, these wolves seem indeed to occupy the central range of isotopic values of prey, and does not contradict the interpretation of the consumption of the carcasses of prey such as horse, bison and

Fig. 19. Prey contribution in the diet of post-LGM cave lions from western Europe and eastern Beringia reconstructed using MixSIR (modified from Yeakel et al., 2013). In both cases, reindeer is the dominant prey.

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reindeer, either while actively hunting or scavenging (Fox-Dobbs et al., 2008; Yeakel et al., 2013). In Europe, two ecological aspects can be tested: the impact of competition with other carnivores, such as cave hyenas and cave lions, and the possible dietary difference between “Pleistocene
et al., 2009; Bocherens wolves” and “paleolithic dogs” (Germonpre et al., 2015a). Niche partitioning between wolves and other predators can be evaluated for Belgium around 40,000 years ago, where isotopic data for wolves, cave hyenas and cave lions have been published (Bocherens et al., 2011a). In this case, the wolves exhibit lower d15N values than cave hyenas and cave lions, with some overlap with some cave lion individuals (Bocherens et al., 2011a). As for cave lions in the same context, it seems that wolves were out-competed by cave hyenas, and had a restricted access to prey with high d15N values, such as mammoth, woolly rhinoceros, and horses. Using a Bayesian mixing model, this pattern is confirmed by Yeakel et al. (2013), with a low consumption of mammoths, woolly rhinoceros, horse and reindeer, while chamois and cervids other than reindeer (i.e. giant deer and red deer) were preferentially consumed (Fig. 20). In contrast, the distribution of isotopic values after the Last Glacial Maximum, around 14,000 years ago, is quite different, with wolves in the center of the predator range, and lions restricted to high d13C values prey (Bocherens et al., 2011a). This pattern reflects a niche partitioning between cave lions and wolves, with the latter having more of less equal access to any prey species, while cave lions essentially consumed reindeer (Yeakel et al., 2013) (Fig. 20). It seems that the extirpation of the cave hyena opened the niche of dominant large predator for the wolf rather than for the cave lion during the Lateglacial, anticipating the next step of the reorganization of the carnivore guild, i.e. the extinction of cave lion while wolves survived until recent times. 3.3.3. “Pleistocene wolves” versus “Palaeolithic dogs” The question of possible dietary differences between “Pleistocene wolves” and “Palaeolithic dogs” was addressed for Belgian
et al., 2009) and for those from the Czech canids (Germonpre Republic, in the Gravettian site of Predmostí I (Bocherens et al., 2015a). The isotopic results measured on the Belgian canids were difficult to interpret due to mixture of undated samples or samples with different ages (around 30,000 years BP to the Holocene), in a context were significant fluctuations of d15N values
are known to occur during the time represented (Germonpre et al., 2009). In contrast, the case of Predmostí I yielded very important isotopic results (Bocherens et al., 2015a). This prehistoric site dated to around 28,000 years BP yielded a diverse faunal assemblage with herbivores and carnivores, including large canids of both types. In contrast with other sites of the mammoth steppe, the stable isotope data show that several carnivores have consumed significant amounts of mammoth meat, first of all the Gravettian humans (Fig. 21). This result shows that mammoth carcasses not only provided raw material for dwelling construction and artefact making, but also an important source of proteins. Moreover, the isotopic results show a difference between both types of canids. Contrarily to the expectation of the “short-faced wolf” as scavenger of very large prey (Crockford and Kuzmin, 2012), this morphotype exhibited high d13C values indicating a significant contribution of reindeer and muskox meat, rather than mammoth and woolly rhinoceros (Fig. 21). The “Pleistocene wolves” had d13C and d15N values more similar to those of prehistoric humans, reflecting a high amount of mammoth meat in the diet. Since brown bears and wolverine also have isotopic values indicative of mammoth meat consumption, it is conceivable that the carcasses of mammoths hunted by humans were regularly

available for scavenging by other predators. In contrast, the virtual absence of mammoth meat in the diet of the possible dogs suggests that these animals had no free access to this resource, and fits well in a scenario where these large canids represent “Palaeolithic dogs” which diet was controlled by humans, who fed their dogs with lower quality food (reindeer meat), as seen in ethnographic examples, and possibly used the dogs as transport helpers (Bocherens et al., 2015a). Interestingly, the other pre-LGM dog from Siberia also has high d13C values (Ovodov et al., 2011). This may also indicate a high amount of reindeer in its diet, but these isotopic data are lacking a context since no other faunal remains from this site have been analysed for isotopes so far. Further isotopic investigations on large canids from prehistoric sites will certainly help to better understand the possible relationships between some of these canids and the prehistoric human populations. 3.4. Hyenas Cave hyenas belong to the same genetic group than extant spotted hyenas (Rohland et al., 2005; Shen et al., 2014). These large carnivores are renowned scavengers but they are also able to hunt efficiently large and medium-sized herbivores, especially since they are gregarious predators, able to steal prey from lions when they deal with single individuals, such as males (e.g. Di Silvestre et al., €ner et al., 2002; Holekamp, 2006). During the late Pleis2000; Ho tocene, cave hyenas were absent from the northern parts of Europe and Siberia, probably due to the lack of morphological adaptations to severe cold conditions in these regions (e.g. Baryshnikov and Petrova, 2008). In the fossil localities where cave hyenas were present together with other large predators of the mammoth steppe, such as cave lions and wolves, hyenas typically cluster in the middle range of isotopic values, with limited variation among individuals (e.g. Bocherens et al., 2011a). This pattern is consistent with a collective predatory and scavenging behaviour for this species, and indicates that cave hyenas consumed more or less all large and mediumsized prey available, in similar amounts on average. This is clearly illustrated by the example of late Pleistocene of Belgium, around 30 to 40 thousand years ago, where the isotopic values of hyenas are well explained by a relatively equal contribution of all available large herbivores, while cave lion is strongly focused on reindeer (Fig. 17). A similar pattern occurs in southwestern Germany (Bocherens et al., 2011a; Yeakel et al., 2013), as well as in southern England (Bocherens et al., 1995b). The overlap of isotopic values between hyenas and other large carnivores is very limited. Only a handful of cases have been observed, with brown bear, leopard and wolverine have d13C and d15N values in the range of those of cave hyenas in Belgium (Bocherens et al., 2011a). The only cave lion in this case was dated to a date younger than the last cave hyena in the region, therefore could be witnessing a shift of dietary niche following the extirpation of its main competitor. Interestingly, Neandertals from Belgium and from western France also plot outside the range of d13C and d15N values of hyenas, with higher d15N values indicating consumption of more mammoth meat (Bocherens et al., 2005, 2011b, 2013). Such a pattern could indicate that cave hyenas were the dominant predator of the mammoth steppe where the climatic conditions were not too rigorous for them, out-competing not only other large predators such as cave lions and wolves, but also Neandertals. Such a key role in the carnivore guild has even been suggested to have limited the dispersal of ancient humans into some areas of Asia, and that only the domestication of wolves could have given a decisive advantage to modern humans against cave hyenas (e.g. Summerill and Turner, 2003).

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Fig. 20. Prey contribution in the diet of pre-LGM and post-LGM wolves from Western Europe reconstructed using MixSIR (modified from Yeakel et al., 2013).

However, there are cases were the isotopic values of cave hyenas are more widespread. For instance, the total range of d13C values for specimens from Great-Britain is relatively large, from 20.7 to 18.4‰ (Bocherens et al., 1995b; Jacobi et al., 2006), suggesting that some individuals were focusing on a narrower range of prey, such as reindeer in the case of high d13C values. This could reflect areas and periods were the availability of prey resources were

changing, due to short-term climatic changes, as it is unlikely that cave hyenas had to reduce their prey selection due to competition with other carnivores. Therefore, the isotopic values of cave hyenas could be indicative of the relative abundance of large herbivores across the part of the mammoth steppe where they were present and provide interesting insight on the biomass of different ungulate species during the late Pleistocene.

Fig. 21. Simplified trophic relationships between predators and their prey based on d13C and d15N values of bone collagen in the Gravettian site of Predmostí I (modified from Bocherens et al., 2015a).

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4. Conclusions The use of carbon and nitrogen stable isotopes in the collagen extracted from fossil skeletal remains of large carnivores from the mammoth steppe has provided essential information on the dietary preferences of extinct species, such as scimitar-tooth cat, cave lion, cave bear and giant short-faced bear. In addition, and probably even more importantly for further research, it also gives a possibility of documenting changes in the trophic relationships among the large mammals of this ancient biome without modern analogue. Indeed, this purely phenotypic record of the conditions of life for each individual available as fossil specimen can be confronted with other environmental indicators to test hypotheses about the reaction of key members of a terrestrial ecosystem in the face of ecological changes. A direct comparison of the isotopic values of different predators that lived together can already provide insights on niche partitioning and competition. To link these isotopic values to differences in prey choice, it is necessary to have a reasonable knowledge of the “isotopic landscape”, i.e. the diversity of isotopic values among potential prey in the same context. The best case is when isotopic data can be gathered on material from the same site and period, or located in close spatial or temporal proximity, with no evidence for isotopic shifts of the baseline in relationships to short-term environmental events. Using different approaches, such as Bayesian mixing models, some quantitative evaluations of the contribution of different prey can be made. The obtained figures allow comparisons between regions, periods and contexts where different large carnivores were coexisting. It is possible to test the impact of different abiotic and biotic factors on the carnivore guild of the mammoth steppe biome, increasing the range of realized niches for the studied carnivores species. This type of information may prove useful for conservation of the remaining populations of these species. The large carnivore guild has been profoundly disrupted during the last 40,000 years in the former territory of the mammoth steppe biome. Large climatic fluctuations may have caused reductions or expansions of the geographic distribution of preferred prey species. In such a context, stable isotope tracking helps to test if a predator reacted through a shift of prey preference or exhibited niche conservatism and retained its previous prey preference as long as possible. Using the knowledge on prey selection and prey partitioning among large carnivores gained from stable isotopic tracking, it appears that the composition of the predator community was probably more important than the climatic conditions. Also of crucial importance are the impacts of prehistoric humans on large carnivores, either indirectly through changes in the abundance of prey or competition for the same prey, or directly through hunting and extermination. For instance, the extensive exploitation of mammoth by Gravettian people in Moravia seems to have given large carnivores such as wolves and brown bears, and even smaller ones such as wolverine and polar foxes, an opportunity to scavenge mammoth carcasses, a phenomenon that stable isotopic tracking did not document in other areas where mammoth were dwelling, such as eastern Beringia. It becomes more and more clear that the interactions between human populations and large carnivores were complex and not uniform, ranging from commensalism and domestication (that could lead to a shift of isotopic values of such carnivores due to sharing human food or control of their diet by humans) to competition and predation on one another (also testable with stable isotopes). The stable isotopic tracking of large carnivore ecology has already provided interesting results but more will come with better interconnections with other disciplines, such as palaeogenetic, in order to understand the possible genetic causes of

dietary variation in ancient populations of carnivores, as well as the ecological consequences of loss of genetic diversity. The collagen preserved in the fossil bones of large carnivores is an archive which isotopic message is just starting to be interpreted and should yield many invaluable insights on non analogue past ecosystems. Acknowledgements This review is based on published data but only on the isotopic analysis of numerous additional fossil remains made accessible by many colleagues who I want to thank warmly: J.-J. Cleyet-Merle, S.
e National de Pre
histoire, Les Eyzies de Tayac, Madelaine (Muse France), Charles Schouwenburg (The Netherlands), Michel Blant (Fribourg, Switzerland), Irka Hajdas (ETH, Zurich, Switzerland), Francine David (MAE, France), Dominique Armand (Univ. Bordeaux, France), Thierry Tillet (Univ. Grenoble, France). I also want to thank all the colleagues whose contribution was essential in the preparation and analysis of the fossil material studied under my supervision. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.quascirev.2015.03.018. References Ambrose, S.H., 1990. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 17, 431e451. Ambrose, S.H., 1991. Effects of diet, climate and physiology on nitrogen isotope abundances in terrestrial foodwebs. J. Archaeol. Sci. 18, 293e317. Ambrose, S.H., DeNiro, M.J., 1986. The isotopic ecology of East African mammals. Oecologia 69, 395e406. Amundson, R., Austin, A.T., Schuur, E.A.G., Yoo, K., Matzek, V., Kendall, C., Uebersax, A., Brenner, D., Baisden, W.T., 2003. Global patterns of the isotopic composition of soil and plant nitrogen. Glob. Biogeochem. Cycles 17, 1031. http://dx.doi.org/10.1029/2002GB001903. Anderson, P.M., Lozhkin, A.V., 2001. The stage 3 interstadial complex (Karginskii/ middle Wisconsinan interval) of Beringia: variations in paleoenvironments and implications for paleoclimatic interpretations. Quat. Sci. Rev. 20, 93e125.
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