Ancient DNA and osteological analyses of a unique paleo-archive reveal Early Holocene faunal expansion into the Scandinavian Arctic.

Paleo-archives are essential for our understanding of species responses to climate warming, yet such archives are extremely rare in the Arctic. Here, we combine morphological analyses and bulk-bone metabarcoding to investigate a unique chronology of bone deposits sealed in the high-latitude Storsteinhola cave system (68°50' N 16°22' E) in Norway. This deposit dates to a period of climate warming from the end of the Late Glacial [~13 thousand calibrated years before the present (ka cal B.P.)] to the Holocene thermal maximum (~5.6 ka cal B.P.). Paleogenetic analyses allow us to exploit the 1000s of morphologically unidentifiable bone fragments resulting in a high-resolution sequence with 40 different taxa, including species not previously found here. Our record reveals borealization in both the marine and terrestrial environments above the Arctic Circle as a naturally recurring phenomenon in past periods of warming, providing fundamental insights into the ecosystem-wide responses that are ongoing today.

Early evidence for bear exploitation during MIS 9 from the site of Schöningen 12 (Germany).

A cutmarked bear metatarsal and phalanx from the German open-air sites of Schöningen 12 II-1 and 12 B, respectively, correlated with the interglacial optimum of MIS 9 (ca. 320 ka), provide early evidence for the exploitation of bear skins. Archaeological sites with evidence of bear exploitation from the Lower Paleolithic are rare, with only Boxgrove (United Kingdom) and Bilzingsleben (Germany) yielding cutmarked bear bones indicating skinning. We interpret these finds as evidence for bear hunting and primary access since bear skins are best extracted shortly after the animal's death. The very thin cutmarks found on the Schöningen specimens indicate delicate butchering and show similarities in butchery patterns to bears from other Paleolithic sites. The Eurasian Lower Paleolithic record does not show any evidence for the exploitation of bear meat; only Middle Paleolithic sites, such as Biache-Saint-Vaast (France; ca. 175 ka) and Taubach (Germany; ca. 120 ka), yield evidence for the exploitation of both skin and meat from bear carcasses. Bear skins have high insulating properties and might have played a role in the adaptations of Middle Pleistocene hominins to the cold and harsh winter conditions of Northwestern Europe.

Shoulder osteoarthritis in a European saber-toothed cat (Homotherium latidens) from the Lower Palaeolithic site of Schöningen (Germany).

Evaluation of a right ventral scapula fragment from a mature Homotherium latidens from Schöningen, Germany (337-300 ka before present - MIS 9) revealed lesions consisting of an osteophyte at the caudal border of the glenoid cavity, and a large, multilobular, cystic feature in the medio-caudal glenoid cavity. Based on the type of lesions, their localization, their severity, and exclusion of several nutritional and other etiologies such as immune mediated disease, joint infection (septic arthritis), and joint tumors, we conclude that the lesion was caused by trauma or age-related shoulder osteoarthritis (or possibly both). We cannot speculate whether the condition was symptomatic, but if it was, the animal must have functioned well enough to hunt or scavenge, since it survived a significant period of lesion development.

Evolution and extinction of the giant rhinoceros Elasmotherium sibiricum sheds light on late Quaternary megafaunal extinctions.

Understanding extinction events requires an unbiased record of the chronology and ecology of victims and survivors. The rhinoceros Elasmotherium sibiricum, known as the 'Siberian unicorn', was believed to have gone extinct around 200,000 years ago-well before the late Quaternary megafaunal extinction event. However, no absolute dating, genetic analysis or quantitative ecological assessment of this species has been undertaken. Here, we show, by accelerator mass spectrometry radiocarbon dating of 23 individuals, including cross-validation by compound-specific analysis, that E. sibiricum survived in Eastern Europe and Central Asia until at least 39,000 years ago, corroborating a wave of megafaunal turnover before the Last Glacial Maximum in Eurasia, in addition to the better-known late-glacial event. Stable isotope data indicate a dry steppe niche for E. sibiricum and, together with morphology, a highly specialized diet that probably contributed to its extinction. We further demonstrate, with DNA sequencing data, a very deep phylogenetic split between the subfamilies Elasmotheriinae and Rhinocerotinae that includes all the living rhinoceroses, settling a debate based on fossil evidence and confirming that the two lineages had diverged by the Eocene. As the last surviving member of the Elasmotheriinae, the demise of the 'Siberian unicorn' marked the extinction of this subfamily.

Excavations at Schöningen and paradigm shifts in human evolution.

The exceptional preservation at Schöningen together with a mixture of perseverance, hard work, and sheer luck led to the recovery of unique finds in an exceptional context. The 1995 discovery of numerous wooden artifacts, most notably at least 10 carefully made spears together with the skeletons of at least 20 to 25 butchered horses, brought the debate about hunting versus scavenging among late archaic hominins and analogous arguments about the purportedly primitive behavior of Homo heidelbergensis and Neanderthals to an end. Work under H. Thieme's lead from 1992 to 2008 and results from the current team since 2008 demonstrate that late H. heidelbergensis or early Neanderthals used sophisticated artifacts made from floral and faunal materials, in addition to lithic artifacts more typically recovered at Lower Paleolithic sites. The finds from the famous Horse Butchery Site and two dozen other archaeological horizons from the edges of the open-cast mine at Schöningen provide many new insights into the technology and behavioral patterns of hominins about 300 ka BP during MIS 9 on the Northern European Plain. An analysis of the finds from Schöningen and their contexts shows that the inhabitants of the site were skilled hunters at the top of the food chain and exhibited a high level of planning depth. These hominins had command of effective means of communication about the here and now, and the past and the future, that allowed them to repeatedly execute well-coordinated and successful group activities that likely culminated in a division of labor and social and economic patterns radically different from those of all non-human primates. The unique preservation and high quality excavations have led to a major paradigm shift or "Schöningen Effect" that changed our views of human evolution during the late Lower Paleolithic. In this respect, we can view the behaviors documented at Schöningen as a plausible baseline for the behavioral sophistication of archaic hominins of the late Middle Pleistocene and subsequent periods.

Lower Paleolithic bone tools from the 'Spear Horizon' at Schöningen (Germany).

The Lower Paleolithic locality of Schöningen 13 II-4 is famous for the discovery of wooden spears found amongst the butchered remains of numerous horses and other large herbivores. Although the spears have attracted the most interest, other aspects of the associated artifact assemblage have received less attention. Here we describe an extraordinary assemblage of 88 bone tools from the 'Spear Horizon.' This sample includes numerous long-bone shaft fragments (mostly of horse), three ribs used as 'retouchers' to resharpen flint tools, and a complete horse innominate that was used as an anvil in bipolar knapping. Most of the retouchers were prepared by scraping the diaphysis of fresh and dry long-bones. Technological analysis of the associated lithic assemblage demonstrates exhaustive resharpening to maintain functional cutting edges. Whereas the flint tools were brought to the site, curated, and maintained, the retouchers had a shorter use-history and were either discarded after a limited period or broken to extract marrow. Horse and bison metapodials with flaked and rounded epiphyses are interpreted as hammers used to break marrow bones. Several of the 'metapodial hammers' were additionally used as knapping percussors. These constitute the earliest evidence of multi-purpose bone tools in the archeological record. Our results highlight the advanced knowledge in the use of bones as tools during the Lower Paleolithic, with major implications for understanding aspects of non-lithic technology and planning depth in early hominins.

Overview and new results from large-scale excavations in Schöningen.

Archaeological finds including spears, other wooden artifacts, lithic artifacts, and bones with impact scars and cut marks document the repeated presence of hominins on the shoreline of an approximately 300,000 year old lake near Schöningen in Northern Germany. Continuing excavations have uncovered in the locality "Schöningen" at least 20 sites dating to the late Lower Paleolithic. Schöningen is therefore not only a singular archaeological site with remarkable finds; it is a vast locality that preserves a multifaceted archaeological landscape with numerous sites. Ongoing excavations have exposed several large surfaces with organic materials dating to MIS 9. In particular, recent excavations have uncovered new sections belonging to the original Spear Horizon from Schöningen 13 II-4 (the Horse Butchery Site). Current research in Schöningen places the exceptional artifacts within a spatial and environmental context, and provides a wealth of new information on the subsistence strategies and settlement dynamics of the inhabitants of these short-term lakeside occupations. Schöningen, with an overall excavated area of 9400 m(2), is one of the largest excavated archaeological localities from MIS 9. Here we present a summary of all the sites, as well as the most relevant excavated areas since 2008 (excavations Tübingen/NLD).

The larger mammal fauna from the Lower Paleolithic Schöningen Spear site and its contribution to hominin subsistence.

The locality Schöningen (Germany) is an important source of knowledge about Lower Paleolithic hominin subsistence. The locality includes a series of sites dated to the late Middle Pleistocene with a Holsteinian (MIS 11) and Reinsdorf Interglacial (MIS 9) age. One of the youngest sites is Schöningen 13 II-4, the Spear Horizon site also known as the Horse Butchery site. The organic remains excavated here are exceptionally well-preserved as they were embedded in anaerobic, waterlogged sediments in an area where the groundwater is rich in calcium carbonate. The fossil assemblage is ideal for the study of patterns in hominin interference with the mammalian species encountered at the site. The vertebrate record is extensive and very diverse. The fossil larger carnivore guild of the Spear Horizon faunal assemblage includes saber-toothed cat, fox, and wolf. Herbivores are represented by an elephant species, two equid species, two rhinoceros species, two cervid species, and two large bovid species. Evidence of hominin interference presents itself as either marks on skeletal remains related to the use of bones as knapping tools or hammers, or as marks that indicate butchering activities such as skinning, dismembering, defleshing, filleting, and marrow extraction. The humerus of the saber-toothed cat clearly shows that the bone has been used as a knapping tool. The fossil remains of the other larger carnivores do not show any signs of hominin interference or exploitation. This also applies to the limited number of elephant and rhinoceros remains found at the site. The large horse Equus mosbachensis dominates the larger mammal record and played a major role in hominin subsistence. Marks on the horse bones indicate that a large number of carcasses have been butchered. Traces on the fossil remains of both red deer (Cervus elaphus) and the large bovids also indicate exploitation by Lower Paleolithic hominins.

The European saber-toothed cat (Homotherium latidens) found in the "Spear Horizon" at Schöningen (Germany).

The 300,000 year old Lower Paleolithic site Schöningen 13 II-4 became world famous with the discovery of the oldest well-preserved and complete wooden spears. Through ongoing excavations, new archaeological discoveries of scientific importance are still being made from the same archaeological layer where the spears were found. In this context, remains of a rare carnivore species, the European saber-toothed cat (Homotherium latidens), were recovered. Here we present five teeth and one humerus fragment that are unambiguously from two individual saber-toothed cats. The humerus is a unique specimen; it shows evidence of hominin impacts and use as a percussor. The Homotherium remains from Schöningen are the best documented finds of this species in an archaeological setting and they are amongst the youngest specimens of Homotherium in Europe. The presence of this species as a carnivore competitor would certainly have impacted the lives of late Middle Pleistocene hominins. The discovery illustrates the possible day-to-day challenges that the Schöningen hominins would have faced and suggests that the wooden spears were not necessarily only used for hunting, but possibly also as a weapon for self-defense.

Carbon and nitrogen stable isotopes of well-preserved Middle Pleistocene bone collagen from Schöningen (Germany) and their paleoecological implications.

Carbon and nitrogen stable isotopes in bone collagen can provide valuable information about the diet and habitat of mammal species. However, bone collagen degrades in normal circumstances very rapidly, and isotope analyses are therefore usually restricted to fossil material with a Late Pleistocene or Holocene age. The Middle Pleistocene site of Schöningen, dated to around 300,000 years ago, yielded bones and teeth with an exceptionally good state of collagen preservation. This allowed us to measure reliable biogenic carbon and nitrogen stable isotope ratios for different herbivorous taxa from the families Elephantidae, Rhinocerotidae, Equidae, Cervidae, and Bovidae. The results provide insights regarding the paleoenvironmental setting in which Middle Pleistocene hominins operated. The vegetation consumed by the herbivores from the famous spear horizon originates from open environments. During the climatic Reinsdorf Interglacial optimum, the landscape seems to have been relatively open as well, but certainly included parts that were forested. The results also indicate some niche partitioning; different herbivore species used different plant resources. For instance, the horses seem to have been predominantly browsers, while the straight-tusked elephants were feeding chiefly on grass.

Investigation of equid paleodiet from Schöningen 13 II-4 through dental wear and isotopic analyses: Archaeological implications.

The paleodietary traits of the equid population from Schöningen 13 II-4 were investigated through tooth mesowear and microwear analyses, as well as stable isotopic analyses. The mesowear pattern observed on the upper teeth indicates a low abrasion diet with a significant amount of browse in the diet of the horses. The tooth microwear analysis and the isotopic data confirm that the horses from Schöningen 13 II-4 were mixed feeders, like many populations from other Pleistocene localities in Northern and Eastern Europe. Microwear also provides information on seasonal changes in the diet of the horses and offers the possibility to test hypotheses about the presence of one or several horse populations. Our analysis determined that the assemblage of horse remains from Schöningen 13 II-4 resulted from multiple accumulation events, which took place at different periods of time.

Effects of late quaternary climate change on Palearctic shrews.

The Late Quaternary was a time of rapid climatic oscillations and drastic environmental changes. In general, species can respond to such changes by behavioral accommodation, distributional shifts, ecophenotypic modifications (nongenetic), evolution (genetic) or ultimately face local extinction. How those responses manifested in the past is essential for properly predicting future ones especially as the current warm phase is further intensified by rising levels of atmospheric carbon dioxide. Here, we use ancient DNA (aDNA) and morphological features in combination with ecological niche modeling (ENM) to investigate genetic and nongenetic responses of Central European Palearctic shrews to past climatic change. We show that a giant form of shrew, previously described as an extinct Pleistocene Sorex species, represents a large ecomorph of the common shrew (Sorex araneus), which was replaced by populations from a different gene-pool and with different morphology after the Pleistocene Holocene transition. We also report the presence of the cold-adapted tundra shrew (S. tundrensis) in Central Europe. This species is currently restricted to Siberia and was hitherto unknown as an element of the Pleistocene fauna of Europe. Finally, we show that there is no clear correlation between climatic oscillations within the last 50 000 years and body size in shrews and conclude that a special nonanalogous situation with regard to biodiversity and food supply in the Late Glacial may have caused the observed large body size.

Losing ground: past history and future fate of Arctic small mammals in a changing climate.

According to the IPCC, the global average temperature is likely to increase by 1.4-5.8 °C over the period from 1990 to 2100. In Polar regions, the magnitude of such climatic changes is even larger than in temperate and tropical biomes. This amplified response is particularly worrisome given that the so-far moderate warming is already impacting Arctic ecosystems. Predicting species responses to rapid warming in the near future can be informed by investigating past responses, as, like the rest of the planet, the Arctic experienced recurrent cycles of temperature increase and decrease (glacial-interglacial changes) in the past. In this study, we compare the response of two important prey species of the Arctic ecosystem, the collared lemming and the narrow-skulled vole, to Late Quaternary climate change. Using ancient DNA and Ecological Niche Modeling (ENM), we show that the two species, which occupy similar, but not identical ecological niches, show markedly different responses to climatic and environmental changes within broadly similar habitats. We empirically demonstrate, utilizing coalescent model-testing approaches, that collared lemming populations decreased substantially after the Last Glacial Maximum; a result consistent with distributional loss over the same period based on ENM results. Given this strong association, we projected the current niche onto future climate conditions based on IPCC 4.0 scenarios, and forecast accelerating loss of habitat along southern range boundaries with likely associated demographic consequences. Narrow-skulled vole distribution and demography, by contrast, was only moderately impacted by past climatic changes, but predicted future changes may begin to affect their current western range boundaries. Our work, founded on multiple lines of evidence suggests a future of rapidly geographically shifting Arctic small mammal prey communities, some of whom are on the edge of existence, and whose fate may have ramifications for the whole Arctic food web and ecosystem.