Millennial processes of population decline, range contraction and near extinction of the European bison.

European bison (Bison bonasus) were widespread throughout Europe during the late Pleistocene. However, the contributions of environmental change and humans to their near extinction have never been resolved. Using process-explicit models, fossils and ancient DNA, we disentangle the combinations of threatening processes that drove population declines and regional extinctions of European bison through space and across time. We show that the population size of European bison declined abruptly at the termination of the Pleistocene in response to rapid environmental change, hunting by humans and their interaction. Human activities prevented populations of European bison from rebounding in the Holocene, despite improved environmental conditions. Hunting caused range loss in the north and east of its distribution, while land use change was responsible for losses in the west and south. Advances in hunting technologies from 1500 CE were needed to simulate low abundances observed in 1870 CE. While our findings show that humans were an important driver of the extinction of the European bison in the wild, vast areas of its range vanished during the Pleistocene-Holocene transition because of post-glacial environmental change. These areas of its former range have been climatically unsuitable for millennia and should not be considered in reintroduction efforts.

Widespread male sex bias in mammal fossil and museum collections.

A recent study of mammoth subfossil remains has demonstrated the potential of using relatively low-coverage high-throughput DNA sequencing to genetically sex specimens, revealing a strong male-biased sex ratio [P. Pecnerová et al., Curr. Biol. 27, 3505-3510.e3 (2017)]. Similar patterns were predicted for steppe bison, based on their analogous female herd-based structure. We genetically sexed subfossil remains of 186 Holarctic bison (Bison spp.), and also 91 brown bears (Ursus arctos), which are not female herd-based, and found that ∼75% of both groups were male, very close to the ratio observed in mammoths (72%). This large deviation from a 1:1 ratio was unexpected, but we found no evidence for sex differences with respect to DNA preservation, sample age, material type, or overall spatial distribution. We further examined ratios of male and female specimens from 4 large museum mammal collections and found a strong male bias, observable in almost all mammalian orders. We suggest that, in mammals at least, 1) wider male geographic ranges can lead to considerably increased chances of detection in fossil studies, and 2) sexual dimorphic behavior or appearance can facilitate a considerable sex bias in fossil and modern collections, on a previously unacknowledged scale. This finding has major implications for a wide range of studies of fossil and museum material.

Adapt or die-Response of large herbivores to environmental changes in Europe during the Holocene.

Climate warming and human landscape transformation during the Holocene resulted in environmental changes for wild animals. The last remnants of the European Pleistocene megafauna that survived into the Holocene were particularly vulnerable to changes in habitat. To track the response of habitat use and foraging of large herbivores to natural and anthropogenic changes in environmental conditions during the Holocene, we investigated carbon (δ13 C) and nitrogen (δ15 N) stable isotope composition in bone collagen of moose (Alces alces), European bison (Bison bonasus) and aurochs (Bos primigenius) in Central and Eastern Europe. We found strong variations in isotope compositions in the studied species throughout the Holocene and diverse responses to changing environmental conditions. All three species showed significant changes in their δ13 C values reflecting a shift of foraging habitats from more open in the Early and pre-Neolithic Holocene to more forest during the Neolithic and Late Holocene. This shift was strongest in European bison, suggesting higher plasticity, more limited in moose, and the least in aurochs. Significant increases of δ15 N values in European bison and moose are evidence of a diet change towards more grazing, but may also reflect increased nitrogen in soils following deglaciation and global temperature increases. Among the factors explaining the observed isotope variations were time (age of samples), longitude and elevation in European bison, and time, longitude and forest cover in aurochs. None of the analysed factors explained isotope variations in moose. Our results demonstrate the strong influence of natural (forest expansion) and anthropogenic (deforestation and human pressure) changes on the foraging ecology of large herbivores, with forests playing a major role as a refugial habitat since the Neolithic, particularly for European bison and aurochs. We propose that high flexibility in foraging strategy was the key for survival of large herbivores in the changing environmental conditions of the Holocene.

Movements of European bison (Bison bonasus) beyond the Bialowieza Forest (NE Poland): range expansion or partial migrations?

The European bison is the largest terrestrial mammal in Europe. After extinction in the wild at the beginning of the twentieth century, it was re-introduced to Bialowieza Forest and other woodlands in Eastern Europe. In this paper, we analysed the movements of European bison beyond the continuous woodlands of the Bialowieza Forest (NE Poland) between 1964 and 2010. In total, 1,117 direct observations of bison were collected. The number of males moving out of the forest fluctuated during the study period, whilst the number of females steadily increased. The number of male observations outside of the forest per annum was dependent on the population size and snow depth, whilst the number of cows in mixed groups moving outside of the forest was correlated with the population size only. Males were observed mainly alone (50 % of observations) or in small groups of two to three individuals (25 %); however, distribution of group size differed from those observed in the population. There was a significant difference between the direction of movement of males and females out of the forest-males moved mainly west and southwest, whilst females moved to the north. This was also significantly different from the expected movement direction. The mean distance of bison observations from the forest border was 1.8 ± 0.13 km and did not differ significantly between sexes. After 1990, males were observed significantly farther away from the forest (2.2 km) than in the previous years (0.9 km). Most observations (94 % of bulls and 93 % of cows) were up to 5 km from the forest edge. The range of bison in the vicinity of the Bialowieza Forest was strictly seasonal. Most observations (78 % in males and 88 % in females) were recorded from November to April. Increasing utilisation of areas beyond the forest habitats may be driven by different factors but most probably it is related to range expansion and the bison's preference for open habitats. The strong seasonal pattern of bison movements indicate that the partial seasonal migrations were initiated in the Bialowieza population.

Farm crops depredation by European bison (Bison bonasus) in the vicinity of forest habitats in northeastern Poland.

European bison, the largest mammal in Europe, after being exterminated in the wild and then restored during the 20th century is still listed by the International Union for Conservation of Nature (IUCN Red List of Threatened Species) as a species vulnerable to extinction. However, the increasing number of European bison, through creation of new and expansion of existing populations strongly increases the risk of human-bison conflict in the near future. We analyzed the depredation of farm crops by bison and the factors influencing the level of damage in the vicinity of two forest areas inhabited by bison in northeastern Poland. Between 2000 and 2010, the total cost of compensation was 196,200. The level of damage and amount of compensation was increasing from year to year in both forests and correlated with the number of bison. The majority of damage (57 % of cases) was recorded in winter (December-March). Snow depth and temperature did not influence the frequency of damage. The incidences of damage increased with decreasing distance from the woodland patches, therefore, 69 % of cases in Bialowieza Forest, and 80 % in Knyszyn Forest were recorded closer than 0.5 km from nearest woodland patch. The majority of the crops damaged by bison were cereals (61 %) but also hay (20 %) and rape (13 %). When compared to the availability of crops, bison strongly selected rape and rye in both regions. This study is the first addressing the increasing problem of human-bison conflict in re-introduced populations and analyzing long-term data on crop depredation. Such situations probably occur in the majority of growing and expanding bison populations, however, it has not yet to be monitored and is rather neglected in post-Soviet countries.

Large-scale mitogenomic analysis of the phylogeography of the Late Pleistocene cave bear.

The cave bear (Ursus spelaeus) is one of the Late Pleistocene megafauna species that faced extinction at the end of the last ice age. Although it is represented by one of the largest fossil records in Europe and has been subject to several interdisciplinary studies including palaeogenetic research, its fate remains highly controversial. Here, we used a combination of hybridisation capture and next generation sequencing to reconstruct 59 new complete cave bear mitochondrial genomes (mtDNA) from 14 sites in Western, Central and Eastern Europe. In a Bayesian phylogenetic analysis, we compared them to 64 published cave bear mtDNA sequences to reconstruct the population dynamics and phylogeography during the Late Pleistocene. We found five major mitochondrial DNA lineages resulting in a noticeably more complex biogeography of the European lineages during the last 50,000 years than previously assumed. Furthermore, our calculated effective female population sizes suggest a drastic cave bear population decline starting around 40,000 years ago at the onset of the Aurignacian, coinciding with the spread of anatomically modern humans in Europe. Thus, our study supports a potential significant human role in the general extinction and local extirpation of the European cave bear and illuminates the fate of this megafauna species.

Stable isotope signatures of large herbivore foraging habitats across Europe.

We investigated how do environmental and climatic factors, but also management, affect the carbon (δ13C) and nitrogen (δ15N) stable isotope composition in bone collagen of the two largest contemporary herbivores: European bison (Bison bonasus) and moose (Alces alces) across Europe. We also analysed how different scenarios of population recovery- reintroduction in bison and natural recovery in moose influenced feeding habitats and diet of these two species and compared isotopic signatures of modern populations of bison and moose (living in human-altered landscapes) with those occurring in early Holocene. We found that δ13C of modern bison and moose decreased with increasing forest cover. Decreasing forest cover, increasing mean annual temperature and feeding on farm crops caused an increase in δ15N in bison, while no factor significantly affected δ15N in moose. We showed significant differences in δ13C and δ15N among modern bison populations, in contrast to moose populations. Variation in both isotopes in bison resulted from inter-population differences, while in moose it was mainly an effect of intra-population variation. Almost all modern bison populations differed in δ13C and δ15N from early Holocene bison. Such differences were not observed in moose. It indicates refugee status of European bison. Our results yielded evidence that habitat structure, management and a different history of population recovery have a strong influence on foraging behaviour of large herbivores reflected in stable isotope signatures. Influence of forest structure on carbon isotope signatures of studied herbivores supports the "canopy effect" hypothesis.

Early cave art and ancient DNA record the origin of European bison.

The two living species of bison (European and American) are among the few terrestrial megafauna to have survived the late Pleistocene extinctions. Despite the extensive bovid fossil record in Eurasia, the evolutionary history of the European bison (or wisent, Bison bonasus) before the Holocene (<11.7 thousand years ago (kya)) remains a mystery. We use complete ancient mitochondrial genomes and genome-wide nuclear DNA surveys to reveal that the wisent is the product of hybridization between the extinct steppe bison (Bison priscus) and ancestors of modern cattle (aurochs, Bos primigenius) before 120 kya, and contains up to 10% aurochs genomic ancestry. Although undetected within the fossil record, ancestors of the wisent have alternated ecological dominance with steppe bison in association with major environmental shifts since at least 55 kya. Early cave artists recorded distinct morphological forms consistent with these replacement events, around the Last Glacial Maximum (LGM, ∼21-18 kya).

European bison as a refugee species? Evidence from isotopic data on Early Holocene bison and other large herbivores in northern Europe.

According to the refugee species concept, increasing replacement of open steppe by forest cover after the last glacial period and human pressure had together forced European bison (Bison bonasus)--the largest extant terrestrial mammal of Europe--into forests as a refuge habitat. The consequent decreased fitness and population density led to the gradual extinction of the species. Understanding the pre-refugee ecology of the species may help its conservation management and ensure its long time survival. In view of this, we investigated the abundance of stable isotopes (δ13C and δ15N) in radiocarbon dated skeletal remains of European bison and other large herbivores--aurochs (Bos primigenius), moose (Alces alces), and reindeer (Rangifer tarandus)--from the Early Holocene of northern Europe to reconstruct their dietary habits and pattern of habitat use in conditions of low human influence. Carbon and nitrogen isotopic compositions in collagen of the ungulate species in northern central Europe during the Early Holocene showed significant differences in the habitat use and the diet of these herbivores. The values of the δ13C and δ15N isotopes reflected the use of open habitats by bison, with their diet intermediate between that of aurochs (grazer) and of moose (browser). Our results show that, despite the partial overlap in carbon and nitrogen isotopic values of some species, Early Holocene large ungulates avoided competition by selection of different habitats or different food sources within similar environments. Although Early Holocene bison and Late Pleistocene steppe bison utilized open habitats, their diets were significantly different, as reflected by their δ15N values. Additional isotopic analyses show that modern populations of European bison utilize much more forested habitats than Early Holocene bison, which supports the refugee status of the species.