Dental microwear foraging ecology of a large browsing ruminant in Northern Hemisphere: The European moose (Alces alces)

International audienceYears of studies have already highlighted the complex combination, in moose feeding ecology, of a marked selectivity coupled with a significant dietary adaptability toward changes in the local resource availability. Dental textures resulting from masticatory movements and the properties of ingested food items constitute a link between the animal, its ecology and the environment it occupies. This approach is efficient to decipher subtle variations in diet, at the interspecific but also intra-populational scales. In this study, we explore inter and intra population dietary variations among six Northern European moose populations using DMTA. We show that moose feeding ecology spans a continuum between a diet dominated by tender leaves and a diet consisting of lignified tissues. The structure of habitats is the main driver of these dietary differences between populations. The absence of significant variation between males and females or between seasons is interpreted as a reflection of the food selectivity of this deer on a finer scale. The moose has a long common history with humans, constituting at certain times and in certain places the main food resource of these populations, adapting in other contexts and at other times to the repercussions of increasing anthropization and global climate change. We aim here at characterizing the dental microwear texture diversity hidden within the “browsing” dietary category. This work is also intended to be used as a reference for future paleontological or archeological investigations. We believe that it will contribute to a better understanding of the(paleo)ecology of the species and of the variations in its feeding ecology through time

Foraging habitats and niche partitioning of European large herbivores during the Holocene – Insights from 3D dental microwear texture analysis

International audienceEnvironmental changes related to forest expansion and later to agricultural development and deforestation during the Holocene in Europe have strongly shaped herbivore distribution and habitat selection, leading to species extinction. In this paper, we examine, through dental microwear textural analysis, the foraging habitats, dietary flexibility and niche partitioning of large herbivores (100 to 1000 kg) including two bovids (European bison Bison bonasus and aurochs Bos primigenius) and two cervids (moose Alces alces and red deer Cervus elaphus). The study focuses on northeast (NE) and south central (SC) Europe during three periods of the Holocene: Neolithic (6500–3500 cal yrs BP), Roman Period and Middle Ages (~2000–450 cal yrs BP) and Recent times (1963–2014). Our study highlights differences in diet between species only in the Neolithic SC Europe. This may have resulted from diversified habitats and dietary niche separation in SC Europe. The absence of differences in NE Europe may suggest more homogeneous habitat conditions in combination with lower densities of large herbivores in forested habitats. Analysis shows that during the Neolithic, in the bison diet there was more herbaceous monocotyledons in SC Europe than in NE Europe. We also found temporal changes in microwear texture variables for the bison in SC Europe suggesting a more herbaceous diet in the Neolithic than during the Roman Period and Middle Ages. However, neither spatial nor temporal differences in microwear texture variables were found in the aurochs. Thus, the diet of the European bison has likely changed, which may indicate a greater plasticity that promoted survival in refuge habitats

European Bison as a Refugee Species? Evidence from Isotopic Data on Early Holocene Bison and Other Large Herbivores in Northern Europe

<div><p>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 (<i>Bison bonasus</i>)—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 (<i>Bos primigenius</i>), moose (<i>Alces alces</i>), and reindeer (<i>Rangifer tarandus</i>)—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.</p></div

Stable isotope signatures of large herbivore foraging habitats across Europe

<div><p>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 (<i>Bison bonasus</i>) and moose (<i>Alces alces</i>) 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.</p></div

Pairwise differences for δ¹³C carbon and δ¹⁵N nitrogen isotope values between species in Early Holocene and Pleistocene and between samples of modern <i>Bison bonasus</i> (Poland) and <i>Bison bison</i> (Prince Albert National Park, Canada) as well as between modern and Early Holocene Bison.

<p>Insignificance at p > 0.05 is indicated in normal font for Mann-Whitney—Wilcoxon test. Bold indicates significant differences. Abbreviations: N = number of specimens.</p><p>Pairwise differences for δ¹³C carbon and δ¹⁵N nitrogen isotope values between species in Early Holocene and Pleistocene and between samples of modern <i>Bison bonasus</i> (Poland) and <i>Bison bison</i> (Prince Albert National Park, Canada) as well as between modern and Early Holocene Bison.</p

Multiple regression model selection (based on the AICc criteria) to investigate the effect of different factors (see Materials and methods) on carbon (δ¹³C_cor) and nitrogen (δ¹⁵N) stable isotope compositions in bone collagen of European bison and moose from different European populations.

<p>Multiple regression model selection (based on the AICc criteria) to investigate the effect of different factors (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0190723#sec002" target="_blank">Materials and methods</a>) on carbon (δ¹³C_cor) and nitrogen (δ¹⁵N) stable isotope compositions in bone collagen of European bison and moose from different European populations.</p

One-way ANOVA for δ¹³C_cor and δ¹⁵N for six European bison <i>Bison bonasus</i> and four moose <i>Alces alces</i> populations.

<p>One-way ANOVA for δ¹³C_cor and δ¹⁵N for six European bison <i>Bison bonasus</i> and four moose <i>Alces alces</i> populations.</p

Locations of analyzed Early Holocene bone remains of <i>Bison bonasus</i>, <i>Bos primigenius</i>, <i>Alces alces</i> and <i>Rangifer tarandus</i> in northern Europe.

<p>Numbers in brackets indicate the number of individuals from the same location. The data used to generate the figure can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.t001" target="_blank">Table 1</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0115090#pone.0115090.s001" target="_blank">S1 Table</a>.</p

Influence of forest cover on carbon isotope compositions δ¹³C_cor in populations of (a) European bison and (b) moose.

<p>Influence of forest cover on carbon isotope compositions δ¹³C_cor in populations of (a) European bison and (b) moose.</p

Influence of (a) forest cover, (b) presence of crop damage and (c) annual temperature on nitrogen δ¹⁵N isotope compositions in European bison based on estimates from multiple regression model.

<p>Influence of (a) forest cover, (b) presence of crop damage and (c) annual temperature on nitrogen δ¹⁵N isotope compositions in European bison based on estimates from multiple regression model.</p