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

Abstract

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.

Fig 1. Locations of analyzed Early Holocene bone remains of Bison bonasus, Bos primigenius, Alces alces and Rangifer tarandus in northern Europe.

Numbers in brackets indicate the number of individuals from the same location. The data used to generate the figure can be found in Table 1 and S1 Table.

Fig 2. Stable δ¹³C_coll and δ¹⁵N_coll isotope values for moose (Alces alces), aurochs (Bos primigenius) and European bison (Bison bonasus) in Early Holocene in northern Europe.

Shaded area denotes range of carbon isotope values characteristic for forest use. Ellipses are plotted in a way to include the extreme points of the range of measured isotopic values and to improve readability of the figure. The data used to generate the figure can be found in Table 1 and S1 Table.

Fig 3. Box plots of stable δ¹³C_coll and δ¹⁵N_coll isotope values measured for Early Holocene moose, aurochs, European bison and reindeer.

(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles while, the whiskers show the range of the data. The data used to generate the figure can be found in Table 1 and S1 Table.

Fig 4. Comparison of δ¹³C_coll and δ¹⁵N_coll values between European bison and aurochs in Early Holocene and Pleistocene steppe bison and aurochs (Belgium and Southwestern France).

(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles, while the whiskers show the range of the data. The data used to generate the figure can be found in Table 1, S1 and S2 Tables.

Fig 5. Box plots of stable δ¹³C_coll values for Early Holocene Bison bonasus, compared to modern populations of European (Bison bonasus) and American bison (Bison bison bison) living in forest habitats.

(* denote statistically significant differences for p between 0.05 and 0.01, **—for p < 0.01). Boxes show the median, upper and lower quartiles, while the whiskers show the range of the data. The data used to generate the figure can be found in Table 1 and S3 Table.