Heavy reliance on plants for Romanian cave bears evidenced by amino acid nitrogen isotope analysis

Abstract

Heavy reliance on plants is rare in carnivora and mostly limited to relatively small species in subtropical settings. The feeding behaviors of extinct cave bears living during Pleistocene cold periods at middle latitudes have been intensely studied using various approaches including isotopic analyses of fossil collagen. In contrast to cave bears from all other regions in Europe, some individuals from Romania show exceptionally high δ 15 n values that might be indicative of meat consumption. Herbivory on plants with high δ 15 N values cannot be ruled out based on this method, however. Here we apply an approach using the δ 15 N values of individual amino acids from collagen that offsets the baseline δ 15 n variation among environments. the analysis yielded strong signals of reliance on plants for Romanian cave bears based on the δ 15 n values of glutamate and phenylalanine. these results could suggest that the high variability in bulk collagen δ 15 N values observed among cave bears in Romania reflects niche partitioning but in a general trophic context of herbivory. Bears represent the largest terrestrial members within the Carnivora alive today and the vast majority of them have carnivorous or omnivorous feeding habits. Until around 25,000 years ago, the coldest period in the Pleistocene, additional, now extinct bear species were living 1-4 , among which the so-called cave bears, a very large type of bear that formed the sister lineage of extant brown bears and polar bears (e.g., ref. 5). The paradox of the cave bear is that their diet has been said to be herbivorous despite their large body sizes while extant herbivorous Carnivora species are smaller 6,7. After their divergence from the brown bear lineage 1.2-1.6 million years ago, cave bear populations showed substantial morphological and genetic variability and multiple forms have been recognized 8 , although their taxonomic status and the relationships among them continue to be debated 9. The possible causes of the extinction of these bears are also intensively debated, involving climate change, human impacts, and (lack of) flexibility in feeding behavior 10-15. Understanding cave bear feeding behavior is therefore important as it might give insights into the extinction of this species, and also it could be relevant for the conservation of extant, herbivorous carnivoran species that are under threat of extinction (e.g., binturong, red panda, giant panda 16,17). More recent studies have shown mixed results based on different lines of evidence including anatomical properties like craniodental morphologies, tooth wear analyses, mortality patterns (e.g., sex ratio), etc. wherein the conclusions were highly context dependent and differed by sample-sets 18-23. This is also the case for stable carbon and nitrogen isotope analyses (δ 13 C and δ 15 N) on collagen extracted from bone/teeth 24-31. Relatively low δ 15 N values of most of these bears so far indicate their highly-plant-dependent feeding habits with possible exceptions for some groups in today's Romania tha...

Ancient Faunal History Revealed by Interdisciplinary Biomolecular Approaches

“…From a biomolecular perspective, traditional isotopic methods based on δ 15 N and δ 13 C from bulk protein (collagen), and more recently δ 15 N analyses of individual amino acids, were used to reconstruct the cave bear's dietary preferences. These studies essentially support a herbivorous diet across its range [41][42][43][44][45]. Palaeogenomic studies have revealed a complex evolutionary history within the cave bear species complex with three major groups: the Caucasian group including praekudarensis and kudarensis taxa; the European group including spelaeus, ingressus, eremus, and kanivetz from the Ural Mountains; and the Ural-specific group made up by rossicus [40].…”

“…Few studies thus far have combined isotopes and aDNA to shed light on cave bear's ecology, evolutionary history, and extinction [45,49,60,61] (Figure 3).…”

Ancestors of domestic cats in Neolithic Central Europe: Isotopic evidence of a synanthropic diet

“…This is, however, true in the case of a single food web. In more complex ecosystems, the particular food webs which rely on different resources may exhibit different isotopic signatures of equivalent trophic levels ( 63 ). Our result is in line with the isotopic relationships observed in modern ecosystems that include agricultural biotopes ( 4 ).…”

Biogeographic problem-solving reveals the Late Pleistocene translocation of a short-faced bear to the California Channel Islands

“…Collagen stable isotopes from Beringia 18 (δ 13 C − 18.27 ± 0.4‰, δ 15 N 8.5 ± 1.02‰) and British Columbia 34 (δ 13 C − 18.9‰, δ 15 N 10.6‰) are suggestive of a high trophic position with terrestrial meat consumption, especially caribou 20 . However, definitive calculation of trophic position, particularly in the case of omnivorous mammals that readily consume meat and plant material, must rely on future analyses of compound specific stable isotopes of individual amino acids and larger sample sizes 47 , 48 . Brown bears, U. arctos , tend to consume more animal protein at northern latitudes 49 , and coastal populations in Alaska today exhibit stable isotope values with more positive carbon values than that of the CCI A. simus , reflecting more marine protein consumption (δ 13 C − 15.46 ± 2.04‰, δ 15 N 10.79 ± 4.15‰; Suess corrected 18 ).…”