Integrative approach reveals new species of water bears (Pilatobius, Grevenius, and Acutuncus) from Arctic cryoconite holes, with the discovery of hidden lineages of Hypsibius

A crucial step in understanding glacial ecosystems is to elucidate their biodiversity. Although tardigrades (water bears) are one of the most common and abundant metazoans inhabiting glaciers, knowledge of their taxonomic diversity on these ice masses remains scarce. The fragmentary data about the diversity of metazoans in glacial ecosystems is a warning sign in the era of global warming that seriously threatens cold-adapted specialists. Based on morphological, morphometric and DNA analyses (18S rRNA, 28S rRNA, COI), we identified tardigrade taxa from water -filled reservoirs in the glacier surface (cryoconite holes) in the Arctic (Svalbard and Greenland). Here we describe three species new to science: Pilatobius glacialis sp. nov., Acutuncus mariae sp. nov. and Grevenius cryophilus sp. nov. In addition to their morphological and genetic differences, these species are easily distinguished from their close relatives by their thermally stable niche, cryoconite holes, in which water temperature at the bottom oscillates around 0.1 degrees C during the polar summer. Moreover, we found the genus Acutuncus, considered a pan-Antarctic taxon, in cryoconite holes on Svalbard. Additionally, we discovered three new species of the Hypsibius dujardini complex by DNA analysis. Their delimitation is currently based on genetic differences and further morphometric studies may aid in distinguishing them. Our study revealed a new view on the biogeography of glacier tardigrades and the genus Acutuncus, as well as emphasized the uniqueness of glacier metazoans. Tardigrade species inhabiting cryoconite holes may be either morphologically the same (P. glacialis sp. nov.), or very similar to species inhabiting other ecosystems (H. dujardini complex), but they differ in DNA. On other hands, others are unique in both morphology and DNA (G. cryophilus sp. nov.) indicating that the properties of specific habitats shape speciation and, as in cryoconite holes, the reason might be their thermal regime. Therefore, we suggest using the ecological background as well as habitat characteristics in taxonomic descriptions and the differential diagnosis of new tardigrade species. (c) 2020 Elsevier GmbH. All rights reserved.