Research Article |
Corresponding author: Anastasia A. Taskaeva ( taskaeva@ib.komisc.ru ) Academic editor: Wanda M. Weiner
© 2019 Alla A. Kolesnikova, Maria A. Baturina, Dmitry M. Shadrin, Tatyana N. Konakova, Anastasia A. Taskaeva.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kolesnikova AA, Baturina MA, Shadrin DM, Konakova TN, Taskaeva AA (2019) New records of Lumbricidae and Collembola in anthropogenic soils of East European tundra. ZooKeys 885: 15-25. https://doi.org/10.3897/zookeys.885.37279
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The terrestrial environment of the East European tundra consists of a mosaic of habitat types. In addition to the natural habitat diversity, various human-influenced types may occur. In the town of Vorkuta, Komi Republic, Russia the manure-enriched soils near hydrogen sulfide springs were observed. This site represents an unusually nutrient-rich location with considerable development of organic soils, in contrast to the naturally forming soils in East European tundra which are typically thin and nutrient poor. In these organic soils, two species of Lumbricidae and two species of Collembola previously not recorded from the natural ecosystems in the study area of research territory were found. One earthworm species, Dendrodrilus rubidus tenuis, is likely to have been introduced. The presence of the three other species (Eiseniella tetraedra, Folsomia fimetaria, and Proisotoma minuta) is quite natural in East European tundra and such anthropogenic soils with high organic content may be a good habitat for them.
DNA barcoding, earthworms, springtails
Tundra ecosystems are characterized by a low number of species, together with low productivity (
The East European tundra is the territory bound by the Kanin Peninsula on the west and the Kara River Basin in the east between 67–71°N and 50–65°E. This territory is diverse, ranging from polar deserts with extremely low plant cover to moss, dwarf birch, willow, and forest tundra. The heterogeneity is also reflected in the soil animal fauna, where often clear relationships can be observed between vegetation cover and invertebrate species diversity (
The earthworm fauna in this territory is very poor and includes only three species: Dendrobaena octaedra (Savigny, 1826), Lumbricus rubellus Hoffmeister, 1843, and Eisenia nordenskioldi nordenskioldi (Eisen, 1879), which widely distributed in the study area because of their ability to withstand soil freezing (
On the other hand, springtails play an important role in tundra ecosystems as they affect the processes of humification and mineralization of organic matter (
The aim of this study was to assess the distribution of earthworms and springtails that are new in the Eastern European tundra, and test the working hypothesis that these records of these species are confined to anthropogenic soils near hydrogen sulfide sources beyond the Arctic Circle.
Soil samples were collected from the sides of a gully formed in the organic soils accumulated near hydrogen sulfide brooks (67°29'N, 64°02'E) in Vorkuta in Komi Republic, Russia (Fig.
Twenty soil samples 10 × 10 × 10 cm were taken near hydrogen sulfide springs in Vorkuta on July 2017 and August 2018. The soil samples were immediately returned to the Institute of Biology, Syktyvkar, Komi Republic, and placed in Tullgren soil extractors within 24 h of sampling. The soil fauna was extracted under 40 W light bulbs into 96 % alcohol for seven days until the soil was completely dry. Accounting of earthworms near hydrogen sulfide springs by manual sorting of soil samples 25 × 25 × 10 cm was not carried out because of the small area of the studied plots. Moreover, the recent results showed that the earthworm abundance estimated by the Tullgren funnel extraction method exceeds the values obtained through manual sorting of the samples by an order of magnitude (
DNA was extracted from several caudal segments using 6 % Chelex 100 DNA extraction kits (Sigma-Aldrich, USA). A fragment of the COI gene was amplified in 50 μl of mixture containing 10 μl ScreenMix (Eurogen, Russia), 10 μl of each primer (0.3 μM) (Eurogen, Russia), 18 μl ddH2O (Ambion, USA), and 2 μl DNA template (1÷100 ng). Two universal primers designed for invertebrate organisms were used to amplify the site of the COI fragment: LCO1490m (5’-TACTC-AACAA-ATCAC-AAAGA-TATTG-G-3’; modified from
Invertebrate species previously unrecorded in East European tundra collected from the anthropogenic soils near a hydrogen sulfide spring in Vorkuta.
Class | Species | Records in East European tundra | Records beyond Arctic Circle in Europe | Distribution | GenBank accession number |
---|---|---|---|---|---|
Oligochaeta | Dendrodrilus rubidus tenuis (Eisen 1874) | Vorkuta (67°29'N, 64°02'E) | Iceland? ( |
Holarctic. Records from the southern hemisphere | MH410150 |
Eiseniella tetraedra (Savigny, 1826) | Pechora delta (68°11'N, 53°82'E) Pymvashor (67°09'N, 60°51'E) Kharbey lakes (67°58'N, 62°34'E) Vorkuta (67°29'N, 64°02'E) | Iceland ( |
Cosmopolitan | MH410149 | |
Collembola | Folsomia fimetaria (Linnaeus, 1758) | Vorkuta (67°29'N, 64°02'E) | Greenland ( |
Holarctic | – |
Proisotoma minuta (Tullberg, 1871) | Vorkuta (67°29'N, 64°02'E) | Fennoscandia ( |
Cosmopolitan | – |
Two species of lumbricids, Dendrodrilus rubidus tenuis (Eisen, 1874) and Eiseniella tetraedra (Savigny, 1826), and two species of springtails, Folsomia fimetaria (Linnaeus, 1758) and Proisotoma minuta (Tullberg, 1871), not previously recorded from East European tundra were collected. Their records on this territory and beyond the Arctic Circle are shown at Table
Both species of Lumbricidae are widespread, including records from the southern hemisphere. Dendrodrilus rubidus is found on every continent except Antarctica and inhabits not only continents, but also many islands. It is often found in wet and moist soils by rivers, brooks, and springs, and thrives in compost heaps and in a variety of man-made habitats including rich soils close to settlements (
Phylogenetic tree constructed by the NJ method on the basis of a comparison of the nucleotide sequences of the COI gene of Dendrodrilus rubidus tenuis (A) and Eiseniella tetraedra (B) species from other regions (Austria JN869909, KT073959; USA KX651130; Canada KM612222, HM400424; Russia, Southern Kuriles KX400643; Finland FJ214209; France MF121728; Switzerland LN810249; Spain KY284185). * the numbers of our data sequences from Komi Republic.
Eiseniella tetraedra is a cosmopolitan earthworm widely distributed in the Old and New World countries (
Two species of Collembola previously unrecorded in East European tundra were found, Folsomia fimetaria and Proisotoma minuta. Both of these are typical members of a fauna associated with soils having a high organic content such as compost, garden soil, fucoid wrack beds along seashores, and stream banks. They are very seldom found in temperate forests in the European part of Russia. Due to their ecological preferences, they could be artificially introduced (
Three of the four new species records for East European tundra observed here appear to be not currently invasive. However, our molecular genetic analysis of the earthworm D. rubidus tenuis that was found in Vorkuta suggests that our sample of this species potentially invasive in nutrient-high habitats. In contrast to the natural soils, the anthropogenic soils provide a nutrient-rich, organic soil (contents of N = 1.3 % and C = 21 %) with excellent water-holding properties and with a cool moist environment during the summer but beneficially altered via human activities. The brook Vodny, in the area of which the studies were conducted, does not freeze as it depends on warm municipal and domestic waste waters flowing into it. Thus, soils with high organic content can stay warm throughout the season as a result of a continuous fermentation process. Consequently, species preferring warm soils probably do not suffer from chilling injuries (
This work was supported by the State Assignment AAAA-A17-117112850235-2, UrD RAS 18-4-4-37 and Russian Foundation for Basic Research and the government of the region of the Russian Federation, grant 18-44-110017. We are grateful to our colleagues who took part in the collection of material, Gleb Nakul and Alexey Kudrin.
Order | Family | Species |
---|---|---|
Poduromorpha | Onychiuridae | Protaphorura sp. |
Hypogastruridae | Ceratophysella denticulata (Bagnall, 1941) | |
Neanuridae | Friesea truncata Cassagnau, 1958 | |
Pseudachorutes subcrassus Tullberg, 1871 | ||
Entomobryomorpha | Isotomidae | Desoria blufusata (Fjellberg, 1978) |
Desoria breviseta Potapov, 2017 | ||
Desoria sp. | ||
Folsomia amplissima Potapov & Babenko, 2000 | ||
Folsomia fimetaria (Linnaeus, 1758) | ||
Folsomia sp. | ||
Isotoma anglicana Lubbock, 1873 | ||
Isotoma viridis Bourlet, 1839 | ||
Isotomiella minor (Schäffer, 1896) | ||
Parisotoma notabilis (Schäffer, 1896) | ||
Proisotoma minuta (Tullberg, 1871) | ||
Symphypleona | Sminthurididae | Sminthurides aquaticus (Bourlet, 1842) |
Sphaeridia pumilis (Krausbauer, 1898) | ||
Katiannidae | Sminthurinus aureus (Lubbock, 1862) |