Abstract
We built a map of the distribution of earthworm abundance in coniferous forests in the area affected by long-term emissions from the Middle Ural Copper Smelter. It is established that a “lumbricide desert” of about 65 km2 without earthworms in the forest litter and soil mineral horizons has been formed near the smelter due to extremely high concentrations of heavy metals. However, we have also found that earthworms (only Dendrodrilus rubidus tenuis) inhabit logs of the late stages of decomposition in this area. Their abundance is comparable to that in the soil of unpolluted (background) areas; single individuals (including cocoons) were also found in the soil directly under the logs. Gastropods, which are absent in standard soil samples in this area, were also recorded in these logs (five species). We suppose that the presence of such “survival microsites” may serve as a mechanism of recolonization of polluted areas by groups sensitive to pollution after the reduction of emissions, followed by a decrease in soil toxicity.
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REFERENCES
Arnold, R.E., Hodson, M.E., and Langdon, C.J., A Cu tolerant population of the earthworm Dendrodrilus rubidus (Savigny, 1862) at Coniston Copper Mines, Cumbria, UK, Environ. Pollut., 2008, vol. 152, no. 3, pp. 713–722.
Bel’skaya, E.A. and Zolotarev, M.P., Changes in the size structure of carabid communities in forest ecosystems under technogenic transformation, Russ. J. Ecol., 2017, vol. 48, no. 2, pp. 152–160.
Bengtsson, G., Nordstrom, S., and Rundgren, S., Population density and tissue metal concentration of lumbricids in forest soils near a brass mill, Environ. Pollut. Ser. A, 1983, vol. 30, no. 2, pp. 87–108.
Bengtsson, J., Disturbance and resilience in soil animal communities, Eur. J. Soil Biol., 2002, vol. 38, no. 2, pp. 119–125.
Bergman, I.E. and Vorobeichik, E.L., The effect of copper smelter emissions on the stock and decomposition of coarse woody debris in spruce and fir woodlands, Lesovedenie, 2017, no. 1, pp. 24–38.
Dudka, S. and Adriano, D.C., Environmental impacts of metal ore mining and processing: a review, J. Environ. Quality, 1997, vol. 26, no. 3, pp. 590–602.
Eijsackers, H., Earthworms as colonizers of natural and cultivated soil environments, Appl. Soil. Ecol., 2011, vol. 50, no. 1, pp. 1–13.
Ermakov, A.I., Structural changes in the carabid fauna of forest ecosystems under a toxic impact, Russ. J. Ecol., 2004, vol. 35, no. 6, pp. 403–408.
Esenin, A.V. and Ma, W.C., Heavy metals (Cd, Cu, Zn) in wood and wood-feeding insects and other invertebrates associated with decaying pine trees, Bull. Environ. Contam. Toxicol., 2000, vol. 64, no. 2, pp. 242–249.
Geras’kina, A.P., The population of earthworms (Lumbricidae) in the main types of coniferous forests of the Pechora–Ilych Nature Reserve, Zool. Zh., 2016, vol. 95, no. 4, pp. 394–405.
Goncharov, A.A., Khramova, E.Yu., and Aleinikov, A.A., The role of micromosaic organization of forest ecosystems in the formation of the structure of soil macrofauna as exemplified by the fir–spruce tall-herb forest in the Pechora River headwaters, in Trudy Pechoro-Ilychskogo zapovednika (Proceedings of the Pechora–Ilych Nature Reserve), Syktyvkar: Komi Nauchn. Tsentr Ural. Otd. Ross. Akad. Nauk, 2015, pp. 62–68.
Gongalsky, K.B., Lesnye pozhary i pochvennaya fauna (Forest Fires and Soil Fauna), Moscow: KMK, 2014.
Gongalsky, K.B., Belorustseva, S.A., Kuznetsova, D.M., Matyukhin, A.V., Pelgunova, L.A., Savin, F.A., and Shapovalov, A.S., Spatial avoidance of patches of polluted chernozem soils by soil invertebrates, Insect Sci., 2009, vol. 16, no. 1, pp. 99–105.
Hanski, I., Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes, Oikos, 1999, vol. 87, no. 2, pp. 209–219.
Harmon, M.E., Franklin, J.F., Swanson, F.J., Sollins, P., Gregory, S.V., Lattin, J.D., Anderson, N.H., Cline, S.P., Aumen, N.G., Sedell, J.R., Lienkaemper, G.W., Cromack, K., Jr., and Cummins, K.W., Ecology of coarse woody debris in temperate ecosystems, Adv. Ecol. Res., 1986, vol. 15, pp. 133–302.
Kaigorodova, S.Yu. and Vorobeichik, E.L., Changes in certain properties of grey forest soil polluted with emissions from a copper-smelting plant, Russ. J. Ecol., 1996, vol. 27, no. 3, pp. 177–183.
Kim, S.W., Kim, D., Moon, J., Chae, Y., Kwak, J.I., Park, Y., Jeong, S.W., and An, Y.J., Earthworm dispersal assay for rapidly evaluating soil quality, Environ. Toxicol. Chem., 2017, vol. 36, no. 10, pp. 2766–2772.
Koptsik, G.N., Lukina, N.V., Koptsik, S.V., Shcherbenko, T.A., and Livantsova, S.Yu., The absorption of macronutrients and heavy metals by spruce under atmospheric pollution on the Kola Peninsula, Lesovedenie, 2008, no. 2, pp. 3–12.
Korkina, I.N. and Vorobeichik, E.L., The humus index: a promising tool for environmental monitoring, Russ. J. Ecol., 2016, vol. 47, no. 6, pp. 526–531.
Korkina, I.N. and Vorobeichik, E.L., Humus index as an indicator of the topsoil response to the impacts of industrial pollution, Appl. Soil. Ecol., 2018, vol. 123, pp. 455–463.
Kozlov, M.V. and Zvereva, E.L., Industrial barrens: extreme habitats created by non-ferrous metallurgy, Rev. Environ. Sci. Biotechnol., 2007, vol. 6, nos. 1–3, pp. 231–259.
Kramarenko, S.S., Active and passive migration of terrestrial snails: a review, Ruthenica, 2014, vol. 24, no. 1, pp. 1–14.
Laakso, J. and Setälä, H., Nest mounds of red wood ants (Formica aquilonia): hot spots for litter-dwelling earthworms, Oecologia, 1997, vol. 111, no. 4, pp. 565–569.
Langdon, C.J., Piearce, T.G., Feldmann, J., Semple, K.T., and Meharg, A.A., Arsenic speciation in the earthworms Lumbricus rubellus and Dendrodrilus rubidus,Environ. Toxicol. Chem., 2003, vol. 22, no. 6, pp. 1302–1308.
Lebedeva, N.V. and Krivolutsky, D.A., Birds spread soil microarthropods to Arctic islands, Dokl. Biol. Sci., 2003, vol. 391, no. 1, pp. 329–332.
Lukkari, T. and Haimi, J., Avoidance of Cu- and Zn-contaminated soil by three ecologically different earthworm species, Ecotoxicol. Environ. Saf., 2005, vol. 62, no. 1, pp. 35–41.
Matyukhin, A.B., Ectoparasites of birds under megacity conditions, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Parazitol. Ross. Akad. Nauk, 2004.
McFee, W.W. and Stone, E.L., The persistence of decaying wood in the humus layers of northern forests, Soil Sci. Soc. Am. J., 1966, vol. 30, no. 4, pp. 513–516.
Mikhailova, I.N., Initial stages of recovery of epiphytic lichen communities after reduction of emissions from a copper smelter, Russ. J. Ecol., 2017, vol. 48, no. 4, pp. 335–339.
Mikryukov, V.S. and Dulya, O.V., Contamination-induced transformation of bacterial and fungal communities in spruce–fir and birch forest litter, Appl. Soil. Ecol., 2017, vol. 114, pp. 111–122.
Mikryukov, V.S., Dulya, O.V., and Vorobeichik, E.L., Diversity and spatial structure of soil fungi and arbuscular mycorrhizal fungi in forest litter contaminated with copper smelter emissions, Water Air Soil Pollut., 2015, vol. 226, no. 4, art. 114, pp. 1–14.
Mukhacheva, S.V., Davydova, Yu.A., and Vorobeichik, E.L., The role of heterogeneity of the environment in preservation of the diversity of small mammals under the conditions of strong industrial pollution, Dokl. Biol. Sci., 2012, vol. 447, no. 1, pp. 338–341.
Nesterkov, A.V., Reaction of mollusk population to emissions from the Middle Ural copper smelter, Contemp. Probl. Ecol., 2013, vol. 6, no. 6, pp. 667–674.
Pacyna, J.M., Pacyna, E.G., and Aas, W., Changes of emissions and atmospheric deposition of mercury, lead, and cadmium, Atmos. Environ., 2009, vol. 43, no. 1, pp. 117–127.
Płytycz, B., Kielbasa, E., Grebosz, A., Duchnowski, M., and Morgan, A.J., Riboflavin mobilization from eleocyte stores in the earthworm Dendrodrilus rubidus inhabiting aerially-contaminated Ni smelter soil, Chemosphere, 2010, vol. 81, no. 2, pp. 199–205.
Rull, V., Microrefugia, J. Biogeogr., 2009, vol. 36, no. 3, pp. 481–484.
Spurgeon, D.J. and Hopkin, S.P., The effects of metal contamination on earthworm populations around a smelting works: quantifying species effects, Appl. Soil. Ecol., 1996, vol. 4, no. 2, pp. 147–160.
Terhivuo, J., Pankakoski, E., Hyvarinen, H., and Koivisto, I., Pb uptake by ecologically dissimilar earthworm (Lumbricidae) species near a lead smelter in south Finland, Environ. Pollut., 1994, vol. 85, no. 1, pp. 87–96.
Trubina, M.R. and Vorobeichik, E.L., Severe industrial pollution increases the β-diversity of plant communities, Dokl. Biol. Sci., 2012, vol. 442, no. 1, pp. 17–19.
Vorobeichik, E.L., Populations of earthworms (Lumbricidae) in forests of the Middle Urals in conditions of pollution by discharge from copper works, Russ. J. Ecol., 1998, vol. 29, no. 2, pp. 85–91.
Vorobeichik, E.L., Seasonal changes in the spatial distribution of cellulolytic activity of soil microflora under conditions of atmospheric pollution, Russ. J. Ecol., 2007, vol. 38, no. 6, pp. 398–407.
Vorobeichik, E.L. and Kaigorodova, S.Yu., Long-term dynamics of heavy metals in the upper horizons of soils in the region of a copper smelter impacts during the period of reduced emission, Eurasian Soil Sci., 2017, vol. 50, no. 8, pp. 977–990.
Vorobeichik, E.L. and Nesterkova, D.V., Technogenic boundary of the mole distribution in the region of copper smelter impacts: shift after reduction of emissions, Russ. J. Ecol., 2015, vol. 46, no. 4, pp. 377–380.
Vorobeichik, E.L. and Pishchulin, P.G., Industrial pollution reduces the effect of trees on forming the patterns of heavy metal concentration fields in forest litter, Russ. J. Ecol., 2016, vol. 47, no. 5, pp. 431–441.
Vorobeichik, E.L., Ermakov, A.I., Zolotarev, M.P., and Tuneva, T.K., Changes in the diversity of soil macrofauna in industrial pollution gradient, Russ. Entomol. J., 2012, vol. 21, no. 2, pp. 203–218.
Vorobeichik, E.L., Trubina, M.R., Khantemirova, E.V., and Bergman, I.E., Long-term dynamic of forest vegetation after reduction of copper smelter emissions, Russ. J. Ecol., 2014, vol. 45, no. 6, pp. 498–507.
Vorobeichik, E.L., Ermakov, A.I., and Grebennikov, M.E., Initial stages of recovery of soil macrofauna communities after reduction of emissions from a copper smelter, Russ. J. Ecol., 2019, vol. 50, no. 2, pp. 146–160.
ACKNOWLEDGMENTS
We are grateful to A.V. Nesterkov for assistance in field studies, as well as to E.V. Golovanova for earthworms identifying and V.S. Mikryukov, O.V. Dulya, M.R. Trubina, and K.B. Gongalskii for discussion and comments on the text of the manuscript.
Funding
The material was collected as part of the state assignment of the Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences; the data analysis and manuscript preparation were supported by the Russian Foundation for Basic Research, project no. 18-04-00160.
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Vorobeichik, E.L., Ermakov, A.I., Nesterkova, D.V. et al. Coarse Woody Debris as Microhabitats of Soil Macrofauna in Polluted Areas. Biol Bull Russ Acad Sci 47, 87–96 (2020). https://doi.org/10.1134/S1062359020010173
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DOI: https://doi.org/10.1134/S1062359020010173