The Role of Coarse Woody Debris in the Survival of Soil Macrofauna in Metal-Contaminated Areas in the Middle Urals
- Autores: Vorobeychik E.L.1, Ermakov A.I.1, Grebennikov M.E.1, Nesterkova D.V.1, Zolotarev M.P.1, Sozontov A.N.1
-
Afiliações:
- Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
- Edição: Nº 4 (2024)
- Páginas: 297-320
- Seção: RESEARCH
- URL: https://modernonco.orscience.ru/0024-1148/article/view/681199
- DOI: https://doi.org/10.31857/S0024114824040019
- EDN: https://elibrary.ru/PDSMVN
- ID: 681199
Citar
Resumo
Soil macrofauna of three microstations was compared between background and contaminated areas: within decaying trunks of deciduous trees (linden, aspen) in the final stages of decomposition, beneath the trunks and outside the influence of the trunks (standard soil samples). The composition of macrofauna was analysed at two levels: (i) supraspecific taxa and (ii) species for several taxocenes (earthworms, centipedes, arachnids, ground beetles, click beetles, and mollusks). The study was conducted in the spruce-fir forests of the southern taiga, in the area affected by emissions from the Middle Ural Copper Smelter. At the level of supraspecific taxa, the composition of macrofauna differs little between decaying trunks and standard soil samples. At the species level, the difference between microsites depends on the specific taxocene: the species composition within decaying trunks either almost coincides with that of standard samples (mollusks), or is more specialized (click beetles), or is more diverse (centipedes, arachnids, ground beetles), or is reduced due to the loss of a specific ecological group (earthworms). The ordination of microsites based on the general list of species for the investigated taxocenes aligns with the ordination based on the composition of macrofauna at the supraspecific level. The total density and abundance of most groups of soil macrofauna are higher in trunks than in standard samples. In the background area, the difference is especially pronounced (2—6 times) for earthworms, harvestmen, lithobiids, herbivorous heteroptera, ground beetles, and chironomid larvae. In contaminated areas, the difference is even more substantial: for earthworms it is 70 times, for mollusks — 30 times, for heteroptera — 10 times, for lepidopteran larvae — 7 times, for spiders — 5 times, for diplopods — 4 times. The predominant habitation of soil macrofauna in decaying trunks within contaminated area may be associated with a significantly lower concentrations of potentially toxic metals in decomposing wood compared to forest litter: for Pb, the difference is 85 times, for Fe — 77 times, for Cu — 25 times, for Cd — 2.6 times, for Zn — 1.7 times. Thus, the negative impacts of pollution on soil macrofauna are less pronounced in decaying tree trunks than in standard soil samples.
Palavras-chave
Texto integral

Sobre autores
E. Vorobeychik
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Autor responsável pela correspondência
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
A. Ermakov
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
M. Grebennikov
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
D. Nesterkova
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
M. Zolotarev
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
A. Sozontov
Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences
Email: ev@ipae.uran.ru
Rússia, 8 Mart St., 202, Yekaterinburg, 620144
Bibliografia
- Arnold R. E., Hodson M. E., Langdon C. J., A Cu tolerant population of the earthworm Dendrodrilus rubidus (Savigny, 1862) at Coniston Copper Mines, Cumbria, UK, Environmental Pollution, 2008, Vol. 152, No. 3, pp. 713—722. https://doi.org/10.1016/j.envpol.2007.06.048
- Ashwood F., Vanguelova E. I., Benham S., Butt K. R., Developing a systematic sampling method for earthworms in and around deadwood, Forest Ecosystems, 2019, Vol. 6: 33. https://doi.org/10.1186/s40663-019-0193-z
- Bel’skii E.A., Lyakhov A. G., Dynamics of the community of hole-nesting birds upon reduction of industrial emissions (the example of the Middle Ural Copper Smelter) Russian Journal of Ecology, 2021, Vol. 52, No. 4, pp. 296—306. https://doi.org/10.1134/S1067413621040044
- Belskaya E. A., Dynamics of trophic activity of leaf-eating insects on birch during reduction of emissions from the Middle Ural Copper Smelter, Russian Journal of Ecology, 2018, Vol. 49, No. 1, pp. 87—92. https://doi.org/10.1134/s1067413617060029
- Belskii E., Lyakhov A., Improved breeding parameters in the pied flycatcher with reduced pollutant emissions from a copper smelter, Environmental Pollution, 2022, Vol. 302(1): 119089. https://doi.org/10.1016/j.envpol.2022.119089
- Bengtsson G., Tranvik L., Critical metal concentrations for forest soil invertebrates. A review of the limitations, Water, Air, Soil Pollut, 1989, Vol. 47, No. 3-4, pp. 381—417.
- Berg M. P., Bengtsson J., Temporal and spatial variability in soil food web structure, Oikos, 2007, Vol. 116, No. 11, pp. 1789—1804.
- Bergman I. E., Vorobeichik E. L., The effect of a copper smelter emissions on the stock and decomposition of coarse woody debris in spruce and fir woodlands, Contemporary Problems of Ecology, 2017, Vol. 10, No. 7, pp. 790—803. https://doi.org/10.1134/S1995425517070022
- Chao A., Gotelli N. J., Hsieh T. C., Sander E. L., Ma K. H., Colwell R. K., Ellison A. M., Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies, Ecological Monographs, 2014, Vol. 84, No. 1, pp. 45—67. https://doi.org/https://doi.org/10.1890/13-0133.1
- Dulya O. V., Bergman I. E., Kukarskih V. V., Vorobeichik E. L., Smirnov G. Y., Mikryukov V. S., Pollution-induced slowdown of coarse woody debris decomposition differs between two coniferous tree species, Forest Ecology and Management, 2019, Vol. 448, pp. 312—320. https://doi.org/10.1016/j.foreco.2019.06.026
- Esenin A. V., Ma W. C., Heavy metals (Cd, Cu, Zn) in wood and wood-feeding insects and other invertebrates associated with decaying pine trees, Bulletin of Environmental Contamination and Toxicology, 2000, Vol. 64, No. 2, pp. 242—249.
- Farzalieva G. S., Esyunin S. L., The harvestman fauna of the Urals, Russia, with a key to the Ural species (Arachnida: Opiliones), Arthropoda Selecta, 2000, Vol. 8, No. 3, pp. 183—199.
- Farzalieva G. S., Opredelitel’ mnogonozhek (Myriapoda) Urala i Priural’ya (The identification keys of Ural Myriapoda), Vestnik Permskogo universiteta, 2009, Vol. 10, No. 36, pp. 66—72.
- Geras’kina A.P., Naselenie dozhdevykh chervei (Lumbricidae) v osnovnykh tipakh temnokhvoinykh lesov Pechoro-Ilychskogo zapovednika (Population of earthworms (Lumbricidae) in the main types ofdark coniferous forests at the Pechora-Ilych nature reserve), Zoologicheskii zhurnal, 2016б, Vol. 95, No. 4, pp. 394—405. https://doi.org/10.7868/S0044513416020094
- Geras’kina A.P., Problemy kolichestvennoi otsenki i ucheta faunisticheskogo raznoobraziya dozhdevykh chervei v lesnykh soobshchestvakh (Problems of quantification and accounting faunal diversity of earthworms in forest communities), Russian Journal of Ecosystem Ecology, 2016a, Vol. 1, No. 2. https://doi.org/10.21685/2500-0578-2016-2-4
- Geras’kina A.P., Shevchenko N. E., Biotopicheskaya priurochennost’ dozhdevykh chervei v malonarushennykh lesakh Teberdinskogo biosfernogo zapovednika (Biotopic association of earthworms in intact forests of Teberda Nature Reserve), Lesovedenie, 2018, No. 6, pp. 464—478. https://doi.org/10.1134/S0024114818060037
- 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 Jr K., Cummins K. W., Ecology of coarse woody debris in temperate ecosystems, Advances in Ecological Research, 1986, Vol. 15, pp. 133—302.
- Haughian S. R., Frego K. A., Does CWD mediate microclimate for epixylic vegetation in boreal forest understories? A test of the moisture-capacitor hypothesis, Forest Ecology and Management, 2017, Vol. 389, pp. 341—351. https://doi.org/10.1016/j.foreco.2017.01.011
- Huhta V., Siira-Pietikäinen A., Penttinen R., Importance of dead wood for soil mite (Acarina) communities in boreal old-growth forests, Soil Organisms, 2012, Vol. 84, No. 3, pp. 499—512.
- Jabin M., Mohr D., Kappes H., Topp W., Influence of deadwood on density of soil macro-arthropods in a managed oak-beech forest, Forest Ecology and Management, 2004, Vol. 194, No. 1-3, pp. 61—69. https://doi.org/10.1016/j.foreco.2004.01.053
- Kappes H., Catalano C., Topp W., Coarse woody debris ameliorates chemical and biotic soil parameters of acidified broad-leaved forests, Applied Soil Ecology, 2007, Vol. 36, No. 2, pp. 190—198. https://doi.org/10.1016/j.apsoil.2007.02.003
- Kappes H., Jabin M., Kulfan J., Zach P., Topp W., Spatial patterns of litter-dwelling taxa in relation to the amounts of coarse woody debris in European temperate deciduous forests, Forest Ecology and Management, 2009, Vol. 257, No. 4, pp. 1255—1260.
- http://dx.doi.org/10.1016/j.foreco.2008.11.021
- Kemencei Z., Farkas R., Pall-Gergely B., Vilisics F., Nagy A., Hornung E., Solymos P., Microhabitat associations of land snails in forested dolinas: Implications for coarse filter conservation, Community Ecology, 2014, Vol. 15, No. 2, pp. 180—186. https://doi.org/10.1556/comec.15.2014.2.6
- Khanina L., Bobrovsky M., Value of large Quercus robur fallen logs in enhancing the species diversity of vascular plants in an old-growth mesic broad-leaved forest in the Central Russian Upland, Forest Ecology and Management, 2021, Vol. 491: 119172. https://doi.org/10.1016/j.foreco.2021.119172
- Kluber M. R., Olson D. H., Puettmann K. J., Downed wood microclimates and their potential impact on plethodontid salamander habitat in the Oregon Coast Range, Northwest Science, 2009, Vol. 83, No. 1, pp. 25—34.
- Korkina I. N., Vorobeichik E. L., Humus Index as an indicator of the topsoil response to the impacts of industrial pollution, Applied Soil Ecology, 2018, Vol. 123, pp. 455—463. https://doi.org/10.1016/j.apsoil.2017.09.025
- Korkina I. N., Vorobeichik E. L., Non-typical degraded and regraded humus forms in metal-contaminated areas, or there and back again, Geoderma, 2021, Vol. 404: 115390. https://doi.org/10.1016/j.geoderma.2021.115390
- Korkina I. N., Vorobeichik E. L., The Humus index: A promising tool for environmental monitoring, Russian Journal of Ecology, 2016, Vol. 47, No. 6, pp. 526—531. https://doi.org/10.1134/s1067413616060084
- Langdon C. J., Piearce T. G., Feldmann J., Semple K. T., Meharg A. A., Arsenic speciation in the earthworms Lumbricus rubellus and Dendrodrilus rubidus, Environmental Toxicology and Chemistry, 2003, Vol. 22, No. 6, pp. 1302—1308.
- Langdon C. J., Piearce T. G., Meharg A. A., Semple K. T., Resistance to copper toxicity in populations of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from contaminated mine wastes, Environmental Toxicology and Chemistry, 2001, Vol. 20, No. 10, pp. 2336—2341.
- Mikhailova I. N., Dynamics of distribution boundaries of epiphytic macrolichens after reduction of emissions from a copper smelter, Russian Journal of Ecology, 2022, Vol. 53, No. 5, pp. 335—346. https://doi.org/10.1134/S1067413622050083
- Mikhailova I. N., Dynamics of epiphytic lichen communities in the initial period after reduction of emissions from a copper smelter, Russian Journal of Ecology, 2020, Vol. 51, No. 1, pp. 38—45. https://doi.org/10.1134/s1067413620010075
- Mikryukov V. S., Dulya O. V., Bergman I. E., Lihodeevskiy G. A., Loginova A. D., Tedersoo L., Sheltering role of well-decayed conifer logs for forest floor fungi in long-term polluted boreal forests, Frontiers in Microbiology, 2021, Vol. 12: 729244. https://doi.org/10.3389/fmicb.2021.729244
- Mikryukov V. S., Dulya O. V., Contamination-induced transformation of bacterial and fungal communities in spruce-fir and birch forest litter, Applied Soil Ecology, 2017, Vol. 114, pp. 111—122. https://doi.org/10.1016/j.apsoil.2017.03.003
- Mikryukov V. S., Dulya O. V., Modorov M. V., Phylogenetic signature of fungal response to long-term chemical pollution, Soil Biology and Biochemistry, 2020, Vol. 140: 107644. https://doi.org/10.1016/j.soilbio.2019.107644
- Mukhacheva S. V., Long-term dynamics of small mammal communities in the period of reduction of copper smelter emissions: 1. Composition, abundance, and diversity, Russian Journal of Ecology, 2021, Vol. 52, No. 1, pp. 84—93. https://doi.org/10.1134/s1067413621010100
- Nesterkov A. V., Grebennikov M. E., Grassland land snail communities after reduction of emissions from a copper smelter, Russian Journal of Ecology, 2020, Vol. 51, No. 6, pp. 578—588. https://doi.org/10.1134/S1067413620060065
- Nesterkov A. V., Recovery signs in grass-stand invertebrate communities after a decrease in copper-smelting emissions, Russian Journal of Ecology, 2022, V. 53, No. 6, pp. 553—564. https://doi.org/10.1134/S1067413622060133
- Nesterkova D. V., Distribution and abundance of European mole (Talpa europaea L.) in areas affected by two Ural copper smelters, Russian Journal of Ecology, 2014, Vol. 45, No. 5, pp. 429—436.
- Paradis E., Schliep K., ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, 2019, Vol. 35, pp. 526—528. https://doi.org/10.1093/bioinformatics/bty633
- Parisi F., Pioli S., Lombardi F., Fravolini G., Marchetti M., Tognetti R., Linking deadwood traits with saproxylic invertebrates and fungi in European forests — A review, IForest, 2018, Vol. 11, No. 3, pp. 423—436. https://doi.org/10.3832/ifor2670-011
- Peel M. C., Finlayson B. L., McMahon T.A., Updated world map of the Köppen-Geiger climate classification, Hydrology and Earth System Sciences, 2007, Vol. 11, No. 5, pp. 1633—1644. https://doi.org/10.5194/hess-11-1633-2007
- Persson T., Lenoir L., Vegerfors B., Which macroarthropods prefer tree stumps over soil and litter substrates?, Forest Ecology and Management, 2013, Vol. 290, pp. 30—39. https://doi.org/10.1016/j.foreco.2012.09.009
- Płytycz B., Kielbasa E., Grebosz A., Duchnowski M., 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. https://doi.org/10.1016/j.chemosphere.2010.06.056
- Pustejovsky J. E., Using response ratios for meta-analyzing single-case designs with behavioral outcomes, Journal of School Psychology, 2018, Vol. 68, pp. 99—112. https://doi.org/10.1016/j.jsp.2018.02.003
- Raymond-Léonard L.J., Bouchard M., Handa I. T., Dead wood provides habitat for springtails across a latitudinal gradient of forests in Quebec, Canada, Forest Ecology and Management, 2020, Vol. 472: 118237. https://doi.org/10.1016/j.foreco.2020.118237
- Römbke J., Blick T., Dorow W. H.O., Allolobophoridella eiseni (Lumbricidae), a truly arboreal earthworm in the temperate region of Central Europe, Soil Organisms, 2017, Vol. 89, No. 2, pp. 75—84.
- Spiders of Europe, available at: www.araneae.nmbe.ch (October 03, 2023).
- Sysoev A., Schileyko A., Land snails and slugs of Russia and adjacent countries, Sofia, Moscow: Pensoft, 2009, 179 p.
- Terhivuo J., Pankakoski E., Hyvarinen H., Koivisto I., Pb uptake by ecologically dissimilar earthworm (Lumbricidae) species near a lead smelter in south Finland, Environmental Pollution, 1994, Vol. 85, No. 1, pp. 87—96.
- Topp W., Kappes H., Kulfan J., Zach P., Distribution pattern of woodlice (Isopoda) and millipedes (Diplopoda) in four primeval forests of the western Carpathians (Central Slovakia), Soil Biology and Biochemistry, 2006, Vol. 38, No. 1, pp. 43—50.
- Trubina M. R., Mikhailova I. N., Dyachenko A. P., Dynamics of communities of cryptogamic organisms on dead wood after reduction of the emissions from a copper smelter, Russian Journal of Ecology, 2022, Vol. 53, No. 6, pp. 437—447. https://doi.org/10.1134/S1067413622060169
- Vorobeichik E., Nesterkov A., Ermakov A., Zolotarev M., Grebennikov M., Diversity and abundance of soil macroinvertebrates along a contamination gradient in the Central Urals, Russia, Biodiversity Data Journal, 2022, Vol. 10: e76968. https://doi.org/10.3897/BDJ.10.e76968
- Vorobeichik E., Nesterkov A., Golovanova E., Nesterkova D., Ermakov A., Grebennikov M., Long-term dynamics of the abundance of earthworms and enchytraeids (Annelida, Clitellata: Lumbricidae, Enchytraeidae) in forests of the Central Urals, Russia, Biodiversity Data Journal, 2021, Vol. 9: e75466. https://doi.org/10.3897/BDJ.9.e75466
- Vorobeichik E. L., Bergman I. E., Bait-lamina test for assessment of polluted soils: Rough vs. Precise scales, Ecological Indicators, 2021, Vol. 122: 107277. https://doi.org/10.1016/j.ecolind.2020.107277
- Vorobeichik E. L., Bergman I. E., Bait-lamina test in the assessment of polluted soils: Choice of exposure duration, Russian Journal of Ecology, 2020, Vol. 51, No. 5, pp. 430—439. https://doi.org/10.1134/S1067413620050136
- Vorobeichik E. L., Ermakov A. I., Grebennikov M. E., Initial stages of recovery of soil macrofauna communities after reduction of emissions from a copper smelter, Russian Journal of Ecology, 2019, Vol. 50, No. 2, pp. 146—160. https://doi.org/10.1134/S1067413619020115
- Vorobeichik E. L., Ermakov A. I., Nesterkova D. V., Grebennikov M. E., Coarse woody debris as microhabitats of soil macrofauna in polluted areas, Biology Bulletin, 2020, Vol. 47, No. 1, pp. 87—96. https://doi.org/10.1134/s1062359020010173
- Vorobeichik E. L., Ermakov A. I., Zolotarev M. P., Tuneva T. K., Izmenenie raznoobraziya pochvennoi mezofauny v gradiente promyshlennogo zagryazneniya (Changes in diversity of soil macrofauna in industrial pollution gradient), Russian Entomological Journal, 2012, Vol. 21, No. 2, pp. 203—218.
- Vorobeichik E. L., Changes in thickness of forest litter under chemical pollution, Russian Journal of Ecology, 1995, Vol. 26, No. 4, pp. 252–258.
- Vorobeichik E. L., 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 Science, 2017, Vol. 50, No. 8, pp. 977–990. https://doi.org/10.1134/s1064229317080130
- Vorobeichik E. L., Korkina I. N., A bizarre layer cake: Why soil animals recolonizing polluted areas shape atypical humus forms, Science of the Total Environment, 2023, Vol. 904: 166810. https://doi.org/10.1016/j.scitotenv.2023.166810
- Vorobeichik E. L., Nesterkova D. V., Technogenic boundary of the mole distribution in the region of copper smelter impacts: Shift after reduction of emissions, Russian Journal of Ecology, 2015, Vol. 46, No. 4, pp. 377—380.
- Vorobeichik E. L., Pishchulin P. G., Effect of trees on the decomposition rate of cellulose in soils under industrial pollution, Eurasian Soil Science, 2011, Vol. 44, No. 5, pp. 547—560. https://doi.org/10.1134/S1064229311050140
- Vorobeichik E. L., Seasonal changes in the spatial distribution of cellulolytic activity of soil microflora under conditions of atmospheric pollution, Russian Journal of Ecology, 2007, Vol. 38, No. 6, pp. 398—407.
- Vorobeichik E. L., Trubina M. R., Khantemirova E. V., Bergman I. E., Long-term dynamic of forest vegetation after reduction of copper smelter emissions, Russian Journal of Ecology, 2014, Vol. 45, No. 6, pp. 498—507. https://doi.org/10.1134/s1067413614060150
- Vsevolodova-Perel’ T.S., Dozhdevye chervi fauny Rossii (Earthworms of Russian fauna), Moscow: Nauka, 1997, 101 p.
- Zolotarev M. P., Changes in the taxonomic structure of herpetobiont arachnids along the gradient of pollution with emissions from a copper smelter, Russian Journal of Ecology, 2009, Vol. 40, No. 5, pp. 378—382.
- Zolotarev M. P., Nesterkov A. V., Arachnids (Aranei, Opiliones) in meadows: Response to pollution with emissions from the Middle Ural Copper Smelter, Russian Journal of Ecology, 2015, Vol. 46, No. 1, pp. 81—88. https://doi.org/10.1134/s1067413614060162
- Zuo J., Fonck M., van Hal J., Cornelissen J. H.C., Berg M. P., Diversity of macro-detritivores in dead wood is influenced by tree species, decay stage and environment, Soil Biology and Biochemistry, 2014, Vol. 78, pp. 288—297. https://doi.org/10.1016/j.soilbio.2014.08.010
Arquivos suplementares
