Green Algae in Tundra Soils Affected by Coal Mine Pollutions*

Biologia 63/6: 831—835, 2008 Section Botany DOI: 10.2478/s11756-008-0107-y

Green algae in tundra soils aﬀected by coal mine pollutions*

Elena N. Patova 1 &MarinaF.Dorokhova2

1Institute of Biology, Komi Scientiﬁc Centre, Ural Division, Russian Academy of Sciences, Kommunisticheskaya st. 28, 167982, Syktyvkar, Komi Republic, Russia; e-mail: [email protected] 2Moscow State University, Faculty of Geography, Vorobievy Gory GSP-2, 119992, Moscow, Russia; e-mail: doro- [email protected]

Abstract: Green algal communities were investigated in clean and pollution-impacted tundra soils around the large coal mine industrial complex of Vorkuta in the E. European Russian tundra. Samples were collected in three zones of open-cast coal mining with different degrees of pollution-impacted soil transformation. A total of 42 species of algae were found in all zones. The species richness decreased from 27 species in undisturbed zones to 19 species in polluted zones. Under open-cast coal mining impacts the community structure simplified, and the dominant algae complexes changed. Algae that are typical for clean soils disappeared from the communities. The total abundance of green algae (counted together with Xanthophyta) ranged between 100–120 × 103 (cells/g dry soils) in undisturbed zones and 0.5–50 × 103 in polluted zones. Soil algae appear to be better indicators of coal mine technogenic pollution than flowering plants and mosses. Key words: green algae; diversity; coal mine impact; soil; north-European Russian tundra

Introduction tundra soils around the large industrial coal mine complex of Vorkuta in the north-European Russian tundra (Fig. 1). Soil algae are an important autotrophic component of This region is exposed to heavy air pollution. Algal sam- the biota in all terrestrial habitats. They play a sig- ples were collected in differently impacted zones near the nificant role in soil genesis, stabilization of substrata open-cast coal mine “Yun Yaga” during the months of June- September in 2001–2004. Experimental plots were chosen to and the formation of organic matter in natural and be typical for the studied area. The soil algae were studied in technogenic soils (Maxwell 1991; Johansen & Shubert seven plots in three zones (Fig. 1, Table 1). Using field data 2001; Hoffmann et al. 2007). Investigations of the soil and Landsat TM satellite images, two impact zones were algae biodiversity in the European Russian tundra re- identified (Kulugina et al. 2005), namely a disturbed pol- gions started a long time ago, but data on distribution luted zone (0–100 m from coal mine dumps), and a slightly of green algae in tundra soils are scant (Getzen et al. disturbed and polluted zone (100–950 m). A third zone was 1994; Andreeva 2004; Andreeva & Czaplygina 2006). an undisturbed area located at a distance of more than 950 The Russian E. Europe tundra regions have a strong m. The higher plant vegetation was described for examined plots. anthropogenic impact because of activities associated 2 3 with the extraction of combustive minerals (coal, oil From each plot (size 10 m ), 10 soil samples (1 cm each) were randomly taken from different places and mixed and gas). The effects of anthropogenic factors on vari- together for analysis. Samples were taken from the upper ous soil algae have been poorly investigated, although 1–2 cm soil layer. Algal species were determined in cultures it is known that soil algae are pioneers of recovery on established by mixing soil samples with liquid Gromova – coal mine dump (Shushueva 1974; Lukešová & Komárek 6 and Bold Basal media, grown in growth room (SHKS- 1987; Lukešová 2001; Pivovarova & Shumlanskaja 2002; 0.6 B, Russia) during three weeks (day/night 16/8 h, under ◦ Dorokhova 2003). temperature 20/12 C). The main literature used for species The goal of this study is to compare soil green al- identification included Korshikov (1953), Ettl & Gärtner gal communities in three open-cast coal mining zones (1995), Lokhorst (1996) and Andreeva (1998). Algae abun- × that are characterised by different degrees of soil trans- dance was assessed by 5-point scale (15 25 magnification): 1 (rare) – from 1 to 10 individuals in a preparation; 2 (quite formation. often)–from10to50ind.inapreparation;3(frequent)– from 10 to 25 ind. in each 45 field of vision in a preparation; Material and methods 4 (very frequent) – from 25 to 50 ind. in each 45 field of vision in a preparation; 5 (in weight) – 50 and more ind. Algal communities were investigated in clean and impacted in each 45 field of vision in a preparation. Samples scan-

* Presented at the International Symposium Biology and Taxonomy of Green Algae V, Smolenice, June 26–29, 2007, Slovakia.

c 2008 Institute of Botany, Slovak Academy of Sciences 832 E.N. Patova &M.F.Dorokhova

Fig. 1. Map of the study region and zones of open-cast coal mine “Yun Yaga” (A, B, C – coal mining impacted zones, see Table 1).

3,5 3 Sr 2,5 Be 2 Mo 1,5 Ni 1 Cu 0,5 Zn 0 Concentration coefficient 1-C 2-B 3-B 4-B 5-A 6-A 7-A Plots

Fig. 2. The ratio of the heavy metals concentration coeﬃcients in polluted sites soil relative to a background zone.

Table 1. Experimental plots of vegetation and soils pH description.

Plot Zone Distance from dump, m Plant vegetation/Soil pH (H2O) in A0 or AT

1-C Undisturbed 1300 Willow – dwarf birch-moss spotty tundra/pH 4.5–5

2-B 850 Small shrub-herbs-moss hummock spotty tundra/pH 4.5–5 3-B Slightly disturbed and polluted 500 Herbs-grasses-sedge meadow/ pH 5.0–5.5 4-B 350 Moss-herbs-willow tundra/pH 4.5–5.5

5-A 12 Dwarf birch-willow-herbs-moss tundra/pH 5.9–6.2 6-A Disturbed and polluted 0 Grasses-herbs-moss primitive plant aggregation pH 6.0–6.2 7-A 0 Herbs-horsetail (Equisetum sp.) primitive plant aggregation/pH 7.5–8.0 ning were repeated five times. The algal communities of pH that was lower than that in the disturbed and pol- the plots were compared using the Sörensen-Czekanovski luted zones (Table 1). Concentrations of heavy metals index of similarity with the help of the clustering program in soils exceeded the background values 2–3 times un- GRAPHS (Novakovsky 2004). der impact conditions (Fig. 2). High concentrations of Soil pH and heavy metal content (in mg/kg of dry mat- Sr, Be, Mo, Ni, Cu and other elements were found in ter) were analysed in the soil samples. For the quantitative the impact zone. analysis of heavy metals we employed the method of atomic- emission spectrometry with inductively coupled plasma us- A total of 145 species and formae of algae were ing a Spectro Ciros CCD spectrometer in the Institute of found in the three zones: 39 Cyanoprokaryota, 22 Xan- Biology Komi SC. The ordination of the study plots with thophyta, 32 Bacillariophyta, and 42 Chlorophyta and heavy metal and algae species diversity was carried out with Streptophyta. Green algae were the most diverse group the PC-ORD software (McCune et al. 2002). and were found in all zones (Table 2). Species richness decreased from undisturbed (27 taxa) to polluted zones Results and discussion (10–12 taxa) (Table 3). In the investigated zones the species composition of algal groups was different (Ta- Plots in the undisturbed zone were characterized by a ble 3). At open-cast coal mining impacted sites the algal Green algae in tundra soils 833

Table 2. Green algae found in three zones of open-cast coal mining with diﬀerent intensity of soil transformation. The list of species is presented in alphabetical order. Symbols used: 1–5 – relative abundance of species in points, x – species found only in liquid nutrient medium, therefore the abundance in the ﬁeld was not determined.

Taxa 1-C 2-B 3-B 4-B 5-A 6-A 7-A

Bracteacoccus sp. x x x x Characium sp. 1 Chlamydomonas sp. x x x x x Chlorella minutissima Fott et Novák. 1 1 C. vulgaris Beijer. 3 2 2 2 4 3 Chlorococcum lobatum (Korsch.) Fritsch et John 2 C. oleofaciens Trainor et Bold 2 Chlorococcum sp. 42xxx Chlorosarcina sp. x x x x Chlorosarcinopsis bastropiensis Groover et Bold x Ch. minor Hernd. x Chlorosarcinopsis sp. xx Coccomyxa gloeobotrydiformis Reisigl 3 C. subglobosa Pasch. x 1 Coenocystis oleifera (Broady) Hind. var. oleifera 44 Cosmarium anceps Lund. 2 C. hexalobum Nordst. 2 C. undulatum Corda 2 Cosmarium sp. x Cylindrocystis brebissonii Menegh. 1 1 Desmococcus olivaceus (Pers. ex Ach.) Laundon 1 Geminella terricola Boye-Pet. 1 Gloeocystis polydermatica (Kütz.) Hind. x x Keratococcus bicaudatus (A. Br.) Boye-Pet. 1 K. rhaphidioides (Hansg.) Pasch. 1 Klebsormidium flaccidum (Kütz.) Silva et al. 4 1 2 4 1 2 2 K. nitens (Menegh. in Kütz.) Lokhorst 1 1 Leptosira terrestris (Fritch et John) Printz x L. terricola (Bristol) Printz x x x Mesotaenium caldariorum (Lagerh.) Hansg. 3 3 M. chlamydosporum f. minus (Reinsch)W.etG.West 1 1 M. macrococcum (Kütz.) Roy et Biss. 1 Myrmecia bisecta Reisigl 1 1 1 1 M. incisa Reisigl 2 2 3 1 1 1 Pseudococcomyxa chodatii (Jaag) Kostikov, Darienko et Hoffmann x x Pseudococcomyxa simplex (Mainx) Fott 1 1 x 2 1 Scotiellopsis oocystiformis (Lund) Fott x Stichococcus bacillaris Näg. x1 S. minor Näg. 3 2 2 3 5 Tetracystis sp. 32 2 Tetracystis sp. x x x Ulothrix variabilis Kütz. 2 1 community structure was simplified, as the number of to be sensitive to the environmental impact caused by dominant algae complexes was reduced from 11 to 1–2 the mining activities. Algae that are known indica- species (Table 3). Figure 3 shows the results of a cluster- tors of relatively clean soils, e.g. Cosmarium hexalo- ing analysis of the species composition of the different bium, C. anceps, C. undulatum, Coenocystis oleifera, plots. Three distinct groups of species complexes could and Cylindrocystis brebissonii were completely absent be distinguished which appeared to be correlated with from communities located in the impact zone. On the the soil pH: plots 1C – 2B (pH 4.5), plots 3B – 5A (pH other hand, stress-tolerant algae such as Bracteacoc- 5.5), and 6A – 7A (pH 6–7). The same grouping of plots cus aggregatus, Spongiochloris gigantea, Chlorella vul- was obtained by a Bary-Curtis component analysis on garis, Klebsormidium flaccidum, Myrmecia incisa and the basis of the content of heavy metals in soils (Fig. 4). Stichococcus minor were present in all plots. In impacted soil the number of Cyanoprokary- The total abundance of green and yellow-green al- ota and Chlorophyta increased, Bacillariophyta de- gae varied between 100–120 × 103 cells g−1 of dry soil in creased and Xanthophyta disappeared. The differences the undisturbed zone, and 0.5–50 × 103 cells g−1 of dry in the structure of the green algal communities could soil in polluted zones. The highest total cell number of be demonstrated at the generic level. Increase of the soil green algae was encountered in the unpolluted plot technogenic pressure resulted in soil alkalization which 1-C whereas the lowest number of algal cells was ob- coincided with the disappearance of Chlorosarcinopsis served in plot 7-A, which had the highest pH and heavy and Mesotaenium as well as decreased diversity of aci- metal contamination. All plots from the impacted zone dophilic species of the genera Cosmarium and Cylin- showed a low algal density. drocystis. The representatives of these genera appeared The diversity of algae and that of higher plants 834 E.N. Patova &M.F.Dorokhova

Table 3. Dominant and characteristic species of algae in the investigated plots.

Plot No of taxa Dominant Characteristic species for this plot

1-C 27 Klebsormidium flaccidum, Coenocys- Chlorosarcinopsis bastropiensis, Cosmarium anceps, C. hex- tis oleifera alobium, C. undulatum, Cylindrocystis brebissonii, Mesotae- nium macrococcum, Scotiellopsis ocystiformis 2-B 19 Bracteacoccus aggregatus, Coenocys- Coccomyxa gloeobotrydiformis, Desmococcus olivaceus, tis oleifera Geminella terricola, Keratococcus bicaudatus, K. rhaphidioides 3-B 13 Klebsormidium flaccidum Chlorosarcinopsis minor 4-B 10 Klebsormidium flaccidum – 5-A 10 Stichococcus minor, Bracteacoccus – aggregatus, Chlorella vulgaris 6-A 12 Chlorella vulgaris – 7-A 10 – Leptosira terrestris

Fig. 3. Diagram obtained after the cluster analysis of the species composition of the diﬀerent plots based on the S¨orensen-Czekanovski index. 1-C, 2-B, 4-B, 5-A, 6-A, 7-A – plots number; 21–52 – values of index (%).

disturbed and polluted zone was between 400–950 m and the relatively clean zone extended from 950 m on- wards. Comparison with the results for higher plants (Table 1), suggested that soil algae are more sensitive to coal mine pollution and are better indicators than ﬂow- ering plants. Our results were similar to those of studies of coal mine impacted soils in more southern climatic zones (Shushueva 1974; Lukešová & Komárek, 1987; Lukešová 2001; Pivovarova & Shumlanskaja 2002). This study has demonstrated that soil algae can be used as indicators of landscape technogenic transformation in tundra areas.

Acknowledgements

This work was made possible by a contract awarded by the Ministry of Environmental Protection of Komi Republic and by grant RFFI N 07-04-00443. The authors would like to Fig. 4. Ordination of study plots on soil characteristics (pH and thank M. V. Getzen for the field work organization and A. heavy metals). Patova for her help with translation. We are very grateful forthecommentsbyHansSluiman. reflected the different levels of pollution caused by References the coal mine in different ways. The diversity of al- Andreeva V.M. 1998. Terrestrial and aerophilic green algae gae showed that the strong impact zone was within a (Chlorophyta: Tetrasporales, Chlorococcales, Chlorosarci- radius of 400 m from the coal mine, the moderately nales). St. Petersburg, Nauka, 352 pp. (In Russian) Green algae in tundra soils 835

Andreeva V.M. 2004. Terrestrial nonmotile green microalgae Lokhorst G.M. 1996. Comparative taxonomic studies on the (Chlorophyta) in Vorkuta tundra (Komi Republic). Plan- genus Klebsormidium (Charophyceae) in Europe. Crypt. tarum non Vascularium 37: 3–8. (In Russian) Studies. 5: 1–132. Andreeva V.M. & Czaplygina O.Ya. 2006. Terrestrial nonmotile Lukešová A. 2001. Soil Algae in brown coal and lignite post- green microalgae (Chlorophyta) in area of industrial pollution mining areas in Central Europe (Czech Republic and Ger- of Vorkuta (Komi Republic). Plantarum non Vascularium 40: many). Restoration Ecol. 9 (4): 341 – 350. 13–18. (In Russian) Lukešová A. & Komárek J. 1987. Succession of soil alga on dumps Dorokhova M. 2003. Diatom algae as indicators of technogenic from strip coal-mining in the Most region (Czechoslovakia). changes in soils adjacent to a coal mine. Acta Bot. Warmiae Folia Geobot. Phytotax.22: 355–362. et Masuriae. 3: 145–154. Maxwell Ch. D. 1991. Floristic changes in soil algae and Ettl H. & Gärtner G. 1995. Syllabus der Boden-, Luft- und cyanobacteria in reclaimed metal-contaminated land at Sud- Flechtenalgen. Stuttgart, G. Fischer, 721 pp. bury, Canada. Water, Air Soil Pollut. 60: 381–393. Getzen M.V., Stenina A.S. & Patova E.N. 1994. Algaeflora of Metting B. 1981. The systematics and ecology of soil algae. Bot. Bolshezemelskaya tundra in conditions of anthropogenic im- Rev. 47: 195–312. pact. Yekaterinburg, Nauka, 148 pp. (In Russian) McCune B., Grace J.B. & Dean L. 2002. Analysis of ecological Kulugina E.E., Patova E.N., Istomina L.N. & Dorokhova M.F. communities. Oregon, Urban, 285 pp. 2005. Change of diversity and structure landscape forming Novakovsky A.B. 2004. Work facilities and principles of program groups of spore and flowering plants, pp. 126–179. In: Getzen module ”GRAPHS”. Syktyvkar, 30 pp. (In Russian) M.V. (ed.), Natural environment of the Vorkuta tundra in Pivovarova J.F. & Shumlanskaja N.A. 2002. Features of the struc- conditions of open-cast coal mining, Syktyvkar. (In Russian) tural organization algae groups of grass agrophytocenosis coal Hoffmann L., Ector L. & Kostikov I. 2007. Algal flora from limed mine spoil heaps in forest-steppe zone of the Kuznetsk depres- and unlimed forest soils in the Ardenne (Belgium). Syst. Ge- sion. Siberian Ecol. J. 1: 53–58. (In Russian) ogr. 77: 15–90. Shushueva M.G. 1974. Development of algae on dumps of Johansen J. & Shubert L.E. 2001. Soil algae. In: Elster J. et Krasnogorsky coal region. Problems of soils reclaiming in the al. (eds), Algae and Extreme Environments. Nova Hedwigia USSR, Novosibirsk, Nauka, pp. 188–194. (In Russian) Beih. 123: 297–306. Korshikov O.A. 1953. Subclass Protococcinaceae. Vyznachnyk Received September 1, 2007 prisnovodnych vodorostey Ukrajnskoj RSR 5. Kyiv, AN Accepted March 17, 2008 URSR, 437 pp.