green algae in spruce forests in the north-east of european russia

Biologia 63/6: 836—842, 2008Section BotanyDOI: 10.2478/s11756-008-0109-9

Green algae in spruce forests in the north-east of European Russia*

Irina V. Novakovskaya & Elena N. Patova

Institute of Biology, Komi Scientific Centre Ural Division, Russian Academy of Sciences, 28, Kommunisticheskaya St.,Syktyvkar, 167982, Russia; e-mail: [email protected], [email protected]

Abstract: The green algal communities in podzolic soils under coniferous forest in N.E. European Russia were studied inareas that were subjected to different technogenic pollution intensities. Sixty-five green algal species belonging to 4 classes,12 orders, 20 families and 27 genera were recorded. The algal communities in the investigated soils of the different typespruce phytocoenoses included from 15 to 38 taxa on one site. Indicator species were identified for background spruceforests (Chlamydomonas gelatinosa, Tetracystis aggregata, T. dissociata, Pseudopleurococcus botryoides, Myrmecia bisecta)and for aerotechnogenically polluted spruce forests (Actinochloris sphaerica). The results may be used for the monitoringof the ecological state of biota in soils under boreal forests of protected areas and spruce forests exposed to intense aerialtechnogenic pollution.

Key words: green algae; spruce forest; aero-technogenic pollution; central and southern taiga; Russia

Introduction

Spruce forests are an important component of taigavegetation. They greatly affect the ecological stateof the natural complexes by performing bio-ecologicalfunctions such as regulation and filtration of waterrun-off; erosion control, as well as preserving and in-creasing soil fertility, enrichment of the atmospherewith oxygen, fixation of carbon, mitigating climateconditions and prevention of aerial pollution. In thearea of industrial cities, forest ecosystems are impor-tant barriers, reducing pollutant accumulation. How-ever, they are exposed to pollution to the greatest ex-tent. Monitoring of the state of all the componentsof biota and use of the most indicative living organ-isms are necessary for the assessment of structuraland functional changes in forest communities. Micro-organisms and soil algae are very sensitive to envi-ronmental changes, and they are widely used for thebiodiagnostics of soils. The disturbance of the com-munities of these organisms is related to the degreeof technogenic impact and begins with the changes inthe biomass and composition of the dominant species.A further increase of the anthropogenic load leads toa poorer species composition and a decrease in thequantitative characteristics (Metting 1981; Aleksakhina& Shtina 1984; Hoffmann 1989; Johansen & Shubert2001).Data on the state of algal groups, including green

algae, in the soils under coniferous forest (the mid-dle and southern taiga zones) under influence different

types of pollution are scarce. This fact determined thechoice of the subject for this work.The aim of this study was to assess the species di-

versity and structure of soil green algae belonging tothe divisions Chlorophyta and Streptophyta in spruceforests under different levels of aero-technogenic pollut-ing stress.

Material and methods

Samples of soils and algae were collected during three fieldseasons (2003–2005) from permanent test plots in differentperiods of vegetation from June to October. The plots werelocated in a spruce forest of the middle and southern taigaof north-east European Russia (Republic of Komi, Kirovregion) under undisturbed reference phytocoenoses, in ar-eas exposed to various technogenic emissions and recreationloads of different degrees (Fig. 1; Tables 1, 2). The pollutionsources included (a) the Kirovo-Chepetsk chemical complex(plot 1), (b) an area for the storage and destruction of chem-ical weapons known as “Maradykovskii” (pl. 3–4), (c) emis-sions from the towns of Kirov and Slobodskoi (pl. 6), (d)a paper-and-pulp factory complex (pl. 7), and (e) a motorway bypass (pl. 8–12).

The sampling was carried out according to the methodsdescribed in Shtina & Gollerbakh (1976). One hundred andfour samples (pooled from 10 individual samples) from conif-erous phytocoenoses of different types were analyzed. Thesoil-algological samples were collected from a depth of 0–15cm (including the forest litter 0–5 cm, eluvial-humus andpodzol horizons 5–15 cm), since at this depth the highestspecies diversity and abundance of soil algae were recorded.The species diversity of algae was studied using dish, liquid

* 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

Green algae in spruce forests 837

Fig. 1. Schematic map of the study region.Middle taiga subzone: 1 – the “Bylina” reserve Podosinovskii and Oparinskii districts, Kirov oblast (pl. 13–17); 2 – outskirts ofSyktyvkar Republic of Komi (pl. 8–12).Southern taiga subzone: 3 – Yur‘yanskii district (pl. 7); 4 – Orichevskii district (pl. 3–4); 5 – Kirovo-Chepetsk district (pl. 1–2); 6 –Slobodskoy district (pl. 5–6).

and agar cultures with Bold’s, Bristol’s, and Drew’s me-dia. Algal cultures were maintained in a growth chamber(SHKS-0.6 B, Russia) during three weeks (day/night = 16/8h, under temperature 20/16◦C). The species composition ofsoil algae was determined using a microscope with ×640and ×1600 magnification. The main literature sources forspecies identification were Ettl & Gartner (1995), Lokhorst(1996) and Andreeva (1998). The systematics and nomen-clature of the taxa was in accordance with the list of soilalgae of Kostikov et al. (2001b).

The algal communities of the plots were comparedusing the Sorensen-Czekanovski index of similarity withthe help of the clustering program GRAPHS (Novakovsky2004). The ordination of the study plots with heavy metaland algal species diversity was carried out with PC-ORDsoftware (Mccune et al. 2002).

The chemical analyses of soil samples (collected froma depth of 0–15 cm at the points of the alga sampling) wasperformed in the Ecoanalytical Laboratory of the Instituteof Biology, Komi Scientific Centre Ural Division, RussianAcademy of Sciences. The contents of C and N (%) wereanalyzed with C, H, N, S, O – element analyzer EA 1110(Italy, CE Instruments); Ca2+ and Mg2+ (mmol/100 g), us-ing the method of atomic absorption on AAS Hitachi 180–60(Japan, Hitachi); P2O5 (mg/kg), using photometry (KFK-3, Russia); K2O (mg/kg) by the method of flame photome-try on SP-90 A Unicam spectrometer (England, PYE UNI-CAM); microelements and heavy metals Pb, Cd, Ni, Zn,Cu, Cr, Mn, Co, and Hg (mg/kg) by the method of atomic-emission spectrometry with inductively coupled plasma us-ing a Spectro Ciros CCD spectrometer (Germany, SpectroAnalytical Instruments GmbH).

Results and discussion

Spruce forest phytocoenoses are characterized by a lowdiversity and abundance of soil algae, because theirsoils are highly acidic, structureless, waterlogged and

nutrient-poor. In spruce forests aero-technogenic pol-lution has a further adverse effect on the ecologicalconditions. However, green algae are the most tolerantgroup to such unfavourable soil conditions (Lukešová &Komárek 1987; Lukešová & Hoffmann 1996; Kostikovet al. 2001a; Hoffmann et al. 2007).The low diversity of green algae in the soils under

the spruce forest was primarily related to low concen-trations of biogenic elements and high acidity of thepodzolic soils (Table 1). In the upper horizons of thesoils, the pHH2O ranged from 4.05 to 5.14. The con-tents of carbon and nitrogen, as well as their ratio(C/N), greatly affected the species diversity of the al-gal communities in the soils. The C/N ratio was ap-proximately 20. The concentration of all microelementsstudied in the soils of the forest located in the zone ofaero-technogenic pollution was higher by several ordersof magnitude than it was in unpolluted soils (Table 2).The low species diversity of algae in spruce forest

was also due to the high canopy density and strong mosscover. These conditions prevented algal development onthe soil surface. Several methods were used that allowedto discover green algae species diversity more com-pletely. Liquid and agar cultures methods were mostsuccessful to reveal the spectrum of alga species.In the spruce forest soil, 112 alga species (121 va-

rieties, including a nomenclature holotype) of 6 divi-sions were identified: Cyanophyta 6 (7), Euglenophyta 3(4), Eustigmatophyta 2 (3), Xanthophyta 9 (11), Bacil-lariophyta 22 (27), Chlorophyta and Streptophyta 65(69). Most of species belonged to the Chlorophyta. The65 green algal species represented 4 classes, 12 orders,20 families, 27 genera (Table 3). Algae from the fami-lies Chlamydomonadaceae, Chlorococcaceae, Bractea-coccaceae, Klebsormidiaceae predominated (Fig. 2).

838 I.V. Novakovskaya & E.N. Patova

Table 1. Concentrations of macroelements in podzolic soils of spruce forest.Note: The highest concentrations are shown in bold.

Ca2+ Mg2+ P2O5 K2OPlot pH H2O C/N

mmol/100 g mg/kg

Aerotechnogenic polluted plots

1 5.14 15.7 9.89 1.1 98.81 125.53 4.56 20.20 10.12 1.27 60.54 110.004 4.87 18.50 8.17 0.87 33.69 191.156 4.47 18.95 2.29 0.23 23.12 82.837 4.95 16.35 2.88 0.53 17.49 79.248 4.67 20.30 1.00 0.21 24.03 45.509 4.41 25.75 1.29 0.23 24.84 56.9510 4.42 18.05 2.03 0.44 53.30 111.3411 4.63 19.55 2.88 0.63 69.15 134.1512 4.65 23.20 2.34 0.36 21.28 89.93

Background plots

2 4.34 15.70 0.72 0.20 51.32 84.155 4.28 24.30 0.59 0.09 10.08 58.5213 4.05 21.33 0.67 0.22 38.15 74.9814 4.07 20.23 1.35 0.36 35.58 89.6915 4.34 19.17 1.02 0.21 27.51 67.4216 4.40 17.60 1.95 0.58 28.58 119.9617 4.69 22.20 4.34 0.87 27.01 120.60

Table 2. Concentrations of microelements and heavy metals in the soils of spruce forest (mg/kg). Note: The highest concentrationsare shown in bold.

Plot no. Pb Cd Ni Zn Cu Cr Mn Co Hg

Aerotechnogenic polluted plots

1 6.90 0.17 13.00 18.00 7.30 12.60 240.00 3.10 0.163 9.05 0.19 5.80 11.25 3.15 8.60 156.00 1.30 0.644 8.75 0.17 9.50 21.90 4.60 10.05 685.00 3.50 0.466 6.10 0.09 3.85 12.70 2.20 6.65 445.00 1.30 0.517 5.20 0.09 7.45 10.15 3.55 10.05 158.00 2.05 0.328 2.00 0.03 1.30 6.30 0.83 2.50 21.50 0.24 0.169 3.45 0.05 2.05 4.80 1.20 3.20 82.00 0.35 0.2510 5.90 0.07 2.55 6.70 1.35 6.15 128.50 0.89 0.2511 7.35 0.11 4.50 11.40 2.20 8.35 288.50 1.70 0.4512 2.10 0.04 0.93 3.55 0.81 1.95 69.00 0.22 0.14

Background plots

2 6.80 0.09 6.40 12.60 3.40 8.20 145.00 2.00 0.405 4.20 0.06 2.50 4.80 2.00 5.20 21.00 0.42 0.2113 3.50 0.04 2.03 4.90 2.07 4.97 37.10 0.53 0.3014 3.50 0.05 2.07 6.75 3.05 5.03 29.07 0.60 0.3315 3.47 0.03 1.64 9.47 1.74 4.33 59.90 0.46 0.2616 6.97 0.07 4.08 11.53 2.73 8.93 48.85 1.06 0.1817 3.10 0.06 2.62 4.73 1.88 4.73 51.40 0.81 0.45

The algal groups in the soils of different types spruceforests included from 15 to 38 taxa on one plot (Ta-ble 3). Wood sorrel-green moss, horse tail-bilberry, andbilberry-green moss spruce forests were remarkable forthe highest species diversity. Unlike other divisions, thespecies diversity of green algae was not reduced un-der aero-technogenic pollution, which is indicative oftheir good adaptability and preference for low soil pH.However, the taxonomic structure and dominants ofgreen algae had distinctions. In the unpolluted soils un-der the spruce forests 59 species of 16 families and 21

genera were identified. Most of the species were fromthe Chlamydomonadaceae, Chlorococcaceae and Kleb-sormidiaceae families. The species Chlamydomonasgelatinosa, C. gloeogama, C. reinhardtii, Chloro-

coccum infusionum, Chlorella vulgaris, Klebsormidiumnitens, Tetracystis aggregata, Stichococcus bacillariswere the most frequent.Fifty-five algal species belonging to 18 families

and 22 genera were identified in the soil of the conif-erous phytocoenoses located in the aero-technogenicpolluted zones. Most of the species belonged to the


Table 3. List of green algae in spruce forests.Note: 1 – horse-tail-aise-weed spruce forest; 2, 4 – wood sorrel spruce forest; 3, 16 – wood sorrel-green moss spruce forest; 5 –cowberry-green moss spruce forest; 6 – bilberry-wood sorrel-green moss spruce forest; 7 – wood sorrel-bilberry spruce forest; 14 –horse-tail-bilberry spruce forest; 8–13, 15, 17 – bilberry-green moss spruce forest.

Aerotechnogenic polluted plots background plotsTaxa

1 3 4 6 7 8 9 10 11 12 2 5 13 14 15 16 17

Actinochloris sphaerica Korsh. + + + + + + +Bracteacoccus aggregatus Tereg + + +Bracteacoccus giganteus Bisch. et Bold +Bracteacoccus grandis Bisch. et Bold + + + + +Bracteacoccus minor (Chod.) Petrová + + + + + + + + + + + + +Carteria multifilis (Fres.) Dill +Chlamydomonas actinochloris Deason et Bold + + + + + +Chlamydomonas acuta Korsh. in Pasch. + + +Chlamydomonas cf. debaryana Gorosch. var. atactogama + + + + + + + + + + + + + +(Korsch.) Gerloff

Chlamydomonas cf. gloeogama Korsch. in Pasch. + + + + + + + + + + + + + + + + +Chlamydomonas cf. incerta Pasch. + + + + + +Chlamydomonas cf. incisa Korsh. in Pasch. + + + + +Chlamydomonas cf. intermedia Chod. + + + + + +Chlamydomonas cf. minutissima Korsh. in Pasch. + +Chlamydomonas cf. noctigama Korsh. in Pasch. + +Chlamydomonas cf. proboscigera Korsh. in Pasch. + + + + + +Chlamydomonas cf. reinhardtii Dang. + + + + + + + + + + + + + + +Chlamydomonas cf. subcylindracea Korsch. + +Chlamydomonas culleus Ettl + + +Chlamydomonas elliptica Korsh. in Pasch. + + + + + + + + + + + + + + + +Chlamydomonas gelatinosa Korsh. in Pasch. + + + + + + + + + + +Chlamydomonas globosa Snow + + + +Chlamydomonas isogama Korsh. in Pasch. + + + + + + + + + + + + + +Chlamydomonas macrostellata Lund + +Chlamydomonas sp. + +Chlorella cf. vulgaris Beijer. var. vulgaris + + + + + + + + + + + + + + + + +Chlorella vulgaris Beijer. f. globosa V. Andr. + + + + + + + + + +


1 3 4 6 7 8 9 10 11 12 2 5 13 14 15 16 17

Chlorococcum cf. costatozygotum Ettl et Gartner +Chlorococcum cf. hypnosporum Starr + + +Chlorococcum infusionum (Schrank) Menegh. + + + + + + + + + + + + +Chlorococcum lobatum (Korsch.) Fritsch et John + + + + + + + + + + + + + +Chlorococcum minimum Ettl et Gartner + + + + + + + + + +Chlorolobion lunulatum Hindák + +Chlorosarcinopsis gelatinosa Chant. et Bold +Chlorosarcinopsis minor Hernd. + + + +Closterium pusillum var. monolithum Wittr. +Coccomyxa spp. + + +Cosmarium impressulum Elfv. + +Cosmarium undulatum Corda +Dictyochloris fragrans Vischer ex Starr +Elliptochloris cf. subsphaerica (Reisigl) Ettl et Gartner + + +Gloeocystis sp. +Keratococcus bicaudatus (A. Br.) B.-Peters. + + +Klebsormidium dissectum (Gay) Ettl et Gartner +Klebsormidium flaccidum (Kutz.) Silva et al. + + + + + + + + + + + + + +Klebsormidium nitens (Menegh. in Kutz.) Lokhorst + + + + + + + + + + + + + + + +Klebsormidium rivulare Kutz. + + + + +Klebsormidium subtilissimum (Rabenh.) Pickett-Heaps + + + +Leptosira sp. + +Leptosira terrestris (Frisch et John) Printz + + + + + + + + + + + +Leptosira terricola (Bristol) Printz + + + +Macrochloris chlorococcoides Ettl et Gartner +Macrochloris dissecta Korsh. + +Macrochloris sp. + +Myrmecia bisecta Reisigl + + + +Myrmecia incisa Reisigl + + + + + + + + + + + + + + + +Parietochloris cf. pseudoalveolaris (Deason et Bold) +Watanabe et Floyd in Deason et al.


Table 3. (continued)


1 3 4 6 7 8 9 10 11 12 2 5 13 14 15 16 17

Pseudococcomyxa cf. pringsheimii (Jaag) Kostikov et al. + +Pseudococcomyxa chodatii (Jaag) Kostikov, + + + +Darienko et Hoffmann

Pseudococcomyxa simplex (Mainx) Fott + + + + + + + + + + + + + +Pseudopleurococcus botryoides Snow + + + + + + +Scotiellopsis rubescens Vinatzer +Spongiochloris minor Chantanachat et Bold + +Stichococcus bacillaris Nag. + + + + + + + + + + + + + + + +Stichococcus cf. fragilis Gay + + + + +Stichococcus minor Nag. + + + + + + + + + + +Tetracystis dissociata Brown et Bold + + + + + + + +Tetracystis aggregata Brown et Bold + + + + + + + + + + +Ulothrix variabilis Kutz. +

Total 15 21 19 20 20 21 22 23 25 24 22 15 33 38 33 35 36

Fig. 2. Predominating families of algae spruce forest.On vertical – species number in family; on horizontal – family.

Chlamydomonadaceae and Chlorococcaceae. The al-gal groups in the soils under the disturbed spruce

forests consisted from 15 to 25 species on one plot (Ta-ble 3). In polluted soils the number of species fromthe families Actinochloridaceae,Myrmeciaceae and thegenus Macrochloris decreased, whereas the numberof Chlorosarcinaceae increased. Stichococcus minor,Pseudococcomyxa chodatii, and Pseudococcomyxa sim-plex were marked with a high abundance. Chlamy-domonas gloeogama, Chlamydomonas elliptica, Myrme-cia incisa, Klebsormidium nitens, Chlorella vulgaris,and Stichococcus bacillaris were marked almost on allaero-technogenic polluted plots, but they had a lowabundance.Indicator species that were identified with the PC-

ORD software (at a significance level of p > 0.05)for background spruce forests included Chlamydomonasgelatinosa, Tetracystis aggregata, T. dissociata, Pseu-dopleurococcus botryoides, Myrmecia bisecta and for

Fig. 3. The dendrogram of similarity between the species composition of algae in the soil under the spruce forest. On vertical –similarity according to the Sorensen-Czekanovski coefficient, %; on horizontal – plots number.


Fig. 4. The ordination of the study plots with heavy metal and species diversity vectors.Study region: open triangles – aerotechnogenic polluted plots; filled triangles – background plots. 1–17 – plot. Vector length Cd, Ni,Ca, pHH2O show the correlation value (Cd – 0.677; Ni – 0.676; Ca – 0.651; pH H2O – 0.743), Div – species diversity (−0.819). Axis 1– species diversity. Axis 2 – not interpreted.

spruce forests located on aero-technogenically pollutedsites Actinochloris sphaerica.A relatively high similarity of the taxonomic com-

position was noted for all the algal communities inves-tigated (the Sorensen-Czekanovski index was >45%).Two clusters of algal communities with a similar speciescomposition were identified (Fig. 3): one including thealgal groups of the soils under the coniferous forest ofthe background area, and a second cluster compris-ing algal groups of the soils in the anthropogenicallydisturbed territories. Within these groups the phyto-coenoses and the physico-chemical parameters of thesoils were similar.The highest negative correlation value, obtained

by PC-ORD, was between the diversity of soil algaeand the concentrations of the heavy metals Cd, Ni, aswell as Ca, and the pHH2O in upper horizons of the soil(Fig. 4).In conclusion, the algal groups in the soils under

the spruce forests were sensitive to aero-technogenicpollution, which was evident in the changes of theirstructure. The taxonomic diversity and structure ofgreen algal groups, their dominant complexes hadchanged in the territories with contents of heavy metals.These areas were located in the zone adjacent to the sitefor storage and destruction of chemical weapons, nearthe paper and pulp complex and the motor way, andin the vicinity of the towns of Kirov and Slobodskoi.The information on the diversity and structure of thealgal complexes in soils under coniferous forests maybe used for diagnostics of the state of the soils in theprotected areas and in the technogenically polluted ter-ritories.

Acknowledgements

This work was supported by a grant of the Ural Division ofthe Russian Academy of Sciences for young scientists andpostgraduates (2005) and by the Federal Agency for Sci-ence and Innovations (project No. RI-111 1002 1016). Theauthors thank the specialists of the Ecoanalytical Labora-tory of the Institute of Biology for the chemical soil analyses.We are very grateful for the comments by František Hindákand Hans Sluiman.

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Received September 1, 2007Accepted March 17, 2008

green algae in spruce forests in the north-east of european russia

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