Ecology of benthic diatoms from Lake Macro Prespa (Macedonia

13
Algological Studies 124 71-83 Stuttgart, July 2007 Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) ZLATKO LEVKOV , SAUL BiANCO 2 ^, SVETISLAV KRSTIC I , TEOFIL NAKOV and Luc EciOR 3 11nstitute of Biology, Faculty of Natural Sciences, Skopje, Republic of Macedonia. 2Area de Ecologi'a, Universidad de Leon, Leon, Spain sRublic Research Center- Gabriel Lippmann, Department Environment and Agro-biotechnologies, Belvaux, Grand-Duchy of Luxembourg With 4 figures and 2 tables Abstract: Lake Prespa belongs to the group of ancient lakes. By subterranean channels it is connected with Lake Ohrid. In the past two decades, Lake Prespa has been character- ized by a decrease of its water level and an increased cultural and natural eutrophication. In this period, very few ecological studies were performed, based mainly on composition and biomass of the phytoplankton community. From June 2002 to May 2003 analyses of 18 physical and chemical parameters and composition of benthic diatoms were per- formed on 12 sampling sites of Lake Macro Prespa. About 300 diatom taxa were identi- fied in the lake. Relative abundances were calculated by counting 200 diatom valves, and 143 diatom taxa had abundances of more than 1 % in at least one sampling site. Deep benthic communities were dominated by Cyclotella ocellata and Diploneis mauleri, while in the littoral region these communities were dominated by small Navicula sensu lato species. For statistical analyses, the 17 most abundant diatom taxa (> 1 % in total abundance) were used. Contrarily to the expectations, TP had a negligible influence on diatom community structure. The main environmental factors controlling species distri- bution and abundances were ammonium and metallic cations (Cu, Mn, K) and, secondar- ily, dissolved oxygen and Secchi depth, as inferred from both correlation and multivariate (CCA) analysis. Key words: benthic diatoms, Lake Prespa, ecology Introduction Some recent studies have focused on different aspects of the biology of algae in ancient lakes throughout the world (e.g. Lake El'Gygytgyn, CHEREPANOVA & BRIGHAM-GRETTE 2001; Lake Tanganyika, COCQUYT 1998; Lake Biwa, GENKAL 2003). Algal floras in these environments are characterized by high levels of di- 1864-1318/07/0124-071 $• ©2007 E. Schweizerbart'scheVerlagsbuchhandlung, D-70176 Stuttgart

Transcript of Ecology of benthic diatoms from Lake Macro Prespa (Macedonia

Algological Studies 124 71-83 Stuttgart, July 2007

Ecology of benthic diatoms from LakeMacro Prespa (Macedonia)

ZLATKO LEVKOV , SAUL BiANCO2^, SVETISLAV KRSTICI ,TEOFIL NAKOV and Luc EciOR3

11nstitute of Biology, Faculty of Natural Sciences, Skopje,Republic of Macedonia.2Area de Ecologi'a, Universidad de Leon, Leon, SpainsRublic Research Center- Gabriel Lippmann, Department Environment andAgro-biotechnologies, Belvaux, Grand-Duchy of Luxembourg

With 4 figures and 2 tables

Abstract: Lake Prespa belongs to the group of ancient lakes. By subterranean channels itis connected with Lake Ohrid. In the past two decades, Lake Prespa has been character-ized by a decrease of its water level and an increased cultural and natural eutrophication.In this period, very few ecological studies were performed, based mainly on compositionand biomass of the phytoplankton community. From June 2002 to May 2003 analyses of18 physical and chemical parameters and composition of benthic diatoms were per-formed on 12 sampling sites of Lake Macro Prespa. About 300 diatom taxa were identi-fied in the lake. Relative abundances were calculated by counting 200 diatom valves, and143 diatom taxa had abundances of more than 1 % in at least one sampling site. Deepbenthic communities were dominated by Cyclotella ocellata and Diploneis mauleri,while in the littoral region these communities were dominated by small Navicula sensulato species. For statistical analyses, the 17 most abundant diatom taxa (> 1 % in totalabundance) were used. Contrarily to the expectations, TP had a negligible influence ondiatom community structure. The main environmental factors controlling species distri-bution and abundances were ammonium and metallic cations (Cu, Mn, K) and, secondar-ily, dissolved oxygen and Secchi depth, as inferred from both correlation and multivariate(CCA) analysis.

Key words: benthic diatoms, Lake Prespa, ecology

Introduction

Some recent studies have focused on different aspects of the biology of algae inancient lakes throughout the world (e.g. Lake El'Gygytgyn, CHEREPANOVA &BRIGHAM-GRETTE 2001; Lake Tanganyika, COCQUYT 1998; Lake Biwa, GENKAL2003). Algal floras in these environments are characterized by high levels of di-

1864-1318/07/0124-071 $•©2007 E. Schweizerbart'scheVerlagsbuchhandlung, D-70176 Stuttgart

72 Z. LEVKOV et al.

versity and endemism (EDLUND et al. 2003). Concerning diatom communities,taxonomic and biogeographical particularities have been more focused on,while ecological aspects are relatively less known. Within European fresh-waters, one of these ecosystems is Lake Prespa (Macedonia). It belongs to agroup of ancient lakes located in a tectonic valley between Mountains Galicicaand Baba at 853 m a. s. 1. Analyses of short cores from Mikri Prespa (STEVENSON& FLOWER 1991) showed that the eutrophication levels have slightly changed inthe second half of the 20th century. The high abundance of Cyclotella ocellataPANTOCSEK throughout the core suggests that this lake is little affected by in-creased nutrient loadings. Studies on Lake Prespa diatoms confirm the domi-nance of C. ocellata in plankton and benthos (MiTicn & NAUMOVSKI 2000, LEV-KOV 2005). However, few studies on plankton assemblages have been carriedout (KOZAROV 1959, 1960), while investigations on benthic diatoms were ori-ented mainly on taxonomy and distribution (HUSTEDT 1945, LEVKOV et al. 2003,LEVKOV 2005). Former taxonomical studies showed the presence of several rareand endemic taxa (LEVKOV et al. 2006a, b), but data for their ecological prefer-ences are still lacking. This article is the first attempt to determine the ecologicalcharacteristics of the most dominant benthic diatom taxa in Lake Prespa.

Material and methods

1. Study site.

Lake Prespa is located in a tectonic valley between Mountains Galicica andBaba at 853 m a.s.l. The total surface area is 274 km2, and the maximal depth is54.2 m, with a total catchment area of 1095.22 km2 (CHAVKALOVSKI 1997). Itsbottom is mainly covered with organic sediment that enables intensive macro-phyte development during the summer period. There is no natural surface wateroutlet, and large amounts of water are discharged through underground channelsinto Lake Ohrid, under the Galicica Mountains and Suva Planina (ANOVSKJ et al.2001). Waters are calcium-rich and their pH is slightly alkaline.

The dry period that started in 1986, along with the intensive evaporation andusage of lake waters, resulted in a decrease of the water level by 7.8 m comparedto the maximal level (CHAVKALOVSKI 2000). More than half of these losses(57.8 %) were due to natural processes, while the rest was lost through the usefor different human purposes, mainly irrigation and water supplies. According toANOVSKJ et al. (2001), three possible natural factors are usually involved in de-creasing the water level (i) tectonic falling of the lake bottom; (ii) widening ofunderground channels connecting the two lakes and (iii) influence of meteoro-logical parameters. Such a decrease of the water level in the early nineties leadto changes in water quality. According to NAUMOVSKI et al. (1997), the waters ofLake Prespa in that period varied between oligotrophic and mesotrophic, whileSHUMKA (1994) found an oxygen depletion during summer. More recent investi-

Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) 73

Fig 1. Map of the study area showing the 12 sampling sites (black dots) on Lake MacroPrespa.

gations (LEVKOV 2005) showed that Lake Prespa is eutrophic during summer,with blooms of blue-green algae. According to GRUPCE (1997), about half of thephosphorus input in the lake (542.36 tons P2O$ per year) has an anthropogenicorigin. The most important sources of phosphorus in Lake Prespa are untreatedcommunal wastewater and fertilizers used in the region (TRPESKI et al. 2000).

2. Methodology

Water samples from Lake Prespa were collected between June 2002 and May2003 at 12 sampling sites (Fig. 1) located between 50 and 200 m from the shore,depending on bottom topography. Temperature, pH, dissolved oxygen concen-tration, and Secchi depth were measured directly in the field with appropriateequipment. Samples for chemical analyses were conserved in HgCh and trans-

74 Z. LEVKOV et al.

ported in a refrigerator at 4° C. Chemical analyses were performed following theprocedures of APHA (1985), MOORE & CHAPMAN (1986) and FISKE & SUBBAR-ROW (1925). Average values and standard deviation of measured physico-chemi-cal parameters are given in Table 1.

Benthic diatoms were collected with a Van Veen bottom sampler on variousdepths. In most of the cases samples were taken from a depth between 2 m and4 m, except for the pelagial zone where samples from 18m were collected. Priorto fixation with 4% formalin, live samples were observed (LEVKOV et al. 2006b).Diatom slides were prepared by acid digestion (KRAMMER & LANGE-BERTALOT1986) and mounted in Naphrax®. The slides are deposited in the Diatom Collec-tion at the Institute of Biology (DCIBS), Faculty of Natural Sciences, Skopje.Relative abundances were calculated by counting 200 diatom valves (BATE &NEWALL 1998).

Only the 17 diatom taxa that reached > 1 % of relative abundance in thewhole dataset were used in multivariate analyses. Diatom abundances were arc-sine square root transformed and the environmental variables, except pH, werelog-transformed due to their skewed distributions. Differences in diatom abun-dances and physico-chemical variables between samples were studied by meansof ANOVA. Detrended Correspondence Analysis (DCA) was carried out to ex-plore the relationships between diatom taxa and sampling stations and months.Canonical Correspondence Analysis (CCA) was used to relate the diatom as-semblages to environmental factors. All ordinations were run using the com-puter program CANOCO version 4.1 (TER BRAAK & SMILAUER 2002).

Results

A total of 297 diatom taxa were identified in Lake Prespa, and 143 of them hadabundances higher than 1 % in at least one sample. The greatest difference in di-atom composition between the eastern and the western coast was observed in thelittoral zone. The bottom of the west coast (from Stenje village to Perovo vil-lage) was covered with organic sediment. The dominant diatom species Cavi-nula scutelloides (W. SMITH) LANGE-BERTALOT, Navicula rotunda HUSTEDT,N. subrotundata HUSTEDT, Amphora pediculus (KuTZlNG) GRUNOW, and charac-teristic species of the two genera Aneumastus and Sellaphora were frequent inthe benthic communities. Additionally, this part of the lake shore consists of cal-careous rocks (limestone), while the eastern part is mainly formed by silicates.The eastern coast (D. Dupeni village to Pretor) is mostly covered by sand or amixture of sand and organic sediment. In this region, several Navicula sensustricto species are sub-dominant (LEVKOV 2005). It is supposed that the distribu-tion of these species is influenced by the substrate. Few species, so far knownonly for the Lake Prespa, could be found on both sides. Diatom assemblages atlarger depths were dominated by taxa of the C. ocellata complex, as well as byspecies with heavily silicified valves as Diploneis mauleri (BRUN) CLEVE,

Table I . Measured physico-chemical parameters in Lake Prespa. Average values (June-May) ± 1 s.d.

Parameter

pHO2 (mg/L)

1.13Sccchi depth

(cm)NO., (mg/L)N02 (mg/L)NH< (mg/L)N- org. (mg/L)Total N (mg/L)Total P (Mg/L)

SO4 (mg/L)

Na (mg/L)K (mg/L)Ca (mg/L)

Mg (mg/L)Cu (Mg/L)

Fe (Mg/L)

Tl-Stenje

8.36 + 0.429.78+ 1.15

266.25± 110.15

3.32 + 3.780.04 + 0.060.18 + 0.141.66 ±0.951.84 + 1.00

16.49+ 13.0729.48+ 8.04

5.06 ±1.211.20 ±0.44

37.93+ 17.28

6.54 ±3.102.65 ± 0.78

3.53+ 1.4757.51

± 30.57

T2-Oteshevo

8.34 + 0.399.69 + 0.92

259.17± 133.52

2.76 + 2.460.04 + 0.070.17 + 0.112.00+1.052.17 ±1.09

14.65+ 8.4027.37±7.85

4.95 + 1.661.31 ±0.55

37.86+ 17.43

7.77 + 2.342.78 ±1.82

3.98±2.2458.82

+ 32.52

T3-Sirhan

8.33 + 0.559.68 + 1.05

261.25±138.86

2.79 + 2.260.04 + 0.070.22 + 0.111.55 ± 1.211.77 ±1.23

12.05±6.0529.93

+ 14.444.93 ±1.701.13 ±0.57

27.97±15.19

6.27 ± 2.952.49+ 1.10

4.62±3.1548.87

± 19.90

T4-Perovo

8.29 + 0.369.55 + 0.93

284.00+ 140.44

2.68 + 2.370.03 + 0.030.27 + 0.211.74+1.242.01 + 1.31

12.03±9.3126.94+ 8.81

4.87 ±1.521.00 + 0.48

37.19± 17.72

6.12 + 3.233.16 ±1.22

4.61±4.2748.35

+ 26.52

T5-Asamati

8.25 + 0.369.63 + 1.33

308.33± 122.89

4.38 + 5.290.04 + 0.050.25 + 0.141.29 ±1.081.53 ±1.03

15.24±8.7832.86±8.22

5.43 ± 2.331.25 ±0.66

52.27± 14.36

6.56 ±2.322.69 + 0.98

2.72±1.0948.46

± 33.73

T6-Pretor

8.29 + 0.419.81 + 1.16

302.92+ 128.11

3.77 + 3.030.03 + 0.040.23 + 0.161.99 ±1.622.22 ±1.58

16.77± 16.0727.93+ 9.77

5.33 ±0.811.24 ±0.40

39.82±21.79

7.15 + 2.683.19± 1.49

10.05±20.1953.75

+ 40.50

T7-Pelagial

8.35+0.419.72 + 1.10

275.00+ 123.97

3.12 + 2.570.04 + 0.050.16 + 0.091.46 + 0.671.69 + 0.91

11.71±7.9330.94±8.12

5.32 ±0.711.22 + 0.31

36.00+ 19.11

7.52 ±1.952.60+1.02

3.73+ 2.2944.43

±31.09

T8- T9- T10-Konjsko Golem Dolno

Grad Dupeni

8.34 + 0.42 8.36 + 0.44 8.41+0.529.86 + 1.38 10.00 + 1.33 9.77 + 1.24

285.00 291.67 280.42+ 115.55 ±138.90 ±133.27

3.31+2.46 2.89 + 3.18 3.64 + 3.820.03 + 0.04 0.02 + 0.02 0.04 + 0.060.30 + 0.24 0.18 + 0.15 0.22 + 0.161.57 ±1.01 1.37 + 0.89 2.10±1.301.70 + 1.07 1.54 ±0.99 2.14+1.24

9.72 10.89 15.55+ 9.08 ± 9.05 ± 17.6529.44 29.55 34.36+ 8.79 + 8.54 + 14.69

5.19 ±1.22 5.31+0.69 4.89+1.751.18 ±0.19 1.07 + 0.37 1.58 + 1.87

39.09 43.33 40.58±16.48 ±15.75 +18.13

7.43 ±1.92 7.50 ±1.68 7.67 + 2.732.35 + 0.88 2.33 ±0.68 2.62 ±1.02

3.52 3.39 12.58±2.13 ±1.75 ±30.8846.69 43.98 37.23

±33.92 +22.68 ±15.70

Tll-Nakolec

8.35 + 0.559.74+ 1.25

273.50+ 127.24

3.44 + 3.410.03 + 0.040.21+0.141.90 + 1.072.07 + 1.06

9.60±6.0931.07±6.56

5.14 + 0.991.28 ±0.73

37.64± 19.06

6.97 ±2.172.73 + 1.37

14.37±29.5335.14

+ 13.82

T12-Krani

8.32 + 0.4410.01 +

301.83± 136.41

3.34 + 2.690.04 + 0.040.28 + 0.261.88 + 1.192.12+1.28

12.74+ 10.4230.29+ 7.45

5.55 + 0.681.19 ±0.28

36.23±17.15

7.41 ± 1.812.68 ± 0.83

3.73+ 2.6349.19

±38.01

Ecology of

CD33-Q.

oms from

ST(0^qO

(Du>•ao>

vlacedon

£.

«i

76 Z. LEVKOV et al.

PNEX

APED

NROT

NSROT ACCB

cscu 12PBAL

11

10

CJUR

GDEC* *COCE *NSUAPSBR

3 NVCAL

.O

NPTR

NPRENKRS* i

Fig. 2. DCA ordination biplot between relative abundance of 17 diatom taxa and12 sampling sites.

Campylodiscus noricus EHRENBERG, Cymatopleura elliptica (BREBISSON)W. SMITH and Navicula hastata JURILJ.

DCA ordination biplots show the distribution of the main diatom taxa accord-ing to their different relative abundances between sampling stations (Fig. 2) andmonths (Fig. 3). No general trend can be inferred from the species/stationsgraphic (Fig. 2). ANOVA analysis showed no significant differences betweenthe values of the physico-chemical variables measured in the different samplingstations (F = 0.87, p = 0.88); however, significant differences were found in di-atom abundances for 14 out of 17 taxa analyzed, thus suggesting the presence ofan additional, unmeasured variable responsible for such differences. A trend to-wards seasonal distribution of points can be found in the species/months biplot(Fig. 3). Species such as Nitzschia subacicularis HUSTEDT, Cyclotella sp. 1 orDiploneis mauleri seem to be associated to winter-spring months, while Navi-cula rotunda, N. subrotundata and Pseudostaurosira brevistriata (GRUNOW)D. M. WILLIAMS et ROUND are plotted associated with summer samples (June,July).

Statistically significant differences were found between the abundances ofeight diatom taxa and 14 physico-chemical variables regarding month of sam-pling CCA biplot (Fig. 4) shows graphically the relationships between diatomassemblages and environmental factors. The eigenvalues of the first two axes

Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) 77

May

DMAU•

NSUA«CJUR Dec

« OMar

OFeb

NVCAL

NPRE

GDEC

NPTR*Oct

PBALPNEX

! CSCU

COCE

NKR?

NovAug

Sep

ACCB.

NROT

NSROTJul

Jun

PSBR

•APED

Fig. 3. DCA ordination biplot between relative abundance of 17 diatom taxa and12 months (from June 2002 to May 2003).

are 0.046 and 0.022, explaining only 6.1 % and 3.0 % of the cumulative varianceof the species dataset, respectively. The sum of all canonical eigenvalues was0.131; however, Monte Carlo permutation tests of significance for the first andalso for all canonical axes (199 unrestricted permutations) were significant(p<0.05). The diatom-environment correlations for CCA axes 1 (0.550) and 2(0.484) were also significant, indicating a relatively strong relation between di-atoms and the measured environmental variables.

According to the CCA results (Fig. 4), physico-chemical variables were themain factors controlling diatom ecology in Lake Prespa. The main variables in-fluencing species distribution and abundances were ammonium and metalliccations (Cu, Mn, K); the secondary variables were, in turn, dissolved oxygen andSecchi depth. Strong colinearity was found within some of the variable sets (e.g.Cu-K-Mn, Mg-SCvC^). The concentration of Cu was significantly correlated tothe relative abundance of 10 out of 17 diatom taxa analyzed, and also affectedspecies diversity (Shannon's index, Pearson's R = 0.2, p = 0.01). Except for NFLtconcentration, variables related to water trophic status ([P], [N], [Norg]) seem tohave a negligible effect on benthic diatom abundances in Prespa Lake. Phospho-rus concentration was only correlated negatively to the abundance of Nitzschiasubacicularis (Pearson's R = 0.2, p = 0.02). The minimal environmental variableset explaining significantly (p <0.05) the variance in the diatom data was identi-fied using the forward-selection option of CCA. Four variables were extracted:concentrations of NH4 (p = 0.005), Fe (p = 0.04), O2 (p = 0.04) and Cu (p = 0.05).

78 Z. LEVKOV et al.

Fig. 4. CCA biplot. Relationships between diatom assemblages and environmental fac-tors.

Discussion

Benthic communities in the Lake Prespa were characterized by a high diversity,which is in accordance with other studies carried out in ancient lakes (MEISTER1913, SKVORTZOW 1936, HUSTEDT 1945, JURILJ 1954, COCQUYT 1998). The di-versity is generally higher in littoral than in sublittoral or deep zones of theselakes, presumably due to higher ecological diversity in shallow zones (MARTENS1997).

One of the most abundant species in bottom samples of Lake Prespa is Cy-dotella ocellata. It was observed in almost all samples from different depths(0.5-18 m). Observations of live material show that the cells even at largerdepths still possess plastids (typical discoid plastids in large number). Similarfindings were recorded by JURILJ (1954) for C.fottii HUSTEDT, which is the dom-inant diatom species in the plankton of Lake Ohrid. According to JURILJ (1954),C. fottii was still capable of photosynthesis at the depth of 40-50 m, where thelight intensity was lower than 1 %.

Another important feature is that in our samples, the population of Cyclotellaocellata was characterized by large-sized vegetative cells, with diameters of

Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) 79

Table 2. Correlation matrix between main benthic diatom species abundances and se-lected chemical variables in Lake Prespa. Pearson's R values shown, p-values in italics.Significant correlations (p < 0.05) in bold. Ha = Shannon's diversity a.

ACCB

APED

CSCU

CJUR

COCE

DMAU

GDEC

NKRS

NPTR

NPRE

NROT

NSROT

NVCAL

NSUA

PBAL

PNEX

PSBR

Ha

[TP]

0,070,410,100,23

-0,010,890,020,81

-0,050,58

-0,020,79

-0,050,550,040,620,080,37-0,140,77

-0,080,330,110,79-0,020,83-0,200,020,000,97

-0,070,42

-0,020,810,000,95

[TN]

-0,060,460,110,20

-0,080,32-0,090,520,080,36

-0,020,84

-0,030,750,070,440,090,270,130,720,040,660,170,050,050,59

-0,210,010,210,010,160,060,160,050,160,06

[K]

0,080,330,200,02-0,030,74

-0,210,01

-0,130,72

-0,190,030,090,270,030,72

-0,010,94

-0,020,78-0,020,550,090,290,080,52-0,230,010,100,240,220,010,130,140,090,28

[Cu]

0,150,070,190,020,140,09

-0,190,03

-0,200,02

-0,200,020,120,770,070,450,170,050,050,560,110,180,210,010,120,76-0,280,000,250,000,200,020,200,020,210,01

Secchi depth

-0,040,67

-0,010,57

-0,060,470,040,670,050,560,130,72-0,110,20

-0,090,50

-0,140,09

-0,140,09

-0,060,47

-0,100,25

-0,080,550,220,01-0,220,01-0,250,00

-0,070,40-0,150,05

6-36 urn. These cells have a morphology and ul(restructure similar to other pop-ulations, except for a larger valve size. Similar valve sizes in C. ocellata wereobserved in Hovsgol, Mongolia (EDLUND et al. 2003). According to EDLUND &STOERMER (1991) species with larger valve sizes can be found in oligotrophicconditions, compared to those in waters under anthropogenic influence. Thiscould be a result of several main factors such as (i) oligotrophy of these lakes;

80 2. LEVKOV et al.

(ii) larger gametangial and initial cell cardinal point size and (iii) evolutionaryprocesses (EDLUND et al. 2003). Thus, species with smaller valve sizes could bethe result of increased nutrient concentration in lakes, because they are morecompetitive in using nutrients (STOERMER et al. 1989).

Despite the recent anthropogenic introduction of large amounts of phospho-rus in the Lake Prespa, this element seems to be stabilized in the bottom sedi-ments, since the water remained oligotrophic throughout the present study(maximal concentration: 65.3 ug.H). This situation contrasts with the eu-trophic conditions observed in former years (LEVKOV, obs. pers.). For that rea-son, phosphorus does not seem to have affected substantially the abundances ofthe studied diatom taxa. Meanwhile, statistical analyses showed that the fre-quency of several species correlated significantly with the concentrations ofNH4 and Cu. Ammonium and copper are known to be main toxicants for fresh-water diatoms (STEEMANN NIELSEN & WIUM-ANDERSEN 1971, HURLIMANN &SCHANZ 1993), but their range of tolerance is very wide (RuGGiu et al. 1998) andthe concentrations found in our survey (maximal concentrations: 0.9 and8.25 ug.H respectively) did not reach the critical values reported in the litera-ture. Hence, diatom species in the present study seem to have increased or de-creased in relative abundance according to their respective autoecological op-tima regarding these pollutants. SNYDER et al. (2002) found that relatively highconcentrations of ammonium are related to an increased diatom diversity, as itwas found in the present work (Table 2).

In conclusion, the pattern of high diatom diversity generally reported for an-cient lakes is also true in Lake Prespa. Our results support the hypothesis thatchemical variables are the main factors controlling the composition of the ben-thic diatom communities in this ecosystem. Additionally, it can be said that, un-der low trophic conditions, other parameters, such as the low concentrations ofpotential pollutants, can be responsible for the differential abundances of diatomtaxa. Further studies will help in determining the causes of the dissimilaritiesfound between sampling stations.

Acknowledgements

Authors are grateful to A. Oliveira for her assistance in English improvements.

ReferencesANOVSKI, T., KOLANECI, M., MILEVSKI, J., RISTEVSKI, P. & STAMOS, A. (2001): Hydrologi-

cal aspects and water balance of Prespa Lakes. - In: ANOVSKI, T. (Ed.): Progress inStudy of Prespa Lake Using Nuclear and Related Techniques, p. 55-66, Skopje.

APHA (1985): Standard Methods for the Examination of Water and Wastewater. - 16thEd. 1266 pp, American Public Health Association, Washington.

BATE, N. & NEWALL, P. (1998): The development of techniques for the use of diatoms inwater quality assessment: How many valves? - In: JOHN, J. (Ed.): Proceedings of 15thInternational Diatom Symposium, p. 153-160. Perth.

CHAVKALOVSKI, I. (1997): Hydrology of Prespa lake. - In: GJIKNURI, L., MIHO, A. &SHUMKA S. (Eds): Proceedings of International Symposium Towards Integrated Con-

Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) 81

servation and Sustainable Development of Transboundary Makro and Micro PrespaLakes, p. 9-14, Korea.

CHAVKALOVSKI, I. (2000): Anthropogenic influence on the denivelation of Makro andMikro Prespa Lake. - In: GRUPCE, Lj. & KUNGULOVSKI, Dz. (Eds): Proceedings of In-ternational Symposium Sustainable Development of Prespa Region, p. 250-257, Ote-shevo.

CHEREPANOVA, M.V. & BRIGHAM-GRETTE, J.K. (2001): Quaternary high-resolution di-atom stratigraphy of pelagic sediments of El'Gygytgyn Lake of Chukotka, site PG1351. - El'Gygytgyn Lake Workshop Report. Science Results and Plans for DeepDrilling International Continental Drilling Program (ICDP), p. 29-30, University ofMassachusetts, Amherst.

COCQUYT, C. (1998): Diatoms from the Northern Basin of Lake Tanganyika. - Biblio-theca Diatomologica 39: 1-275.

EDLUND, M.B. & STOERMER, E.F. (1991): Sexual reproduction in Stephanodiscus nia-garae (Bacillariophyta). - Journal of Phycology 27: 780-793.

EDLUND, M. B., WILLIAMS, R. M. & SONINKHISHIG, N. (2003): The planktonic diatom di-versity of ancient Lake Hovsgo'l, Mongolia. - Phycologia 42: 232-260.

FISKE, C. A. & SUBBAROW, Y. (1925): The colorimetric determination of phosphorus. - J.Biological Chemistry 66: 357-400.

GENKAL, S. I. (2003): New data on Bacillariophyta of Lake Biwa (Japan). - InternationalJournal on Algae 5: 26-36.

GRUPCE, Lj. (1997): Autochthonous and allochthonous quantities of phosphorus inPrespa lake waters. - In: GJIKNURI, L., MIHO, A. &. SHUMKA, S (Eds): Proceedings ofInternational Symposium Towards Integrated Conservation and Sustainable Develop-ment of Transboundary Makro and Micro Prespa Lakes, p. 68-72, Korea.

HURLIMANN, J. & SCHANZ, F. (1993): The effects of artificial ammonium enhancement onriverine periphytic diatom communities. -Aquatic Sciences 55: 40—64.

HUSTEDT, F. (1945): Diatomeen aus Seen und Quellgebieten der Balkan-Halbinsel. -Archiv fur Hydrobiogie 40: 867-973.

JURILJ, A. (1954): Flora i vegetacija dijatomeja Ohridskog Jezera (Flora and vegetation ofdiatoms of Ochrida Lake). - Prirodoslovnih Istrazivanja 26: 99-190.

KOZAROV, G. (1959): Phytoplankton of Lake Prespa. - Recueil des Travaux de la StationHydrobiologique d'Ohrid 7: 1-13.

- (1960): The phytoplankton investigations in Lake Prespa during the course of threeyears. - Recueil des Travaux de la Station Hydrobiologique d'Ohrid 8: 1-57.

KRAMMER, K. & LANGE-BERTALOT, H. (1986): Bacillariophyceae. 1. Teil: Naviculaceae.- In: ETTL, H., GERLOFF, J., HEYNIG, H. & MOLLENHAUER, D. (Eds): SuBwasserfloravon Mitteleuropa 2/1. 876 pp., Gustav Fischer Verlag, Stuttgart.

LEVKOV, Z. (2005): Taxonomy and Ecology of Diatoms from Lake Prespa and St. NaumSprings. - 731 pp. PhD Thesis, Faculty of Natural Sciences, Skopje.

LEVKOV, Z., KRSTIC, S., METZELTIN, D. & NAKOV, T. (2006a): Diatoms from LakesPrespa and Ohrid. - Iconographia Diatomologica 16: 1-603.

LEVKOV, Z., KRSTIC, S. & NAKOV, T. (2003): Diversity of diatom microflora of LakePrespa - preliminary results. - In: MELOVSKI, Lj. (Ed.): Proceedings of 2nd Congressof Ecologists of Republic of Macedonia, p. 443-449, Ohrid.

LEVKOV, Z., NAKOV, T. & METZELTIN, D. (2006b): New species and combination fromgenus Sellaphora MERESCHKOWSKY (Bacillariophyceae) from Macedonia. - DiatomResearch 21: 297-312.

MARTENS, K. (1997): Speciation in ancient lakes. -Tree 12: 177-182.MEISTER, F. (1913): Beitrage zur Bacillarienflora Japans. -Archiv fur Hydrobiologie 8:

305-312.MITICH, V. & NAUMOVSKI, T. (2000): Physico-chemical and biological investigations of

littoral region of Lake Prespa. - In: GRUPCE, Lj. & KUNGULOVSKI, • (Eds): Proceed-ings of International Symposium Sustainable development of Prespa region, p. 66-71,Oteshevo.

MOORE, P. & CHAPMAN, S. (1986). Methods in Plant Ecology. - 590 pp., Blackwell Sci-ence Publications, Oxford.

82 Z. LEVKOV et al.

NAUMOVSKI, T. B., NOVEVSKA, V. R., LOKOSKA, S. L. & MITICH, V. S. (1997): Trophicstate of Prespa lake. - In: GJIKNURI, L., MIHO, A. & SHUMKA S. (Eds): Proceedings ofInternational Symposium: Towards Integrated Conservation and Sustainable Devel-opment of Transboundary Makro and Micro Prespa Lakes, p. 132-137, Korea.

RUGGIU, D., LUGLIE, A., CATTANEO, A. & PANZANI, P. (1998): Paleoecological evidencefor diatom response to metal pollution in Lake Orta (N. Italy). - Journal of Paleolim-nology 20: 333-345.

SHUMKA, S. (1994): Annual dynamics of zooplankton in Lake Prespa. - 200 pp. MSciThesis, Faculty of Natural Sciences, Skopje.

SKVORTZOW, B. W.. (1936): Diatoms from Biwa Lake, Honshu Island, Nippon. - Philip-pine Journal of Sciences 61: 253-296.

SNYDER, E. B., ROBINSON, C. T, MINSHALL, W. & RUSHFORTH, S. R. (2002): Regionalpatterns in periphyton accrual and diatom assemblage structure in a heterogeneousnutrient landscape. - Canadian Journal of Fisheries and Aquatic Sciences 59:564-577.

STEEMANN NIELSEN, E. & WIUM-ANDERSEN, S. (1971): The influence of Cu on photosyn-thesis and growth in diatoms. - Physiologia Plantarum 24: 480-484.

STEVENSON, A. C. & FLOWER, R. J. (1991): A palaeoecological evaluation of environmentaldegradation in Lake Mikri Prespa, NW Greece. - Biological Conservation 57: 89-109.

STOERMER, E. F, EMMERT, G. & SCHELSKE, C. L. (1989): Morphological variation ofStephanodiscus niagarae EHRENB. (Bacillariophyta) in a Lake Ontario sediment core.- Journal of Paleolimnology 2: 227-236.

TER BRAAK, C. J. F. & SMILAUER, P. (2002): CANOCO reference manual and CanoDrawfor Windows user's guide. Software for Canonical Community Ordination (version4.5), Biometrics, Wageningen, NL.

TRPESKI, V., SPIROVSKI, J., STOJANOVA, M., DAMEVSKI, K. & KOCEVSKI, V. (2000): Resultsfrom researches of some soil characteristics, application of mineral fertilizations inPrespa region and steps for protection of life environment. - In: GRUPCE, Lj. & KUN-GULOVSKI, Dz. (Eds): Proceedings of International Symposium Sustainable develop-ment of Prespa region, p.200-209, Oteshevo.

Manuscript received May 19, 2006, accepted February 6, 2007.

Authors' addresses:ZLATKO LEVKLOV,SVETISLAV KRSTIC,TEOFIL NAKOVInstitute of Biology,Faculty of Natural Sciences,Gazi Baba bb.,1000 Skopje,Republic of MacedoniaE-mail: [email protected] Blanco,Area de Ecologia,Universidad de Leon,E-24071 Leon,Spain.Saul Blanco,Luc Ector,Public Research Center- Gabriel LippmannDepartment Environment and Agro-biotechnologies (EVA),41 rue du Brill,L-4422 Belvaux,Grand-Duchy of Luxembourg

Ecology of benthic diatoms from Lake Macro Prespa (Macedonia) 83

List of acronymsACCB - Achnanthes devei var. balcanica HUSTEDTAPED - Amphora pediculus (KOTZINO) GRUNOWCSCU - Cavinula scutelloides (W. SMITH) LANGE-BERTALOTCJUR - Cyclotella sp. 1.COCE - Cyclotella ocellata PANTOCSEKDMAU - Diploneis mauled (BRUN) CLEVEGDEC - Geissleria decussis (0STRUP) LANGE-BERTALOT ET METZELTINNKRS- Navicula krsticii LEVKOVNPTR - Navicula petwvskae LEVKOV et KRSTICNPRE - Navicula prespanensis LEVKOV et METZELTINNROT - Navicula rotunda HUSTEDTNSROT - Navicula subwtundata HUSTEDTNVCAL - Navicula viridulacalcis LANGE-BERTALOTNSUA - Nitzschia subacicularis HUSTEDTPB AL - Placoneis balcanica (HUSTEDT) LANGE-BERTALOT, METZELTIN et LEVKOVPNEX - Placoneis neoexigua LANGE-BERTALOT et MIHOPSBR - Pseudostaurosira brevistriata (GRUNOW) D.M. WILLIAMS et ROUND