TEOFIL NAKOV and Luc EciOR3. 11nstitute of Biology, Faculty of Natural Sciences, Skopje,. Republic of Macedonia. 2Area de Ecologi'a, Universidad de Leon, ...
Algological Studies 124
71-83
Stuttgart, July 2007
Ecology of benthic diatoms from Lake Macro 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, 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 characterized 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 performed on 12 sampling sites of Lake Macro Prespa. About 300 diatom taxa were identified 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 distribution and abundances were ammonium and metallic cations (Cu, Mn, K) and, secondarily, 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
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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 freshwaters, one of these ecosystems is Lake Prespa (Macedonia). It belongs to a group of ancient lakes located in a tectonic valley between Mountains Galicica and 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 in the second half of the 20th century. The high abundance of Cyclotella ocellata PANTOCSEK throughout the core suggests that this lake is little affected by increased nutrient loadings. Studies on Lake Prespa diatoms confirm the dominance of C. ocellata in plankton and benthos (MiTicn & NAUMOVSKI 2000, LEVKOV 2005). However, few studies on plankton assemblages have been carried out (KOZAROV 1959, 1960), while investigations on benthic diatoms were oriented mainly on taxonomy and distribution (HUSTEDT 1945, LEVKOV et al. 2003, LEVKOV 2005). Former taxonomical studies showed the presence of several rare and endemic taxa (LEVKOV et al. 2006a, b), but data for their ecological preferences are still lacking. This article is the first attempt to determine the ecological characteristics 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 and Baba at 853 m a.s.l. The total surface area is 274 km2, and the maximal depth is 54.2 m, with a total catchment area of 1095.22 km2 (CHAVKALOVSKI 1997). Its bottom is mainly covered with organic sediment that enables intensive macrophyte development during the summer period. There is no natural surface water outlet, and large amounts of water are discharged through underground channels into 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 and usage of lake waters, resulted in a decrease of the water level by 7.8 m compared to 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 use for different human purposes, mainly irrigation and water supplies. According to ANOVSKJ et al. (2001), three possible natural factors are usually involved in decreasing the water level (i) tectonic falling of the lake bottom; (ii) widening of underground channels connecting the two lakes and (iii) influence of meteorological parameters. Such a decrease of the water level in the early nineties lead to changes in water quality. According to NAUMOVSKI et al. (1997), the waters of Lake Prespa in that period varied between oligotrophic and mesotrophic, while SHUMKA (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 Macro Prespa.
gations (LEVKOV 2005) showed that Lake Prespa is eutrophic during summer, with blooms of blue-green algae. According to GRUPCE (1997), about half of the phosphorus input in the lake (542.36 tons P2O$ per year) has an anthropogenic origin. The most important sources of phosphorus in Lake Prespa are untreated communal wastewater and fertilizers used in the region (TRPESKI et al. 2000). 2. Methodology Water samples from Lake Prespa were collected between June 2002 and May 2003 at 12 sampling sites (Fig. 1) located between 50 and 200 m from the shore, depending on bottom topography. Temperature, pH, dissolved oxygen concentration, and Secchi depth were measured directly in the field with appropriate equipment. Samples for chemical analyses were conserved in HgCh and trans-
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ported in a refrigerator at 4° C. Chemical analyses were performed following the
procedures of APHA (1985), MOORE & CHAPMAN (1986) and FISKE & SUBBAR-
ROW (1925). Average values and standard deviation of measured physico-chemical parameters are given in Table 1. Benthic diatoms were collected with a Van Veen bottom sampler on various depths. In most of the cases samples were taken from a depth between 2 m and 4 m, except for the pelagial zone where samples from 18m were collected. Prior to fixation with 4% formalin, live samples were observed (LEVKOV et al. 2006b). Diatom slides were prepared by acid digestion (KRAMMER & LANGE-BERTALOT 1986) and mounted in Naphrax®. The slides are deposited in the Diatom Collection 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 the whole dataset were used in multivariate analyses. Diatom abundances were arcsine square root transformed and the environmental variables, except pH, were log-transformed due to their skewed distributions. Differences in diatom abundances and physico-chemical variables between samples were studied by means of ANOVA. Detrended Correspondence Analysis (DCA) was carried out to explore the relationships between diatom taxa and sampling stations and months. Canonical Correspondence Analysis (CCA) was used to relate the diatom assemblages to environmental factors. All ordinations were run using the computer 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 had abundances higher than 1 % in at least one sample. The greatest difference in diatom composition between the eastern and the western coast was observed in the littoral zone. The bottom of the west coast (from Stenje village to Perovo village) was covered with organic sediment. The dominant diatom species Cavinula scutelloides (W. SMITH) LANGE-BERTALOT, Navicula rotunda HUSTEDT, N. subrotundata HUSTEDT, Amphora pediculus (KuTZlNG) GRUNOW, and characteristic species of the two genera Aneumastus and Sellaphora were frequent in the benthic communities. Additionally, this part of the lake shore consists of calcareous 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 a mixture of sand and organic sediment. In this region, several Navicula sensu stricto species are sub-dominant (LEVKOV 2005). It is supposed that the distribution of these species is influenced by the substrate. Few species, so far known only for the Lake Prespa, could be found on both sides. Diatom assemblages at larger depths were dominated by taxa of the C. ocellata complex, as well as by species 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
Tl-
Stenje
T2Oteshevo
T3Sirhan
T4Perovo
T5-
T6-
Asamati
Pretor
T7Pelagial
T8Konjsko
T9Golem Grad
T10Dolno Dupeni
TllNakolec
T12Krani
266.25 ± 110.15 3.32 + 3.78 0.04 + 0.06 0.18 + 0.14 1.66 ±0.95 1.84 + 1.00 16.49 + 13.07 29.48 + 8.04 5.06 ±1.21 1.20 ±0.44 37.93 + 17.28 6.54 ±3.10 2.65 ± 0.78 3.53 + 1.47
1.13
SO4 (mg/L) Na (mg/L) K (mg/L) Ca (mg/L) Mg (mg/L) Cu (Mg/L)
Fe (Mg/L)
57.51 ± 30.57
259.17 ± 133.52 2.76 + 2.46 0.04 + 0.07 0.17 + 0.11 2.00+1.05 2.17 ±1.09 14.65 + 8.40 27.37 ±7.85 4.95 + 1.66 1.31 ±0.55 37.86 + 17.43 7.77 + 2.34 2.78 ±1.82 3.98 ±2.24 58.82 + 32.52
261.25 ±138.86 2.79 + 2.26 0.04 + 0.07 0.22 + 0.11 1.55 ± 1.21 1.77 ±1.23
12.05 ±6.05 29.93 + 14.44 4.93 ±1.70
1.13 ±0.57 27.97 ±15.19 6.27 ± 2.95 2.49+ 1.10 4.62 ±3.15 48.87
± 19.90
284.00 + 140.44 2.68 + 2.37 0.03 + 0.03 0.27 + 0.21 1.74+1.24 2.01 + 1.31 12.03 ±9.31 26.94 + 8.81 4.87 ±1.52 1.00 + 0.48 37.19 ± 17.72 6.12 + 3.23 3.16 ±1.22 4.61 ±4.27 48.35 + 26.52
308.33 ± 122.89 4.38 + 5.29 0.04 + 0.05
0.25 + 0.14 1.29 ±1.08
1.53 ±1.03 15.24
302.92 + 128.11 3.77 + 3.03 0.03 + 0.04 0.23 + 0.16 1.99 ±1.62 2.22 ±1.58
275.00 + 123.97 3.12 + 2.57 0.04 + 0.05 0.16 + 0.09 1.46 + 0.67
16.77
11.71
285.00 291.67 280.42 273.50 + 115.55 ±138.90 ±133.27 + 127.24 3.31+2.46 2.89 + 3.18 3.64 + 3.82 3.44 + 3.41 0.03 + 0.04 0.02 + 0.02 0.04 + 0.06 0.03 + 0.04 0.30 + 0.24 0.18 + 0.15 0.22 + 0.16 0.21+0.14
301.83 ± 136.41 3.34 + 2.69 0.04 + 0.04 0.28 + 0.26
1.57 ±1.01 1.37 + 0.89 2.10±1.30 1.90 + 1.07 1.88 + 1.19 1.69 + 0.91 1.70 + 1.07 1.54 ±0.99 2.14+1.24 2.07 + 1.06 2.12+1.28
± 16.07 ±8.78 ±7.93 30.94 32.86 27.93 ±8.12 ±8.22 + 9.77 5.43 ± 2.33 5.33 ±0.81 5.32 ±0.71 1.25 ±0.66 1.24 ±0.40 1.22 + 0.31 36.00 52.27 39.82 ±21.79 + 19.11 ± 14.36 6.56 ±2.32 7.15 + 2.68 7.52 ±1.95 2.69 + 0.98 3.19± 1.49 2.60+1.02 2.72 3.73 10.05 + 2.29 ±1.09 ±20.19 44.43 48.46 53.75 ± 33.73 + 40.50 ±31.09
9.72
10.89
15.55
9.60
12.74
+ 9.08 29.44
± 9.05 29.55
± 17.65 34.36
±6.09
+ 10.42 30.29
+ 8.54
+ 14.69
+ 8.79
5.19 ±1.22
1.18 ±0.19 39.09 ±16.48
7.43 ±1.92 2.35 + 0.88
3.52 ±2.13 46.69 ±33.92
31.07
±6.56 + 7.45 5.31+0.69 4.89+1.75 5.14 + 0.99 5.55 + 0.68 1.07 + 0.37 1.58 + 1.87 1.28 ±0.73 1.19 ±0.28 37.64 36.23 43.33 40.58 ±17.15 ±15.75 +18.13 ± 19.06 7.50 ±1.68 7.67 + 2.73 6.97 ±2.17 7.41 ± 1.81 2.33 ±0.68 2.62 ±1.02 2.73 + 1.37 2.68 ± 0.83 3.39 12.58 14.37 3.73 + 2.63 ±1.75 ±30.88 ±29.53 35.14 49.19 43.98 37.23 +22.68 ±15.70 + 13.82 ±38.01
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8.36 + 0.42 8.34 + 0.39 8.33 + 0.55 8.29 + 0.36 8.25 + 0.36 8.29 + 0.41 8.35+0.41 8.34 + 0.42 8.36 + 0.44 8.41+0.52 8.35 + 0.55 8.32 + 0.44 9.78+ 1.15 9.69 + 0.92 9.68 + 1.05 9.55 + 0.93 9.63 + 1.33 9.81 + 1.16 9.72 + 1.10 9.86 + 1.38 10.00 + 1.33 9.77 + 1.24 9.74+ 1.25 10.01 +
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APED
PNEX
12
cscu
PBAL
NROT
11 NSROT
ACCB
10
CJUR GDEC*
*COCE *NSUA PSBR
3
NVCAL .O
NPTR NKRS* i NPRE
Fig. 2. DCA ordination biplot between relative abundance of 17 diatom taxa and 12 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 according to their different relative abundances between sampling stations (Fig. 2) and months (Fig. 3). No general trend can be inferred from the species/stations graphic (Fig. 2). ANOVA analysis showed no significant differences between the values of the physico-chemical variables measured in the different sampling stations (F = 0.87, p = 0.88); however, significant differences were found in diatom abundances for 14 out of 17 taxa analyzed, thus suggesting the presence of an additional, unmeasured variable responsible for such differences. A trend towards seasonal distribution of points can be found in the species/months biplot (Fig. 3). Species such as Nitzschia subacicularis HUSTEDT, Cyclotella sp. 1 or Diploneis mauleri seem to be associated to winter-spring months, while Navicula 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 of eight diatom taxa and 14 physico-chemical variables regarding month of sampling CCA biplot (Fig. 4) shows graphically the relationships between diatom assemblages and environmental factors. The eigenvalues of the first two axes
Ecology of benthic diatoms from Lake Macro Prespa (Macedonia)
77
NVCAL NPRE
May DMAU
GDEC •
NPTR *
NSUA «CJUR Dec « O Mar O
PBAL
PNEX
Oct !
CSCU
Feb
COCE NKR?
Jun
NROT
Nov Aug
NSROT
Sep
Jul
ACCB.
•APED
PSBR
Fig. 3. DCA ordination biplot between relative abundance of 17 diatom taxa and 12 months (from June 2002 to May 2003).
are 0.046 and 0.022, explaining only 6.1 % and 3.0 % of the cumulative variance of the species dataset, respectively. The sum of all canonical eigenvalues was 0.131; however, Monte Carlo permutation tests of significance for the first and also for all canonical axes (199 unrestricted permutations) were significant (p
