Hydrobiologia 438: 25–41, 2000.
P.B. Hamilton, H. Kling & M.T. Dokulil (eds), Cyanoprokaryotes and Chlorophytes across Lake Trophic States.
© 2000 Kluwer Academic Publishers. Printed in the Netherlands.
25
Planktic green algae of Bulgarian coastal wetlands
Maya P. Stoyneva
Sofia University, Faculty of Biology, Departament of Biology, 8 Bld. Dr. Zankov, BG-1421 Sofia, Bulgaria
E-mail: mstoynev@techno-link.com
Received 12 December 1999; accepted 15 July 2000
Key words: green algae, phytoplankton, trophic state, coastal wetlands
Abstract
The present paper reports on the contribution of green algae to the phytoplankton community structure in 13 euto hypertrophic Bulgarian coastal wetlands which were different in morphometry and salinity. The results obtained
revealed the important role of green algae, which formed 43% of the total species composition, 18% of numbers
and 21% of biomass and often had a dominant or subdominant role in phytoplankton community structure.
Introduction
Green algae (Chlorophyta) comprise a characteristic
part of the phytoplankton community in all types of
lakes and in small eu- to hypertrophic water bodies (Reynolds, 1984; Happey-Wood, 1988; Olrik,
1994). In most of the reported studies, almost all
qualitatively and quantitatively important green algae belong to Chlorococcales (e.g. Hecky & Kling,
1981; Krienitz & Scheffler, 1994; Padisák & Dokulil,
1994; Trifonova, 1998). Zygnemophytes often occur
in insignificant amounts but notable development of
desmids has been detected (Nauwerck, 1963; Dokulil, 1979; Sommer, 1981; Reynolds, 1984; Coesel
& Kooijman-Van Blockland, 1991; Barone & Naselli
Flores, 1994; Tremel, 1996; Spijkerman & Coesel,
1998). Likewise, some filamentous tychoplanktonic
green algae can successfully compete against true
planktonic forms in acidified shallow soft-water lakes
(Olrik & Sörensen, 1994). Green flagellates also
play an important role in phytoplankton of various
natural water bodies (Kisselev, 1980; Olrik, 1994).
These flagellates are common in temperate and cold
regions (Olrik, 1994; Izaquirre et al., 1998), particularly during periods of lower light intensity and lower
temperature (Ramberg, 1979; Dokulil, 1979). Many
representatives of this group, as well as other green
algae, including chlorococcales and zygnemophytes
are highlighted as important species in habitats with
a broad spectrum of salt content (Hammer et al., 1983;
Olrik, 1994).
However, there are gaps in our knowledge about
the detailed species composition and phytoplankton
succession in various water bodies even from some
temperate European regions. Such a region is the
Bulgarian Black Sea coastline with a total area of
7420 km2 where are located most of the recent Bulgarian natural water bodies (Michev, 1993). Algological research on these waters started with the work of
Petkoff (1905) although, studies on the phytoplankton
are irregular, scarce and consist mainly in the establishment of floristic lists. A detailed review on the
literature is presented by Stoyneva (in press, a). The
present paper reports a study on the contribution of
green algae to the phytoplankton community structure
in 13 Bulgarian natural coastal wetlands, different in
their morphometry, salinity and trophic state.
Description of sites studied
The main characteristics of the studied coastal wetlands (Figure 1) are presented in Table 1. Some
additional information is provided below. Durankulak (D) is a firth lake. At the end of the 1960s, its
connection with the Black Sea was interrupted by a
dike of carbonate sand. Orlovo Blato (DO) was previously a part of Durankulak Lake. Nowadays, due to
26
Figure 1. Map of Bulgaria with the location of the studied coastal wetlands: 1 – Durankulak Lake; 2 – Orlovo Blato; 3 – Ezeretz; 4 – Shabla;
5 – Shablenska Tuzla; 6 – Atanasovsko Lake; 7 – Poda; 8 – Uzungeren; 9 – Foros Bay; 10 – Alepu; 11 – Arkutino; 12 – Veljov Vir; 13 –
Stamopolu; 14 – Ropotamo River.
Table 1. Main characteristics of the investigated Bulgarian coastal wetlands. Abbreviations: DO – Orlovo Blato; D – Durankulak; E – Ezeretz,
Sh – Shabla; ST – Shablenska Tuzla; Af – freshwater part of Atanasovsko Lake; As – salinas of Atanasovsko Lake; Ac – canal of Atanasovsko
Lake; Al – Alepu; Ar – Arkutino; VV – Veljov Vir; St – Stamopolu; R – Ropotamo River
Date/Sites
DO
Altitude (m a.s.l.)
Total area (ha)
Open water surface (ha)
Maximum depth (m)
Average summer water temperature
(◦ C)
Salinity range ( ‰)
pH
Average annual values of NH4 +
(mg l−1 )
Average annual values of NO3 − +
NO2 − (mg l−1 )
Average annual values of HPO4 3−
(mg l−1 )
Average total phytoplankton
biomass (mg l−1 )
0.5
20
20
1.5
28
D
E
Sh
0.5
0.8
0.8
350
72
79
250
70
72
4
8.5
9.5
26–27 25–26 25–26
ST
Af
As
Ac
Al
Ar
VV
St
R
0.7
19
19
0.8
30
−0.5–1
8
2
1.3
26
−1
1930
1930
0.8
28
−1–1
12
12
1.5
26
0.4
167
164
1
28
0.2
1
36 13.6
36 13.6
0.5 1.2
26 27
0.4
7
7
0.5
28
0–1
1001
1001
3
29
0.6–1.3 0.3–0.4 0.4–0.6 0.5 4–5.3 0.12–0.18 18–280 0.12–169 <0.5 <0.5 <0.5 <0.5 4.1–18.2
8.6
8.8
8.6
8.6
8
7.5–8.8 8.4–8.8 7.4–8.3 6.5–7.6 6.8 7.3 7.9–9.2 8.1–8.5
2.8
2.3
1.5
1.3 3.7
0.39
0.24
0.13
0.5
0.5 0.3
0.2
0.4
0.204
0.104
1.55
0.68 0.59
0.47
0.27
0.13
0.35
0.42 0.18
0.32
4.203
0.12
0.18
0.37
0.52
0.3
0.43
0.15
0.19
0.1
0.012 0.05
0.9
0.15
13.63
7.71
12.4
6.59
6.7
30.53
27.39
10.78
32.82
17.58
80.78 21.16 6.0
27
dike-building, it is separated as an adjacent shallow
marsh with underground influx of Black Sea water.
Both Shabla (Sh) and Ezeretz (E) are firths connected by a narrow, 1–1.6 m deep canal. There was a
small canal between the Black Sea and Shabla-Ezeretz
lake complex, which was filled by sand in the beginning of the 1960s. The closely situated Shablenska
Tuzla lagoon (ST) was previously a well known Bulgarian hyperhaline lagoon (Ivanov et al., 1964) but
now has a salinity of 4–5.3 ‰ depending on influx
of underground freshwater. The wetland Atanasovsko
Lake consists of a system of freshwater bodies (Af)
and salinas (As) connected through lock-links with a
surrounding canal (Ac), which has a lock-link with the
Black Sea. Thus, the salinity of this canal changes
irregularly, but rapidly due to the sluice-opening and
closing in relation with the needs of industrial saltproduction. Poda comprises a system of freshwater
(Pf) and brackish (Pb) small water bodies (maximum
depth – 0.5 m) with an average salinity 3.7 ‰ (Ivanov
et al., 1964) and a crossing canal. It is connected with
the nearby site Uzungeren (PG) and with the Foros
Bay (PF) of Black Sea. The salinity of Foros Bay has
decreased over the last years from 16 ‰ to 6–9 ‰,
depending on the influx from tubes with underground
freshwater (Marinov, pers. com.). The lagoons Alepu
(Al), Arkutiono (Ar) and Stamopolu (St) are separated
from the Black Sea sand strips by asphalt roads and
in this way they are artificially turned into freshwater
marshes. Arkutino marsh recently has become overgrown by Nymphaea alba L. The development of this
macrophyte (though not as abundant as in Arkutino
marsh) is also characteristic of the freshwater Veljov Vir marsh (VV) located nearby at the mouth of
Ropotamo River (R) at the Black Sea.
Materials and methods
The present study was based on the analysis of 378
phytoplankton samples collected in 1995 and 1996.
Additional samples (10) were collected in 1992 and
1994. All samples were collected in plastic bottles
with a volume of 1l and fixed with 2–4% formaline. In some cases, extra samples were fixed with
Lugols’ solution for examination of flagellates. All
determinations and measurements were done almost
immediately after sampling on an Amplival microscope with a magnification up to 1200×. Stoyneva
(1998) described the taxonomic background in detail.
Counting was done across 64 small squares of the
Thoma blood-counting chamber in eight reiterations.
Cells were the main counting unit. Cell numbers were
converted to volumes by reference to the closest volumetric shape. Species were considered as dominant
if they contributed more than 25% to the total biomass, as sub-dominant if they contributed between 20
and 25% and as abundant if the contribution exceeded
0.5% of the total biomass.
Classification of the wetlands studied in relation to
their salinity was based on the Venice-system amended
by den Hartog (1960). The trophic state was evaluated
through the average annual algal biomass (Table 1)
according to the open-boundary OECD system (Vollenweider, 1989). Statistical analyses were made by
TWINSPAN (Hill, 1979) and BIODIV-programme
(Baev & Penev, 1995). Correlations between structural phytoplankton parameters, biomass of dominants, sub-dominants, abundant species and measured
physical and chemical variables of the studied sites
(area, depth, salinity, water temperature, transparency
acc. to Secchi disk, mineralisation (TDS), hardness
(dH), P–PO4 3− , N–NH4 + and SiO2 ) were made and
considered as significant when probability thresholds
were p<0.05.
Results
In total, 569 algal taxa were found and 247 of them
were chlorophytes (Table 2) which contributed notably
to the phytoplankton structure of all studied wetlands
(Figure 2). One hundred and thirty two algal taxa
from various groups were important contributors to
the total phytoplankton biomass and 96 of them were
green algae (Table 2). Chlorococcales were the most
important group of green algae, contributing significantly to the species list (150 Chlorococcales were
recorded) and to total algal biomass. They were often
the most numerically abundant group and contributed significantly to phytoplankton even during the
blooms of cyanoprokaryotes (Stoyneva, in press, a, b).
Generally, Chlorococcales were most important during the summer and autumn periods. On a biomass
basis, nine of them were dominant: Ankistrodesmus
falcatus (PF), Chlorella sp. (Pf), Coelastrum microporum var. octaedricum (Sh), Golenkinia radiata
(Af), Monoraphidium irregulare (VV), Oocystella lacustris (D), Pseudodictyosphaerium lacunare (Sh),
Pseudokirchneriella rotunda (PG) and Scenedesmus
communis (D). Among them, C. microporum var.
octaedricum and O. lacustris also occurred as sub-
28
Figure 2. Average contribution of green algae to the total species composition (S), to the total phytoplankton numbers (N) and to the total
phytoplankton biomass (B) in Bulgarian coastal wetlands. Abbreviations: DO – Orlovo Blato; D – - Durankulak; E – Ezeretz; Sh – Shabla;
ST – Shablenska Tuzla; Af – freshwater part of Atanasovsko Lake; As – salinas of Atanasovsko Lake; Ac – canal of Atanasovsko Lake; Pb
– brackish small water bodies of Poda wetland; Pf – freshwater small water bodies of Poda wetland; PF – Foros Bay; PG – Uzungeren; Al –
Alepu; Ar – Arkutino; VV – Veljov Vir; St – Stamopolu; R – Ropotamo River.
29
Table 2. Distribution of green algal species in Bulgarian coastal wetlands and their contribution to phytoplankton (4 – dominance; 3 –
sub-dominance; 2 – abundance; 1 – occurrence). Abbreviations: DO – Orlovo Blato; D – Durankulak; E – Ezeretz; Sh – Shabla; ST –
Shablenska Tuzla; Af – freshwater part of Atanasovsko Lake; As – salinas of Atanasovsko Lake; Ac – canal of Atanasovsko Lake; Pb –
brackish small water bodies of Poda wetland; Pf – freshwater small water bodies of Poda wetland; PF – Foros Bay; PG – Uzungeren; Al
– Alepu; Ar – Arkutino; VV – Veljov Vir; St – Stamopolu; R – Ropotamo River
Algal taxa/Sites
CHLOROPHYTA
EUCHLOROPHYTINA
Actinastrum hantzschii Lag.
Actinastrum hantzschii Lag. var. subtile Wol.
Ankistrodesmus falcatus (Corda) Ralfs
Ankistrodesmus tortus Hind.
Binuclearia sp. (fragments)
Botryococcus braunii Kütz.
Botryococcus neglectus (W. et G. S. West) Kom.
et Marv.
Bulbochaete sp. (fragments)
Carteria globulosa Pasch.
Carteria sp.
Catenococcus tortuosus Hind.
Chlamydomonas spp.
Chlorella ellipsoidea Gern.
Chlorella neustonica Bourr.
Chlorella sp.
Chlorogonium gracile Matw.
Chlorogonium minimum Playf.
Chlorogonium sp.
Chlorolobion obtusum Kors.
Chloromonas sp.
Choricystis cylindracea Hind.
Cladophora glomerata (L.) Kütz.
Cladophora sp. (fragments)
Closteriopsis acicularis (G. M. Sm.) Bel. et Sw.
Coccomonas sp.
Coelastrum astroideum De-Not.
Coelastrum indicum Turn.
Coelastrum microporum Näg.
Coelastrum microporum Näg. Var. octaedricum
(Skuja) Sodomk.
Coelastrum pseudomicroporum Kors.
Coenochloris polycocca (Kors.) Hind.
Coenococcus planctonicus Kors.
Coenocystis subcylindrica Kors.
Crucigenia fenestrata (Schm.) Schm.
Crucigenia quadrata Morr.
Crucigenia tetrapedia (Kirchn.) W. et G. S. West
Crucigeniella apiculata (Lemm.) Kom.
Crucigeniella rectangularis (Näg.) Kom.
Dangeardinella saltathrix Pasch.
Desmatractum indutum (Geitl.) Pasch.
Dicelulla geminata (Printz.) Kors.
Dictyosphaerium chlorelloides (Naum.) Kom.
et Perm.
D D
O
E
Sh ST
Af As
2
1
2
2
2
1
1
2
1
1
2
1
Ac
Pb Pf
1
PF PG Al
1
1
4
1
Ar VV
1
St
R
1
1
1
1
1
1
1
1
1
3
1
3
1
4
3
3
1
1
3
1
1
3
1
1
3
3
2
3
3
3
2
1
2
1
1
1
3
3
1
1
1
1
2
1
1
1
2
1
2
1
1
1
1
1
1
1
1
1
1
1
1
3
1
1
1
3
3
3
3
1
3
3
3
1
3
3
3
3
3
3
3
4
1
2
2
2
1
2
2
2
3
2
2
2
3
2
1
1
1
1
1
1
1
1
1
1
1
2
3
2
1
2
2
1
3
1
1
2
2
2
2
2
2
1
2
1
2
1
2
2
1
Continued on p. 30
30
Table 2. Continued
Algal taxa/Sites
CHLOROPHYTA
EUCHLOROPHYTINA
Dictyosphaerium elongatum Hind.
Dictyosphaerium pulchellum Wood
Didymocystis inermis (Fott) Fott
Didymogenes palatina Schm.
Diplochloris lunata (Fott) Fott
Dunaliella lateralis Pasch. et Jah.
Dunaliella paupera Pasch.
Dunaliella salina Teod.
Dunaliella viridis Teod.
Dunaliella spp.
Elakatothrix sp.
Enteromorpha intestinalis (L.) Grev. (fragments) 1
Eremosphaera viridis De-Bary
Eremosphaera sp.
Ettliella tetraspora Hind.
Eudorina elegans Ehr.
Franceia ovalis (Francé) Lemm.
Franceia tenuispina Kors.
Gloeoactinium europaeum Hind.
Gloeotilla curta Skuja
Gloeotilla pelagica (Nyg.) Skuja
Golenkinia radiata Chod.
Golenkiniopsis solitaria (Kors.) Kors.
Granulocystopsis coronata (Lemm.) Hind.
Hormidium flaccidum A. Br.
Hormidium fluitans (Gay) Heer.
Keratococcus suecicus Hind.
Kirchneriella hindakiana Marv., Kom. et Com.
Kirchneriella lunaris (Kors.) Mösb.
Kirchneriella obesa (West) Schm.
Kirchneriella pinguis Hind.
Koliella longiseta (Visch.) Hind.
Koliella setiformis (Nyg.) Nyg.
Koliella sp.
Komarekia sp.
Lagerheimia ciliata (Lag.) Chod.
Lagerheimia genevensis Chod.
Lagerheimia longiseta (Lemm.) Printz
Lagerheimia octacantha Lemm.
Lagerheimia quadriseta (Lemm.) G. M. Sm.
Lagerheimia wratislaviensis Schröd.
Lobomonas sp.
Micractinium crassisetum Hortob.
Micractinium parvulum (Kuff.) Heg. et Schn.
Micractinium parvum Hind.
Micractinium pusillum Frés.
Micractinium quadrisetum (Lemm.) G. M. Sm.
Microspora stagnorum (Kütz.) Lag.
Microspora sp.
D D
O
E Sh ST Af As Ac Pb Pf PF PG Al Ar VV St R
1
2
1
2
1
2
1
2
1
1
1
2
1
1
1
1
1
4
1
1
1
1
1
2
2
1
2
1
1
1
1
11
1
2
2
2
2
1
2
2
2
3
1
2
2
1
1
1
1
2
2
2
1
1
1
1
1
2
2
1
2
1
1
1
1
4
2
2
2
2
1
1
1
2
2
1
1
2
1
1
1
2
2
2
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
2
1
1
1
1
1
2
1
1
1
Continued on p. 31
31
Table 2. Continued
Algal taxa/Sites
CHLOROPHYTA
EUCHLOROPHYTINA
Monoraphidium arcuatum (Kors.) Hind.
Monoraphidium circinale (Nyg.) Nyg.
Monoraphidium contortum (Thur.) Kom.-Legn.
Monoraphidium flexuosum Kom.
Monoraphidium griffithii (Berk.) Kom.-Legn.
Monoraphidium irregulare (G. M. Sm.) Kom.-Legn.
Monoraphidium komarkovae Nyg.
Monoraphidium pseudobraunii (Bel. et Sw.) Heyn.
Monostroma wittrockii Born. (fragments)
Nephrochlamys rotunda Kors.
Nephroselmis discoidea Skuja
Nephroselmis sp.
Oedogonium sp. st. (fragments)
Oocystella borgei (Snow) Hind.
Oocystella lacustris (Chod.) Hind.
Oocystella cf.parva (W. et G. S. West) Hind.
Oocystella solitaria (Wittr.) Hind.
Palmella sp.
Pandorina charkowiensis Kors.
Pandorina morum (O. F. Müll.) Bory
Pandorina smithii Chod.
Papenfusiomonas cordata (Pasch. et Jah.) Des
Pediastrum angulosum Ehr. ex Menegh.
Pediastrum boryanum (Turp.) Menegh.
Pediastrum boryanum (Turp.) Menegh. var.
cornutum (Racib.) Sulek
Pediastrum duplex Meyen
Pediastrum kawraiskii Schm.
Pediastrum tetras (Ehr.) Ralfs
Pediastrum tetras (Ehr.) Ralfs var. tetraodron
(Corda) Hansg.
Phacotus coccifer Kors.
Phacotus lenticularis (Ehr.) Stein
Phacotus minusculus Bourr.
Planctococcus sphaerocystiformis Kors.
Planophilla sp.
Pocillomonas flos-aquae Stein.
Pocillomonas sp.
Polytomella sp.
Provasoliella cf. simplicissima (Pasch.) Ettl
Pseudocarteria peterhofiensis (Kissel.) Ettl
Pseudodictyosphaerium elegans (Bachm.) Hind.
Pseudodictyosphaerium lacunare Hind.
Pseudodictyosphaerium minusculum Hind.
Pseudodictyosphaerium scoticum Hind.
Pseudodidymocystis lineata (Kors.) Hind.
Pseudodidymocystis planctonica (Kors.) Hegew.
et Deas.
Pseudokirchneriella contorta (Schmidle) Hind.
D D E Sh ST Af As Ac Pb Pf PF PG Al Ar VV St R
O
2
2
2
1
1
2
1
3
2
2
2
2
1
1
3
2
2
2
2
3
1
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
1
1
2
1
2
1
1
1
1
1
1
1
2
4
1
1
1
1
1
3
1
1
1
2
2
1
1
2
1
2
1
1
3
2
3
3
4
3
3
1
1
1
2
1
2
1
2
1
2
1
2
2
2
1
2
2
1
3
1
3
1
1
1
1
1
4
2
1
1
2
2
2
1
1
2
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
2
2
3
1
2
3
1
4
3
1
3
1
2
1
2
1
1
1
1
1
Continued on p. 32
2
1
1
1
32
Table 2. Continued
Algal taxa/Sites
CHLOROPHYTA
EUCHLOROPHYTINA
Pseudokirchneriella danubiana (Hind.) Hind.
Pseudokirchneriella major (Bern.) Hind.
Pseudokirchneriella roselata (Hind.) Hind.
Pseudokircneriella rotunda (Kors.) Hind
Pseudokirchneriella subcapitata (Kors.) Hind.
Pseudokirchneriella van-goori (Nyg., Kom., Krist.
et Skulb.) Hind.
Pseudoschroederia robusta (Kors.) Hegew. et Schn.
Pteromonas aculeata Lemm.
Pyramimonas micron Conr. et Kuff.
Pyramimonas minima Pasch.
Pyramimonas tetrarhynchus Schm.
Pyramimonas sp.
Quadrigula lacustris (Schröd.) G. M. Sm
Quadrigula pfitzeeri (Schröd.) G. M. Sm.
Quadrigula sp.
Raciborskiella salina Wisl.
Radiococcus nimbatus (De Wild) Schm.
Radiococcus planctonicus Lund
Raphidonema sp.
Rhizoclonium sp. (fragments)
Scenedesmus acuminatus (Lag.) Chod.
Scenedesmus arcuatus (Lemm.) Lemm.
Scenedesmus arcuatus Lemm. var. platydiscus
G. M. Sm.
Scenedesmus armatus Chod.
Scenedesmus bicellularis Chod.
Scenedesmus breviaculeolatus Chod.
Scenedesmus brevispina (G. M. Sm.) Chod.
Scenedesmus communis (Turp.) Hegew.
Scenedesmus ecornis (Ehr. ex Ralfs) Chod.
Scenedesmus ellipticus Corda
Scenedesmus flavescens (Chod.) Hegew.
Scenedesmus intermedius Chod.
Scenedesmus maximus (W. et G. S. West) Chod.
Scenedesmus naegeli Bréb.
Scenedesmus obliquus (Turp.) Kütz.
Scenedesmus obtusus Meyen
Scenedesmus opoliensis P. Richt.
Scenedesmus opoliensis P. Richt. var.
mononensis Chod.
Scenedesmus parvus (G. M. Sm.) Bourr.
Scenedesmus pectinatus Meyen
Scenedesmus pleiomorphus Hind.
Scenedesmus protuberans Fritsch et Rich
Scenedesmus sempervirens Chod.
Scenedesmus spicatus W. et G. S. West
D D E Sh ST Af As Ac Pb Pf PF PG Al Ar VV St R
O
2
1
2
1
1
2
1
2
2
1
1
2
1
2
1
1
1
1
2
1
2
1
1
1
1
1
4
2
1
1
4
4
1
1
2
2
1
1
2
1
1
1
2
1
1
1
1
1
2
1
1
2
2
1
1
1
2
1
1
1
1
1
3
3
2
2
2
2
1
1
1
2
2
2
1
1
1
1
4
3
2
2
2
2
1
1
2
1
1
1
3
3
3
2
1
1
1
1
1
2
1
1
1
1
3
1
1
1
1
1
1
2
1
1
1
2
2
1
2
2
2
1
2
2
1
1
1
1
1
1
1
Continued on p. 33
33
Table 2. Continued
Algal taxa/Sites
CHLOROPHYTA
EUCHLOROPHYTINA
Scenedesmus spinosus Chod.
Scenedesmus subspicatus Chod.
Scenedesmus verrucosus Roll
Schroederia setigera (Schröd.) Lemm.
Schroederia spiralis (Printz) Kors.
Selenastrum gracile Reinsch.
Siderocelis ornata (Fott) Fott
Siderocelopsis kolkwitzii (Naum.) Hind.
Siderocelopsis oblonga (Naum.) Hind.
Siderocystopsis punctifera (Bol.) Hegew. et Schn.
Sorastrum spinulosum Näg.
Spermatozopsis exsultans Kors.
Tetraedron caudatum (Corda) Hansg.
Tetraedron minimum (A. Br.) Hansg.
Tetraedron pentaedricum W. et G. S. West
Tetraedron triangulare Kors.
Tetraedron trilobatum (Reinsch.) Hansg.
Tetrachlorella alternans Kors.
Tetraselmis arnoldii (Proshk.-Lavr.) Norr., Hori
et Chih.
Tetraselmis cf. arnoldii (Proschk.-Lavr.) Norr., Hori
et Chih.
Tetraselmis cordiformis (Carter) Stein
Tetraselmis subcordiformis (Wille) Butcher
Tetraselmis sp.
Tetraspora sp.
Tetrastrum elegans Playf.
Tetrastrum glabrum (Roll) Ahlstr. et Tiff.
Tetrastrum heteracanthum (Nordst.) Chod.
Tetrastrum komarekii Hind.
Tetrastrum punctatum (Schm.) Ahlstr. et Tiff.
Tetrastrum staurogeniaeforme (Schröd) Lemm.
Thorakomonas korschikoffii Conr.
Thorakomonas sabulosa Kors.
Treubaria euryacantha (Schm.) Kors.
Treubaria planctonica (G. M. Sm.) Kors.
Treubaria triappendiculata Bern.
Ulothrix implexa Kütz.
Ulothrix zonata (Web. et Mohr.) Kütz.
Uronema elongatum Hodg.
Willea irregularis (Wille) Schm.
Unidentified green flagellates
Unidentified prasinophycean algae
ZYGNEMOPHYTINA
Closterium acerosum (Schr.) Ehr. ex Ralfs
Closterium aciculare T. West
Closterium acutum Bréb.
Closterium ceratium Perty
D D E Sh ST Af As Ac Pb Pf PF PG Al Ar VV St R
O
2
2
2
2
1
2
2
1
2
2
2
1
2
2
1
1
1
3
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
3
1
1
1
1
1
3
1
2
2
2
1
2
2
1
2
1
1
1
1
1
1
1
1
1
1
2
1
4
1
1
2
2
1
2
1
2
1
2
2
1
2
2
2
1
2
1
1
1
1
1
2
1
1
1
1
1
1
1
1
2
1
1
1
1
2
4
1
4
4
4
4
1
2
1
4
1
1
2
4
2
3
3
1
4
Continued on p. 34
34
Table 2. Continued
Algal taxa/Sites
Closterium dianae Ehr. ex Ralfs
Closterium exiquum W. et G. S. West
ZYGNEMOPHYTINA
Closterium limneticum Lemm.
Closterium moniliferum (Bory) Ehr. ex Ralfs
Closterium nordstedtii Chod.
Closterium parvulum Näg.
Closterium pronum Bréb.
Closterium tortum Griff.
Closterium tumidulum Kütz. ex Ralfs
Closterium venus Kütz. ex Ralfs
Cosmarium bioculatum Bréb.
Cosmarium depressum (Näg.) Lund.
Cosmarium formosulum Hoff.
Cosmarium impressulum Elfv.
Cosmarium laeve Rabenh.
Cosmarium sp.
Cosmoastrum sp.
Mougeotia sp. st. (fragments)
Spirogyra sp. st. (fragments)
Staurastrum gracile Ralfs
Staurastrum manfeldtii Delp.
Staurastrum tetracerum Ralfs
D
O
D
E
Sh
3
3
ST
Af
As
Ac
Pb
Pf
PF
PG
Al
Ar
VV
St
R
1
1
1
1
2
2
1
1
3
3
1
2
2
1
1
1
1
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
dominants, while A. falcatus, G. radiata and M.
irregulare sometimes occurred as abundant species.
Chlorella spp. and S. communis occupied all possible
positions in the quantitative phytoplankton structure.
Forty-eight chlorococcal algae occurred as abundant species, while Choricystis cylindracea, Closteriopsis acicularis, Coelastrum astroideum, C. microporum, Crucigenia tetrapedia, Scenedesmus ecornis and Siderocystopsis punctifera, if quantitatively important, occupied a subdominant position.
The needle-like forms Gloeotilla curta, Koliella setiformis and Quadrigula lacustris only occurred as
abundant species. Zygnemophytes were present in
low numbers, both in total species composition (26)
and group biomass (11). However, on several occasions, they (including desmids) played an important
role in the quantitative structure of the phytoplankton community, especially during the summer–autumn
periods. The desmids Closterium acerosum (E) and
C. aciculare (Al) occurred as dominants, while C.
ceratium (D, E), C. dianae (E, SH), Cosmarium bioculatum (D) and C. depressum (D) were subdomin-
ants. Further, Closterium aciculare, C. ceratium, C.
pronum, C. tortum and Cosmarium sp. were typically
observed as abundant species. All chloroccoccal, filamentous green and desmid species mentioned above
were important contributors to the phytoplankton biomass in freshwater and oligohaline sites (DO, D, SH,
E, Af, Pf, PF, PG, Al, VV, St).
Green flagellates were also well represented in the
phytoplankton assemblages of the studied wetlands.
In comparison with chlorococcal algae, they had a
smaller role in determining phytoplankton community
structure (44) and group biomass (13). Nevertheless,
green flagellates often occupied dominant positions in
various meso-, eu- and hyperhaline sites (ST, As, Pb),
as well as in sites with changing salinity (Ac, R). Such
flagellates were Dunaliella salina (As), Dunaliella sp.
(Pb), Pyramimonas minima (As), Tetraselmis sp. (As)
and some miscellaneous unidentified forms (ST, As,
Ac, Pb, R). Representatives of the genera Chlamydomonas and Chloromonas, as well as Pyramimonas
micron, contributed notably to the total phytoplankton
biomass in some freshwater and oligohaline sites (DO,
35
D, Pf, St) mainly during spring, autumn and winter
periods. Pandorina morum dominated the plankton
one summer in the highly eutrophic stagnant waters
of Atanassovsko Lake. Green flagellates of the genera
Chlorogonium, Tetraselmis, Pyramimonas and several Prasinophyceae superseded other green algae both
qualitatively and quantitatively in the freshwater small
and shallow Arkutino marsh, which was covered by
Nymphaea alba. The above mentioned genera were
similarly important in the lower part of the highly
eutrophic Ropotamo River which receives frequent
influx of Black Sea waters.
Correlations between the biomass of dominants,
sub-dominants and abundant algae, and trophic state,
physical and chemical parameters varied significantly
among species. Some species were strongly related
to trophic state (e.g. Golenkinia radiata – the correlation coefficient r is 0.9; Schroederia setigera – r
= 0.95; Pseudokirchneriella rotunda – r = 0.8; Oocystella solitaria – r = 0.7; Closterium tortum – r =
−0.95). Whereas others were better related to physical and chemical factors (e.g. Pseudodictyosphaerium
lacunare – with depth (r = 0.93), salinity (r = 0.93)
and temperature (r = 0.8); Micractinium pusillum –
with TDS (r = 0.9), depth (r = −0.8) and area (r =
−0.64); Dunaliella salina – with salinity (r = 0.99),
Quadrigula lacustris – with dH (r = 0.87), Cosmarium
depressum – with dH and TDS (r = −0.9), Closterium
aciculare – with temperature (r = 0.9).). By contrast,
the biomass of species like Coelastrum microporum,
C. microporum var. octaedricum, Oocystella lacustris, Pediastrum duplex, P. tetras, Scenedesmus communis, Tetrastrum staurogeniaeforme or of some taxa
identified only at genus level (Chlamydomonas spp.,
Chlorella sp.) was not correlated with any other measured variable (r = 0.1–0.3). For Crucigenia terapedia,
Monoraphidium irregulare and Quadrigula lacustris,
these correlations were distinctly higher (r = 0.3–0.5).
Some of these relations are presented using habitat
templates in Figure 3, with arms representing the specific requirements or tolerances of named algae to
separate variable characters of the environment.
The statistical results derived from BIODIV confirm that green algae comprise a significant part of
the total species composition (r = 0.98) and that the
total number of phytoplankton species in each wetland
depends more on depth (r = 0.56) than on area (r =
−0.01) or salinity (r = −0.03). These correlations with
depth, area and salinity were higher when considering
only the number of green algal species (r = 0.62, r =
−0.07 and r = −0.13, respectively). The number of
Chlorococcales and zygnemophyte species increased
with depth (r = 0.69 and r = 0.5, respectively), while
the number of filamentous green algae slightly decreased with depth (r = −0.42). Strong correlations
among the number of species of coccal, filamentous green algae and zygnemophytes were detected
(r = 0.87–0.89). Whereas there was no correlation
between total phytoplankton numbers and depth, although the densities of both coccal and filamentous
green algae were found to increase with depth (r =
0.96). Both total phytoplankton and green algal numbers in each water body showed low and insignificant
correlations with trophic state as assessed through average annual biomass (r = 0.24 and r = −0.24). By
contrast, the numbers of green flagellates were better related to the trophic state (r = 0.76). The total
green algal abundance of each water body showed a
relatively high correlation (r = 0.78) with its trophic
state. The average annual biomass of green flagellates
and zygnemophytes increased with trophic state (r =
0.61 and r = 0.5, respectively), whereas the biomass
of other green algal groups was not related with the
trophic state (r = 0.03–0.1).
The ordination of studied sites based on their green
algal flora and by data processing with TWINSPAN
and BIODIV (Figure 4) corresponded better with their
ordering according to P–PO4 3−− loading (r = −0.61)
than to their ranking according to annual average biomass (r = −0.44). Correlations with other physical
and chemical factors were lower, NH4 + (r = −0.09)
and depth (r = −0.41) being the extremes. Another
analysis run with the same procedure, but including
only the most important biomass contributors (Figure 5) resulted in a different ordination of studied
sites, which showed no relationship with trophic state,
expressed either through average annual biomass or
through P–PO4 3−− loading (r = −0.04). In addition,
separate analyses were run based on dominant, subdominant and abundant species. The ordination of
sites obtained from analysis of the subdominant algae
corresponded better to trophic structure, when considering the physical and chemical data (r = −0.57).
Discussion
Most of the 247 green algal taxa found in Bulgarian
coastal wetlands are classified as species typical of eutrophic waters (e.g. Komárek & Fott, 1983). According to OECD-criteria, the trophic state of studied water
bodies varies from eutrophic to hypertrophic. It is al-
36
Figure 3a
Figure 3. Habitat templates for some species with important quantitative contribution to the phytoplankton structure: b – species biomass [mg
l−1 ]; a – area [ha×10−2 ]; d – depth [m×10−1 ]; sal – salinity [Cll]; t – temperature [◦ C×10−1 ]; Sec – transparency acc. to Secch disk [m];
tb – total phytoplankton biomass [mg l−1 ×10−1 ]; P – PO4 3−− [mg l−1 ]; N – NH4 + [mg l−1 ]; TDS – mineralisation [g l−1 ×10−1 ]; dH –
water hardness [dH0 ×10−1 ]; S – SiO2 [mg l−1 ×10−2 ]. (∗ – for Dunaliella salina real values of total biomass, salinity, TDS and temperature
are used.)
37
Figure 3b.
38
Figure 4. Arrangement of studied sites according to their floristic similarity through BIODIV. Abbrevations used follow those in Figure 2.
most completely accepted that trophic state is one of
the main factors which influence phytoplankton structure (Seip & Reynolds, 1995) and many green algae
are included in the provisional trophic spectrum of major phytoplankton genera (Reynolds, 1998). Most of
these representatives are found in the studied wetlands.
However, the correlations between number of green
algal species and trophic state, as expressed through
P–PO4 3−− loading and through annual average biomass of the wetlands studied, are lower than expected
(r = −0.61 and r = 0.44, respectively). The same
observation is valid for correlations made with total
phytoplankton abundance and total green algal abundance. Most probably, one of the reasons for the lower
correlations is that this study includes habitats across
a wide salinity range (from freshwater to hyperhaline)
for which there still is a lack of settled and accepted
criteria for assessment of trophic state (Vollenweider,
1989). Several authors report that algal response to
eutrophication is modified by salinity, e.g. Bierhuizen
& Prepas (1985) and Campbell & Prepas (1986).
Moreover, other biotic factors (including allelopathy
& grazing) can have a strong influence on phytoplankton structure. For instance, during the studied period,
strong summer cyanoprokaryote blooms (Microcystis
wesenbergii, Aphanizomenon flos-aquae, etc.) were
detected in most of the studied wetlands (Stoyneva,
in press, b) and zooplankton and zoobenthos were
abundant (Kovachev, pers. com.). It is also worth mentioning that almost all quantitatively important green
algae found in those lakes are considered as inedible by zooplankton and may even be stimulated by
passage through the digestive tract of these organisms (Porter, 1973; Krienitz et al., 1996). In addition,
our study demonstrates the influence of morphometry
on phytoplankton structure, as shown by significant correlations between depth and species number
and abundance of groups like Chlororococcales and
zygnemophytes. Salinity seems to influence the composition of green flagellates (r = 0.69). The compar-
39
Figure 5. Arrangement of studied sites according to the quantitatively important species through BIODIV. Abbreviations used follow those in
Figure 2.
ison of habitat templates for species which contribute significantly to phytoplankton biomass shows that
even taxa from one species (Coelastrum microporum
& C. microporum var. octaedricum), one genus (Pediastrum tetras – P. duplex, Oocystella solitaria –
O. lacustris) one family (Koliella setiformis – Quadrigula lacustris, Micractinium pusillum – Golenkinia
radiata, Tetrastrum staurogeniaeforme – Scenedesmus
communis) and finally one Order (Closterium tortum
– Cosmarium depressum) have different requirements
and tolerances to the envronmental factors and to the
trophic state.
Our study stresses the important role of green algae
in the phytoplankton structure of various Bulgarian
coastal water bodies, where they form 43% of the total
species composition, 18% of algal numbers, 21% of
algal biomass and often have dominant or subdominant roles. The high number of species found reflects
their importance to the communities as bearers of eco-
logical memory and indicators of ecological stability
as observed in other natural water bodies (Padisák,
1991, 1992).
Acknowledgements
The author wishes to thank Mrs V. Chainadjieva, Mr
M. Dimitrov, Mr I. Botev and Mr Chr. Naydenov for
obtaining and providing the chemical characteristics
of the studied lakes. Special thanks are due to Mr T.
Michev, Dr St. Kovachev, Mrs V. Chajnadjieva and Dr
St. Andreev for their inestimable help in the collecting of the samples. The biggest part of the study was
done within the framework of BSBCP. The author is
obliged to Mr G. Dandliker, Mrs M. Konstantinova,
Mr T. Michev, Mr D. Georgiev, Mr St. Dobrev, Mr
G. Georgiev and Mr M. Marinov for the opporunity
to study these interesting environments. The help of
Dr G. Vassileva and Mr I. Stoyanov during the statist-
40
ical processing of data is highly appreciated. Special
thanks are due to Dr H. Kling for the invitation to
present this work at the 12th IAP-meeting in Canada,
to Dr P. Hamilton for his support and suggestons on the
text, to Prof. J.-P. Descy for the comments and correction of the manuscript and to both unknown referees
for the critical comments on the manuscript, which
improved its quality.
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