The relationship between phytoplankton species dominance and environmental variables in a shallow lake (Lake Vrana, Croatia)

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SHALLOW LAKES

The relationship between phytoplankton speciesdominance and environmental variables in a shallow lake(Lake Vrana, Croatia)

Marija Gligora Æ Andelka Plenkovic-Moraj ÆKoraljka Kralj Æ Istvan Grigorszky Æ Danijela Peros-Pucar

� Springer Science+Business Media B.V. 2007

Abstract The shallow Lake Vrana was studied

over a 1-year period, special attention being paid

to the phytoplankton. Phytoplankton was inves-

tigated monthly with respect to temporal vari-

ability of selected environmental factors. The

regular annual development observed was in

species contribution to total biomass rather than

in seasonal changes in species composition. The

assemblage was dominated by Cosmarium tenue

Arch. and Synedra sp. In winter and in spring the

phytoplankton assemblage was dominated by

Cosmarium tenue and high contribution of Syne-

dra sp. was observed during the summer and

autumn. Results suggest that concentrations of

inorganic nitrogen and phosphorus were critical

in regulating phytoplankton biomass and species

dominance.

Keywords Phytoplankton � Shallow lake �Species dominance

Introduction

One of the two states in shallow lakes is a clear

state rich in submerged vegetation (Scheffer,

1998). Macrophytes provide refuge for pelagic

grazers (Stephen et al., 1998), support a diverse

fish population, prevent sediment resuspension

and are also one of several mechanisms that can

suppress phytoplankton growth by reducing nutri-

ent concentration in the lake water column

(Jeppesen et al., 1997; Søndergaard et al., 2003;

Fernandez-Alaez et al., 2004). The rates at which

organisms consume resources depend on the

availability of such resources. Phytoplankton

utilizes nutrients and becomes a component of

the pelagic food web (Lampert & Sommer, 1997;

Gliwicz, 2002; Stephen et al., 2004; Auer et al.,

2004). Interannual variability in nutrient

resources can play an important role in the

determination of phytoplankton distribution and

abundance (Sommer, 1987; Reynolds, 1997;

Naselli-Flores, 2000). Phytoplankton is affected

by external factors but is also influenced by the

outcome of the competition itself (Kilham &

Guest editors: R. D. Gulati, E. Lammens, N. De Pauw &E. Van DonkShallow lakes in a changing world

M. Gligora (&) � A. Plenkovic-Moraj �K. KraljDivision of Biology, Department of Botany, Facultyof Science, University of Zagreb, Rooseveltov trg 6,HR-10000 Zagreb, Croatiae-mail: [email protected]

I. GrigorszkyBotanical Department, Debrecen University,P.O. Box 14, Debrecen 4010, Hungary

D. Peros-PucarPublic Health Institute Zadar, Kolovare 2, Zadar,Croatia

123

Hydrobiologia (2007) 584:337–346

DOI 10.1007/s10750-007-0590-0

Page 2

Tilman, 1979; Tilman et al., 1982; Huisman &

Weissing, 1999). There were two working hypoth-

eses during this investigation. First, that environ-

mental variables influence phytoplankton species

composition and biomass. Second, that phyto-

plankton seasonality and changes in species

dominance are correlated with nutrient availabil-

ity in a shallow vegetated lake.

Study site

Lake Vrana (Vransko jezero) is situated on the

East Adriatic coast. It is a freshwater (salinity

range 0.7–1.2&), karstic cryptodepression con-

nected at the south west to the Adriatic Sea by a

narrow artificial channel. Lake Vrana is polymic-

tic, shallow waterbody with a mean depth of 2 m.

Catchments are characterized mainly by karst.

Because of the karst morphology and the agri-

cultural nature of the surrounding area, in con-

junction with the presence of a bird sanctuary in

the north west part, the lake receives considerable

external nutrient loads. The lake is dominated by

macrophytes, especially during the warm summer

months. Macrophyte coverage, as visually esti-

mated, exceeded 50% of the surface area during

summer (dominants: Najas marina L., Potamog-

eton pectinatus L. and Potamogeton perfoliatus

L.). The macrophyte association also includes

Phragmites australis (Cav.) Trin. ex Steud., Scir-

pus triqueter L. Tavlen, Myriophyllum spicatum

L., Utricularia australis R. Br, Chara sp., Typha

angustifolia L. and Potamogeton lucens L., as

accompanying species (M. Mrakovcic, pers.

comm.).

Materials and methods

Phytoplankton was sampled monthly at four

selected sites, in the period from January to

December 2004. Samples for phytoplankton anal-

ysis were collected at 0.5 m depth, preserved in

2% formaldehyde (final concentration) and

stored at 4�C. After 24 h sedimentation, 10 ml

subsamples were analyzed. Cell counts were

obtained with the inverted microscope following

Uthermohl’s method (1958). A minimum of 400

settling units were counted, nanophytoplankton

(<20 lm) at 1000· magnification in 15 randomly

selected fields and microphytoplankton (>20 lm)

cells in a transect at 400· magnification, providing

a counting error of <10% (Lund et al., 1958).

Measurements of the 20 randomly chosen cells

were obtained by AxioVision software and bio-

mass was calculated according to Rott (1981).

Transparency was measured with a Secchi disc.

Samples for water chemistry were taken simulta-

neously with phytoplankton samples. They were

stored in refrigerated boxes and analyzed in the

laboratory for nitrate, nitrite, ammonium, soluble

reactive phosphorus, total phosphorus, chlorides,

and pH, alkalinity, conductivity, oxygen and its

saturation (APHA, 1995). Chlorophyll a concen-

trations were analyzed fluorometrically according

to Method 445.0 after filtration onto Whitman

GF/F glass filters and acetone extraction (Arar &

Collins, 1997).

For statistical evaluation PRIMER 5 software

package was employed (Clarke & Warwick,

2001). Principal-component analysis (PCA) of

all physical and chemical variables (Table 1,

excepted chl a) was used to identify the main

environmental variables in the dataset. Distances

between samples on the ordination attempt to

match the corresponding dissimilarities in the

environmental data. The correlation between the

individual and combined environmental parame-

ters and the phytoplankton biomass was analyzed

using PRIMER 5 submodule BIO-ENV. A stan-

dard Spearman’s rank correlation was used in this

procedure. Only taxa contributing more than 5%

to the total phytoplankton biomass were included

in the analysis. All physical and chemical data as

well as phytoplankton biomass were normalized

for PCA and BIO-ENV. To reduce the influence

of absolute biomass, the data were standardized

to a 0–1 range (Jackson, 1993). The same trans-

formation was used for all physical and chemical

parameters since data were not normally distrib-

uted (except conductivity and chloride values).

The draftsman plot of all pairwise combinations

suggested that linearity was satisfied under this

transformation, which is appropriate for these

variables. The analysis of differences between

samples and groups was restricted to non-para-

metric tests, Kruskal–Wallis and Mann–Whitney

338 Hydrobiologia (2007) 584:337–346

123

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Hydrobiologia (2007) 584:337–346 339

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U tests. Pearson’s correlation coefficients, as well

as Kruskal–Wallis and Mann–Whitney U tests,

were calculated using Statistica 6.0 software.

Results

In the course of the year water temperature in

Lake Vrana ranged between 1.6�C and 26.2�C

and was greatly influenced by the Mediterra-

nean climatic conditions. It was typically higher

during the summer (Table 1, group III) and

lower in the winter period (Table 1, group I).

The water was alkaline (7.7–9.4), with very high

conductivity (1638–3960 lS cm–1). Nitrate con-

centrations varied between 0.5 mg l–1 and

2.34 mg l–1 reaching, a maximum in March and

decreasing towards summer. The lowest nitrate

concentration was recorded in September.

Ammonium ranged from 0.004 mg l–1 to

0.3 mg l–1 with a decreasing trend from winter

to spring-summer. Mean concentration of

ammonium during summer (from July to Sep-

tember, Group III) was 0.018 mg l–1. Following

lower summer values, an increase in ammonium

concentration was recorded. Nitrite concentra-

tions ranged from 0.0013 mg l–1 to 0.023 mg l–1.

Nitrite concentrations were higher (mean

0.018 mg l–1) during the spring period (from

April to June, Group II) and decreased in the

lake during the summer and autumn. Monthly

variation of total phosphorus concentrations

changed between 0.01 mg l–1 and 0.059 mg l–1

except in January, when a mean value of

0.25 mg l–1 was recorded. Soluble phosphorus

ranged from 0.001 mg l–1 to 0.025 mg l–1 during

the study period except for a peak in January

(January mean value 0.04 mg l–1). Dissolved

inorganic N (as NH4–N + NO2–N + NO3–N) to

P (PO4–P) ratio was higher than 30:1 during

whole research period.

Among the 55 species identified during 2004,

only 15 species contributed more than 5% to the

total phytoplankton biomass. The assemblage was

dominated by Cosmarium tenue Arch. and

Syneda sp. The winter and spring assemblages

were dominated by Cosmarium tenue. The assem-

blage was determined by a high contribution of

Synedra sp. during summer and autumn (Fig. 1).

The high species diversity in January was caused

by the highest species number (24). Diversity

significantly decreased from January to June and

it was lowest in June, due to the great predom-

inance of Cosmarium tenue.

The two axes in PCA analyses accounted for

60.3% of the cumulative variance in physico-

chemical data set with eigenvalues of 5.29 and

2.55, respectively (Table 2). Axes 3, 4 and 5

accounted for 29.5% and are not discussed

further. PCA 1 was presented by temperature,

in the positive direction (r = 0.395) and ammo-

nium in the negative (r = –0.382), explaining

40.7% of the variance. PCA axis 2 was positively

influenced by NO2–N (r = 0.490) and NO3–N

(r = 0.575) (Fig. 2).

The BIO-ENV procedure presented phyto-

plankton assemblages and biomass in correlation

with concentrations of inorganic nitrogen com-

pounds, temperature and chlorides (qw = 0.389).

According to the analyses, winter samples

(January/March) were joined in Group I and

correlated with high ammonium concentrations

(Table 1) but also with high oxygen, chlorides and

alkalinity values (Fig. 2). The dominant species

during this period was Cosmarium tenue, accom-

panied by Gonatozygon sp. (Table 3). There was

significant difference in phosphorus concentration

between January and March (p < 0.05). Group II

joined the spring samples (April/May/Jun) with

the clear dominance of Cosmarium tenue (Ta-

ble 3) and high concentrations of nitrites and

nitrates, but lower ammonium values (Table 1).

The temporal distribution of Synedra sp. mostly

affected groups III and IV. According to the

statistical analysis, Group III represents summer

(July/August/September) assemblages dominated

by Synedra sp. associated with low nitrogen

concentrations, oxygen and chlorides (Fig. 2). In

terms of species dominance two subgroups of

Group III can be recognized. The first subgroup

consists of July samples where Synedra sp. was a

codominant species due to biomass, and

Gomphosphaeria sp. was the dominant species

accompanied by Planktolyngbya contorta (Lem-

mermann) Anagnostidis & Komarek and

Cosmarium tenue. The second subgroup was

represented by August and September assem-

blages with the clear dominance of Synedra sp.,

340 Hydrobiologia (2007) 584:337–346

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and Gomphospaheria sp. as accompanying

species (Table 3). There was a statistically signif-

icant difference in levels of nitrites and nitrates

between subgroups within Group III (p < 0.01).

During autumn, nitrogen compounds again

reached higher values (Table 1) determining the

assemblage in Group IV with the dominance of

Synedra sp. and codominance of Cosmarium

tenue.

Other species, Pseudanabaena catenata Lauter-

born, Chroococcus sp., Crucigenia tetrapedia

(Kirchner) W. & G. S. West, Monoraphidium

minutum (Nageli) Komarkova-Legenerova,

Ankistrodesmus densus Korshikov, Koliella tenuis

(Nygaard) Hindak and Navicula sp. also typified

the assemblages in Lake Vrana but contributed

less to the total phytoplankton biomass during

most of the investigation period, with no distinct

seasonal differences in the assemblages.

Kruskal–Wallis and Mann–Whitney U tests

performed on the four statistically identified

groups confirmed significant differences in the

nitrogen concentrations and also temperature,

alkalinity, oxygen, concentrations of chlorides

and chlorophyll a (Table 1).

Concentrations of chlorophyll a ranged from

0.05 lg l–1 to 9.54 lg l–1 and clearly correlated

with concentration of nitrites (r = 0.66, p <

0.001). Biomass ranged from 0.94 mg l–1 to

51.60 mg l–1 and reached a higher concentration

during winter period due to the high contribution

of large benthic diatoms to the phytoplankton

biomass. Total phytoplankton biomass showed a

Fig. 1 Changes inShannon–WienerDiversity Index (H)through the investigationperiod (mean values andstandard deviation onfour sampling points)indicating groupsidentified by statisticalanalyses and dominantspecies

Table 2 Summary statistics for the first five axes of PCAperformed on the environmental data set during theresearch period

PCA axis 1 2 3 4 5

Eigen values 5.29 2.55 1.76 1.27 0.80% Variation 40.7 19.6 13.5 9.8 6.2Cumulative % variation 40.7 60.3 73.5 83.5 89.7

Hydrobiologia (2007) 584:337–346 341

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great positive correlation with phosphates

(r = 0.54, p < 0.001) but also a very high correla-

tion with all nitrogen compounds, especially with

nitrites (r = 0.33, p < 0.05).

Discussion

The present study indicates that nutrients are

significant variables influencing phytoplankton

biomass. The regular annual development ob-

served was in species contribution to total bio-

mass rather than in seasonal changes in species

composition. According to the statistical analysis,

it was the inorganic nitrogen compounds in the

water column that mostly affected species dom-

inance. PCA showed seasonality of nitrogen

compounds, which was followed by changes in

species dominance. High nitrogen concentrations

during winter and especially during spring period

coincided with the dominance and high biomass

of Cosmarium tenue. Nitrogen compounds

reached their lowest values during summer, and

this coincided with change in species dominance.

In this time of the year, a low concentration of

inorganic nitrogen was followed by a high contri-

bution of Synedra sp. to the phytoplankton

biomass. This relationship was further supported

by the species biomass–environmental correla-

tions in statistical analyses.

According to the catchments morphology and

the characteristics of the surrounding area it can

be assumed that Lake Vrana receives a high

nutrient input. Despite the high external nutrient

loads, phosphorus was present in much lower

concentrations than nitrogen and might have a

limited effect on phytoplankton total biomass.

The Redfield ratio is one of the methods fre-

quently used to identify potentially limiting

nutrients, and phosphorus limitation in Lake

Vrana is evident considering the high concentra-

tion values of nitrogen in relation to phosphorus

in water column (Redfield, 1958). The influence

of phosphorus on the phytoplankton assemblage

Fig. 2 PCA ordination ofphysico-chemicalparameters showingsample grouping andgeneral trends of thoseparameters for eachgroup. Full line arrowsindicate tendencies ofmain parametersassociated with first andsecond PC axis. Dottedarrows are projection ofphytoplankton speciesdominance on axis 2

Table 3 Contribution(%) of dominant andaccompanying species infour groups and twosubgroups identified bystatistical analyses

Group I Group II Group III Subgroups III Group IV

Jul Aug Sep

Cosmarium tenue 50 87 10 15 7 29Diatoma tenue 7Gomphosphaeria sp. 30 35 22 15Gonatozygon sp. 14Navicula sp. 6 6Planktolyngbya contorta 10Synedra sp. 6 40 20 54 35Ulnaria ulna 8

342 Hydrobiologia (2007) 584:337–346

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is shown by the high correlation between the total

phytoplankton biomass and phosphates.

Although not supported by statistical analyses,

Table 1 suggests that the lowest values of phos-

phates were recorded in group III when the

concentration of soluble reactive phosphorus was

on average below 0.01 mg l–1 during three sum-

mer months. Apart from the external nutrient

load in lake, the internal load, especially of

phosphorus, is very important in shallow lakes.

Although the phosphorus and nitrogen content in

sediment were not determined in this study, the

phosphorus exchange process over the sediment-

water interface can play important role in the

phosphorus budget in shallow lakes. There is

considerable evidence for phosphorus sediment

immobilization resulting in the phosphorus limi-

tation condition in the water column (Scheffer,

1998). Chemical adsorption of phosphorus in

sediment may be caused by a number of pro-

cesses, which can be critical to phosphorus release

and can apparently cause phosphorus limitation

for phytoplankton. Water that is rich in calcium

and carbonate, such as karstic Lake Vrana, may

buffer the pH and lead to a decrease in phospho-

rus release from the sediment (Scheffer, 1998). In

Lake Vrana, a high concentration of nitrate was

detected. It has been suggested that a high

concentration of nitrate may buffer the redox

potential of the sediment surface, preventing a

release of iron bound phosphorus in the same way

as oxygen (Scheffer, 1998). Also, at high turbu-

lence, which is frequently present in the shallow

Lake Vrana, the sediment surface becomes oxy-

genated and phosphorus can be immobilized by

iron again. The great accumulation of phosphorus

in sediment found in shallow lakes does not occur

with nitrogen (Jensen et al., 1991). Apart from

chemical absorption macrophytes can change

nutrient retention and its effect on the nitrogen

is more consistent than on phosphorus. Spring

and summer concentration of nitrogen decreased

in the presence of high macrophyte coverage. The

high uptake of nitrogen by macrophytes appar-

ently caused a nitrogen limitation for the phyto-

plankton (Van Donk et al., 1993). The low

concentration of nutrients during the summer

period in Lake Vrana followed the dynamics of

macrophyte coverage. It can be assumed that

aquatic macrophytes in Lake Vrana, due to high

coverage during summer, affect nutrient dynam-

ics in the lake and have an impact on phyto-

plankton biomass (Scheffer et al., 1993; Jeppesen

et al., 1997) and changes in the species domi-

nance. Cosmarium tenue was dominated as long

as high concentrations of inorganic nitrogen were

recorded in water column. The summer domi-

nant, Synedra sp., was present in the lake with

high biomass when nitrogen was exhausted from

the water column and it is evident that phospho-

rus limitation during the summer period for

Cosmarium tenue was not limiting for Synedra

sp. (Sommer, 1987).

Results showed a range of diversity values in this

stable, well-mixed system, inconstant with respect

to chemical features, and temporarily disturbed.

Low diversity values were strongly affected by the

most abundant species. Individual species adapta-

tions to an environment suitable to host steady-

state assemblages (Mischke & Nixdorf, 2003)

resulted in low diversity values, especially during

June. From January to June, diversity decreased

steeply, affected by the predominance of only one

species (Padisak, 1993), Cosmarium tenue. Diver-

sity was reduced to minimal levels by competitive

exclusion or some other biotic interaction that can

result in steady state assemblages (Naselli-Flores

et al., 2003; Rojo & Alvarez-Cobelas, 2003). Over-

looking the fact that steady state phases are not

frequently attained in phytoplankton succession

(Padisak et al., 2003), and the monthly (instead of

weekly) sampling dynamics during this investiga-

tion (Rojo & Alvarez-Cobelas, 2003), theoreti-

cally, this phytoplankton assemblage, is close to

establishing equilibrium (Sommer et al., 1993), as

was manifested by the monodominance of Cos-

marium tenue (Padisak et al., 2003), with more

than 80% in total biomass over 3 months. How-

ever, external factors may prevent the establish-

ment of equilibrium by favoring the dominance of a

new species (Reynolds, 1993). Changes in species

dominance and high contribution of Synedra sp.

coincided with decreases in concentrations of

inorganic nitrogen. The same values of nitrogen

yielded greater diversity values. Considering diver-

sity and disturbance as indirectly linked (Reynolds

et al., 1993) and disturbance as a force that can be

measured as a reaction, it could be suggested that

Hydrobiologia (2007) 584:337–346 343

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the sufficient intensity of disturbance (Sommer

et al., 1993) was caused by a sudden event of low

concentration of nitrogen in the lake water.

According to BIO-ENV analysis, assemblages

were also affected by temperature and chloride

concentrations. High concentrations of chlorides

due to the artificial connection between the Lake

and Adriatic Sea were recorded in winter, while

lower and stable concentrations were observed in

summer. During stable summer temperature

conditions, changes in environmental variables,

such as nitrogen availability, produced noticeable

shifts in species dominance.

The phytoplankton assemblage in Lake Vrana

can be characterized in general as nanoplankton.

Cell size was found to be important in the deter-

mination of predominant species but could not be

considered the decisive factor for species selection

and their growth kinetics (Suttle et al., 1987;

Sommer, 1989). Species with small cell-sizes,

because of volume/surface area ratio and cell

shape, benefit from low nutrient concentration

and from phosphorus limited conditions and out-

compete larger-sized species (Smith & Kalff, 1982;

Grover, 1989). The species Cosmarium tenue in

Lake Vrana is characterized by a large mucous cell

envelope. The presence of an extracellular mucous

envelope is considered evidence indicative of

several functions suggested by Coesel (1994),

Decho (1990) and Whitton (1967). According to

Coesel (1994) mucilage sheets of desmids might be

indicatively related to the capture of scarce nutri-

ents. Apart from such results there are contradic-

tory experimental data with no clear indication of

the storage role of the extracellular mucous enve-

lope (Spijkerman & Coesel, 1998). It can be

deduced from Table 1 and statistical analyses that

species assemblage in Lake Vrana is naturally

selected according to the temperature, salinity

conditions, high conductivity, pH values and avail-

ability of CO2 (Reynolds, 1997) but also affinity for

the resource and species storage capacity (Spijk-

erman & Coesel, 1996a, b). According to Sommer

et al. (1993) phosphorus limitation of species with

high requirements becomes possible if SRP con-

centration falls below 10 lg l–1 and intracellular

stores have been depleted. Such conditions in Lake

Vrana were evident occasionally during the year

and for a period of 3 months during summer.

Species with low phosphorus demand, such as

pennate diatoms, would only become limited at

undetectable SRP concentrations (Sommer et al.,

1993). It can be assumed that the species domi-

nance in a given lake is determined by competition

for nutrients (Sommer, 1989). The species Synedra

sp. was competitively superior for phosphorus at a

low concentration of nitrogen and it became a

more productive summer species. This ability gives

a significant advantage to these organisms in

summer and Synedra sp. developed a larger pop-

ulation than Cosmarium tenue. It was able to

compete for phosphorus and reach dominance as

long as Cosmarium tenue was excluded by nitrogen

depletion (Lampert & Sommer, 1997).

In conclusion, the present study shows that in

the vegetated shallow Lake Vrana the concentra-

tion of nitrogen, like that of phosphorus, may be

important in the determination of phytoplankton

dominants. The phytoplankton annual succession

in Lake Vrana seems to be mainly controlled by

nutrients. Nutrient resources seem to be critical in

regulating phytoplankton species dominance and

total species biomass in Lake Vrana. In this way,

the phytoplankton community might be regulated

by external factors and also by competitive

interactions between the dominant species. The

influence of nutrients on the phytoplankton in

Lake Vrana was discussed in the specific lake

environment and should be considered a factor

controlling phytoplankton assemblages, biomass

and changes in dominance overlooking other

environmental features of the Lake.

Acknowledgments We would specially like to thankProfessor M. Mrakovcic, who initiated the study of LakeVrana. We, are also we are grateful to the CroatianMinistry of Science, Education and Sport, and theHungarian Scholarship Board for financial support.Special gratitude goes to the reviewers whose commentshelped us improve this paper.

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