Phytoplankton Community Structure in Artificial Salty Lake Near Kikinda City

Predojević Dragana1, Trbojević Ivana1, Pećić Marija1, Subakov-Simić Gordana1

 

 

1 University of Belgrade, Faculty of Biology, Institute of Botany and Botanical Garden "Jevremovac", Takovska 43, Belgrade, Serbia; E-mail: This e-mail address is being protected from spambots. You need JavaScript enabled to view it

 

Abstract

Aquatic inland ecosystems with increased water salinity have always been attractive because of the specific flora and fauna inhabiting them. Considering that, the phytoplankton community of the artificial saline lake near Kikinda city (Vojvodina province, Republic of Serbia) was investigated for the first time. A total of 27 detected algal taxa were classified in 5 divisions: Cyanobacteria, Chlorophyta, Euglenophyta, Bacillariophyta and Chrysophyta. A few taxa characteristic for saline or brackish water, such as Oocystis submarina, Merismopedia warmingiana, Euglena proxima, have been found. Still, the majority of recorded ones could be characterized as halotolerant rather than halophilic. Low chlorophyll-a concentration (12.8 µg/l), low biomass (855.7 µg/l), but high cell abundance (20882 cell/ml) were recorded, which could be explained by a small-dimension algae dominance in the phytoplankton, as well as abundant submerged vegetation. Chroococcalean cyanobacteria contributed with 70% of the total cell abundance that could be the response to low nutrient conditions as well as the adaptation to more effective osmoregulation process essential for living in such environment. Green algae dominate in total phytoplankton biomass, followed by diatoms and blue-green algae.

Keywords: saline inland waters, halophiles, halotolerant species, Kikinda city, phytoplankton, high conductivity.

Introduction

 

Water ecosystems all over the world represent a unique medium where different influences are met together. Chemical and physical parameters have an effect on characteristic wildlife development, but the organisms also affect the environment (Karadžić, 2011). So, this interdependent relationship among all of these parameters (chemical, physical and biological) is usually very complex and hard to explain, but in some situations it can be simplified. On that occasion, one factor usually prevails and has a strong effect on other constituents of the ecosystem. Unique community adapted to that specific environment is going to be developed. Among many others, that factor can be salinity of the water. It is a very important parameter, especially in inland waters, where high salinity is not expected.

Salinity is used as the correct chemical term for the sum concentration of all the ionic constituents dissolved in inland waters, both fresh and saline (Wetzel, 1975). Dilute solutions of alkalis and alkaline earth compounds, particularly bicarbonates, carbonates, sulfates and chlorides dominated in the ionic composition of fresh waters. Therefore, the concentrations of four major cations (Ca2+, Mg2+, Na+ and K+) and four major anions already mentioned (HCO3-, CO3-, SO4- and Cl-), usually constitute the total ionic salinity of the water (Wetzel, 1975). Salinity is best expressed as total ion concentration in mg per liter (Wetzel, 1975). In practice, it is usual to determine salinity in two ways: by measuring total dissolved solids (TDS) and expressing them as milligrams per liter (mg/l TDS) or by measuring specific conductivity of water and expressing it as micro Siemens per centimeter (µS/cm) (Waiser and Robarts, 2009).

Waiser and Robarts (2009) classified lakes according to TDS, specific conductivity and salinity in several groups. Freshwater lakes have TDS less than 500 mg/l, conductivity less than 850 µS/cm and salinity less than 0.5‰, while subsaline lakes are those whose TDS ranges from 500 to 3000 mg /l, conductivity ranges from 850 to 5500 µS/cm and salinity ranges from 0.5 to 3‰. Saline lakes can be further differentiated into hyposaline (TDS: 3000-20000 mg/l; Conductivity: 5500-30000 µS/cm; Salinity: 3-20‰), mesohaline (TDS: 20000-50000 mg/l; Conductivity: 30000-70000 µS/cm; Salinity: 20-50‰), and hypersaline (TDS: >50000 mg/l; Conductivity: >70000 µS/cm; Salinity: >50‰). Seawater has TDS of 35000 mg/l, conductivity of 53000 µS/cm and salinity of 35‰.

When inland saline lakes considered, there are both natural and artificial ones. The chemical composition of these waters is mainly governed by the composition of influents from the drainage basin (Wetzel, 1975). Therewith, the other important source of salts is from springs rich in minerals leached from underground rocks and sediments (Waiser and Robarts, 2009). Additionally, determinants of salinity are surface catchment geology, the evaporation and precipitation ratio, the composition of atmospheric precipitation, climate, soil age, distance from the sea (dry ion deposition), etc (Wetzel, 1975; Marić and Rakočević, 2009; Waiser and Robarts, 2009).

High water salinity induces an osmoregulatory stress on organisms not adapted to these conditions (Cvijan, 2013). The term osmoregulation refers to the maintenance of the stable internal cell ion concentration by the regulation of ion content across a semi-permeable cell membrane (Waiser and Robarts, 2009). Halophiles are organisms adapted to life in saline environments and they overcome the problem by accumulating organic solutes like glycerol, sucrose and glycine within their cells (Waiser and Robarts, 2009; Cvijan, 2013). Most of the organisms living in subsaline and hyposaline lakes are rather halotolerant species than the true halophilic species, while halophiles are obligatory hypersaline environment inhabitants. These specific ecosystems usually have simplified food web with a very small number of organisms adapted to an osmoregulatory stress. Among algae, halophilic green flagellate - Dunaliella salina (Dunal) Teodoresco is frequently cited example as the main or sole primary producer present worldwide in hypersaline environments (Stephens and Gillespie, 1976; Cvijan, 2013; Wehr and Sheath, 2015).

Bearing in mind all of the above, it can be expected saline lakes to be distinguished by a particular structure of the phytoplankton community. Because of that, one artificial saline lake with high values of conductivity near Kikinda city (Vojvodina province, Republic of Serbia) was selected for investigation of the phytoplankton community. Phytoplankton of this water body has never been explored earlier, but in the Vojvodina province there are several natural saline lakes or marshes studied before which can be classified as subsaline or hyposaline according to Waiser and Robarts (2009) (Subakov-Simić et al., 2004, 2006, 2007; Cvijan and Krizmanić, 2009; Fužinato et al., 2010; Cvijan and Fužinato, 2011).

 

Materials and Methods

Study Area

Field measurements and collecting of samples for chemical and phytoplankton analyses were conducted on 18th July 2018 from the shore in one artificial lake near Kikinda city. This is shallow water body (<1m) with a clay bottom. There are several similar water bodies placed nearby. One of them, the Plava Banja lake, has been redesigned into the popular resting area and in this lake Chara canescens Loiseleur was detected for the first time after more than 10 years in Serbia (Trbojević et al., in press). All of these artificial lakes were made by clay digging by local company Toza Marković from the Kikinda city and one by one were abandoned. They are characterized by high conductivity (>8000 µS/cm) and consequently high salinity (http://www.zavodki.org.rs).

 

Measuring of Physical and Chemical Parameters

Conductivity, pH and temperature of water were measured in situ using digital field Eutech Instruments Oakton® instruments. Samples for chemical analyses were collected by a plastic bottle on the field, put in the transport fridge and transported to the laboratory. Chemical analyses were done by standard analytical methods (APHA, 1995) in the Institute of Public Health of Serbia "Dr Milan Jovanović Batut" in Belgrade.

 

Collecting and Analyses of Phytoplankton Community

Samples for determination of chlorophyll-a concentration and qualitative phytoplankton analysis were collected by submerging and filling a plastic bottle (1 liter) with water, about 10 cm below the surface. The sample for qualitative phytoplankton analysis was taken using a plankton net (mesh size 22–23 mm, net frame 25 cm ø). Samples for qualitative and quantitative phytoplankton analyses were preserved in Lugol's solution (at ratio 1:100) according to the European standard EN 15204 (2008).

In laboratory of the Department of Algology, Mycology and Lichenology in the Institute of Botany and Botanical Garden "Jevremovac" (Belgrade), the standard spectrophotometric method (ISO 10260:1992 (E)) was used for determination of chlorophyll-a concentration from the water sample and obtained values were expressed in micrograms per liter (µg/l). The Carl Zeiss AxioImager M.1 microscope equipped with a digital camera AxioCam MRc5 and AxioVision 4.8 software for manipulation of micrographs was used for detailed phytoplankton observation. Identification of the particular algal taxa in the plankton community was made using a standard taxonomic literature (Huber-Pestalozzi et al., 1983; Starmach, 1983, 1985; Komárek and Anagnostidis, 1998, 2005; John et al., 2002; Hofmann et al., 2013). The Utermöhl method (Utermöhl, 1958) was carried out for quantitative phytoplankton analysis on the Leica DMIL inverted microscope. Results were expressed as a number of cells per milliliter. Additionally, phytoplankton biomass was determined according to the standard formula for biovolume of algal taxa (Hillebrand et al., 1999; Sun and Liu, 2003) and obtained data were expressed in micrograms per liter (µg/l).

The diversity of the phytoplankton community was calculated according to the Shannon (1948). Level of water pollution based on obtained Shannon index values was assessed according to Wilhm and Dorris (1968) and Wilhm (1970). These authors based water quality assessment on fact that the values of diversity index are higher in clear than in polluted water, so values of Shannon index below 1 indicate very polluted water, between 1 and 3 moderately polluted and values above 3 correspond to clear water (Wilhm and Dorris, 1968; Wilhm, 1970).

 

Results and Discussion

Ecosystems with increased salinity have always been interesting because of their specific flora and fauna. Generally, saline inland waters are characterized by exceptionally high mineralization of their water and consequently high conductivity and pH values (Cvijan and Krizmanić, 2009). High conductivity and pH values characterized investigated lake near Kikinda city as well (Table 1). According to Waiser and Robarts (2009) and taking into account measured values of conductivity it can be classified as hyposaline one. Shallow saline inland waters, especially those depending on groundwater and atmospheric precipitation, can fluctuate their water level strongly and consequently change the level of salinity (Subakov-Simić et al., 2007; Cvijan and Krizmanić, 2009). Water level fluctuations occur in investigated lake, but it never dries up. In the period of low water, when the water is withdrawn, the shore remains with white scum on it, which is actually a salt. It is important to stress out that detailed chemical analyses had not been conducted, so we cannot be sure which ions contribute the most to high conductivity. Bearing in mind that chemical analyses of similar artificial saline lake nearby, the Plava Banja pond (similar depth, base of the bottom and the same origin and macrophytic vegetation), were done about 10 days before our sampling time and showed that sulfates, chlorides and bicarbonates contribute the most to high conductivity in that pond (Trbojević et al., in press), it can only be assumed that the same ions, beside Mg2+ ion, are responsible for high conductivity in investigated lake (Table 1).

 

tab01

 

A total number of 27 algal taxa belonging to 5 divisions was detected (Table 2). The most numerous divisions were Cyanobacteria (7), Chlorophyta (7) and Euglenophyta (6), followed by Bacillariophyta (5) and Chrysophyta (2). Merismopedia tenuissima, Spirulina major, Cosmarium leave var. octangulare, Euglena intermedia, Phacus pleuronectes and Phacus undulates have already been detected earlier in hyposaline lakes Slatina and Pečena Slatina (Subakov-Simić et al., 2004, 2006). Among other detected algal taxa, there are few characteristic for saline or brackish water - Oocystis submarina, Merismopedia warmingiana, Euglena proxima (Huber-Pestalozzi et al., 1983; Komárek and Anagnostidis, 1998; Subakov-Simić, 2006). However, the majority of detected phytoplankton taxa can be characterized as halotolerant taxa rather than halophilic ones. Previous study of saline inland water in Serbia (Velika Slatina and Pečena Slatina) revealed some specific and interesting algal taxa - Anabaena bergii Ostenfeld and Arthrospira fusiformis (Voronichin) Komárek & J.W.G. Lund (Cvijan and Krizmanić, 2009; Fužinato et al., 2010). Those species were detected for the first time in Serbia in mentioned saline ecosystems, but in our study none of them was found.

 

tab02

 

Further, phytoplankton community of the hyposaline lake near Kikinda city is characterized by low chlorophyll-a concentration (12.8 µg/l) and low biomass (855.7 µg/l), but quite a high abundance of cells (20882 cell/ml). The recorded phytoplankton biomass in this study is about fourfold lower than biomass recorded in an earlier study of a similar ecosystem with approximately the same values of conductivity (Subakov-Simić et al., 2007), but the value of abundance is about ten times higher. This is due to the small-dimension algae dominance in phytoplankton community from hyposaline lake near Kikinda city. Bearing in mind that the primary production of investigated phytoplankton is not high, it seems those results also confirm that biomass is a better provider of information about plankton production than abundance (Predojević, 2017). On the other hand, salt tolerant organisms expend a great deal of energy in osmoregulation, but a decreasing ratio of surface and volume seems to be one of the advantages in those environments (Waiser and Robarts, 2009), which is accomplished by small dimensions of algae. Additionally, Suthers and Rissik (2008) pointed out that chroococcalean cyanobacteria are considered to be better competitors in comparison to the larger-celled species of other cyanobacterial groups and eukaryotic algae at lower concentrations of dissolved phosphorus. Considering that chroococcalean cyanobacteria (Merismopedia warmingiana and Aphanocapsa delicatissima) contribute with 70% to the total cell abundance in the investigated lake, it can be assumed that small dimensions of these as well as other small-dimension taxa represent the response to low nutrient conditions (Table 1). The dominance of small-dimensions chroococcalean cyanobacteria is obvious when the percentage share of particular algal division in the total phytoplankton biomass and abundance are considered and compared (Figure 1 and 2). So, small dimensions of representatives of algae in the investigated plankton community could be a consequence of low nutrient loading in this lake as well as a consequence of the osmoregulation process. Additionally, green algae dominate in total phytoplankton biomass, followed by diatoms and blue-green algae (Figure 2). Representatives of these three divisions are most often cited as characteristic inhabitants of saline waters with the dominance of green algae when lake salinity exceeded 10‰ (Waiser and Robarts, 2009).

 

fig01
Figure 1: The percentage share of particular algal division in the total phytoplankton number of cells in the hyposaline lake near Kikinda city.

 

fig02
Figure 2: The percentage share of particular algal division in the total phytoplankton biomass in hyposaline lake near Kikinda city.

 

During collecting of phytoplankton samples, very abundant submerged vegetation was noticeable. It covered about 95% of the bottom of this shallow water body (depth was <1m). Further, there was a fragmented population of Phragmites australis (Cav.) Trin. ex Steud. along shore.

According to the theory of alternative stable states (Scheffer et al., 1993; Scheffer and van Nes, 2007), one of the stable equilibrium in shallow water ecosystem is achieved by a balance between dense development of macrophytes and phytoplankton which is characterized with low biomass, low abundance and high diversity. Abundant macrophytes were developed in hyposaline lake near Kikinda city as well as low biomass of phytoplankton, but, contrary to the mentioned theory, low diversity was detected (Shannon index is 1.47). This deviation is not surprising considering that species diversity generally inversely related to lake salinity (Waiser and Robarts, 2009; Wehr and Sheath, 2015), so it can be concluded that equilibrium between macrophytes and phytoplankton is achieved and maintained. Additionally, the water of the investigated lake can be considered as moderately polluted based on diversity index (Wilhm and Dorris, 1968; Wilhm, 1970), but salinity does not necessarily have to be a reflection of the pollution. So, in this case it's more likely that this value of Shannon index is a reflection of specific conditions with a reduced number of species able to tolerate them.

The last, but not the least is the fact that there are many benefits from salty inland lakes. Species adapted to these habitats produce commercially important products such as glycerol and β-carotene (Cvijan, 2013; Waiser and Robarts, 2009), so they can be a significant source of these substances and in accordance with that these ecosystems should certainly be protected.

 

Conclusion

Phytoplankton community in the artificial, hyposaline lake near Kikinda city has been investigated for the first time. This ecosystem is characterized by high conductivity (8180 µS/cm) and very abundant submerged macrophytes. Phytoplankton community is rather composed of halotolerant than halophilic species with a total of 27 identified taxa. Obtained values of biomass and concentration of chlorophyll-a point to low phytoplankton production, which is in accordance with the equilibrium state established in this ecosystem where macrophytes dominance is present. In that alternative stable state, high diversity of phytoplankton is expected, but in this shallow, saline lake it does not occur. The low value of diversity index in phytoplankton of this investigated lake is reflection of the specific, salty conditions, so mentioned situation with low phytoplankton biomass and diversity balanced with abundant macrophytes development could be understood as a modification of the stable state in the shallow lake with macrophyte dominance.

Bearing in mind that saline inland waters hide specific flora and fauna, one sampling time is not enough for those to be discovered. More detailed and numerous analyses of phytoplankton community are needed as well as detailed monitoring of dynamic of physical and chemical parameters which would contribute to the better understanding of this ecosystem.

 

Acknowledgments

This research was supported by the Ministry of Education, Science and Technological Development, Republic of Serbia, Project No. OI 176020 and Rufford small grant project- Guardians of the Fragile Equilibrium in the Shallow Ecosystems of a Ramsar Sites in Serbia: Stoneworts Diversity and Distribution (leader: Ivana Trbojević). The authors would also like to thank Mr. Nebojša Krištof for technical and field support.

 

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