Monitoring planktonic cyanobacteria in Lake Maninjau, West Sumatra, Indonesia

Harmful Cyanobacterial blooms are global environmental issue. Some efforts have been made to prevent and minimize their occurrence in waters. This study aims to monitor the planktonic Cyanobacteria community and environmental factors that influence their dominance in Lake Maninjau. Samples of Phytoplankton and water quality data were collected in 2001, 2005, 2009, 2014, 2015, 2016, 2018, and 2019. Twenty-four species of planktonic Cyanobacteria which belonged to orders Chroococcales, Oscillatoriales, and Nostococales. Percentage of Cyanobacteria abundance ranged from 2.9% to 95.32%. High percentage of Aphanocapsa (76.21%), Anabaena (33.25%), Chroococcus (86.4%), Microcystis aeruginosa (94.37%), Oscillatoria (50.94%), and Aphanizomenon gracile (72.43%) was recorded in different periods. Cylindrosprmopsis raciborskii was often found in the lake with percentage of abundance not more than 20.75%. Cyanobacteria abundance ranged from 734.2 to 4,180,867 individualL-1. The lowest Cyanobacteria abundance was characterized by low total phosphorus and conductivity. High Cyanobacteria abundance was related to the high levels of TP, concentration, conductivity and low TN/TP ratio. Nutrient, conductivity, and temperature were also the factors that influenced the dominance of Cyanobacterial species in Lake.


Introduction
Cyanobacterial blooms are global environmental issues because of their ability to produce toxins material which has detrimental effects on the aquatic ecosystem [1].Cyanobacterial blooms produce cyanotoxins, which pose a threat to human health, animals, and stability of aquatic ecosystems [2].Cyanotoxins not only deteriorate water quality but also they have an impact on human health and socioeconomic aspect [3].Cyanobacterial blooms enhance turbidity and eliminate oxygen, resulting in hypoxia and anoxia which cause fish kills in waters.Some species of Cyanobacterial which have been identified, contain cyanotoxin such as Microcystis, Planktothrix, Aphanizomenon, Oscillatoria, Lyngbya, Nodularia, Nostoc, Anabaena, Anabaenopsis, and Cylindrospermopsis [4].Rising CO2 and global warming are major factors influence Cyanobacterial blooms in many aquatic ecosystems worldwide [5].
In Indonesia, eutrophication has a serious problem in inland waters, which influence water quality degradation and Cyanobacteria bloom.Land use change, urbanization, agricultural activities, and fish culture in lakes are major sources of nutrients which cause eutrophication and Cyanobacterial blooms 1260 (2023) 012018 IOP Publishing doi:10.1088/1755-1315/1260/1/012018 2 in waters [6,7].In Indonesia, Cyanobacterial bloom events have already occurred in many inland waters, Cyanobacterial species which commonly bloom are Microcystis aeruginosa and Planktothrix agardhii, and dominant species waters such as Cylindrospermopsis raciborskii, Aphanizomenon sp., Anabaena spp., and Oscilatoria spp.[7,8,9].Microcystis bloom events has been occurred several times in Lake Maninjau [8].The problem of eutrophication in this lake was reported because of increasing fish culture activity in lake.Lake Maninjau with the surface area of 9,737.50ha and the average depth of 105 m has been utilized for fish culture since 1996.Lake Maninjau located at tropical area, has two peak rainy seasons with rainfall relatively high over of the year (Figure 1, Figure 2).Fish culture in lake and climate condition could stimulate cyanobacterial growth in waters as Lake Maninjau.
Microcystis blooms in this lake caused odor problems, deteriorating water quality, and massive fish kills leading to economic loss.Some efforts have been made to reduce Cyanobacterial blooms and eutrophication risks in Lake Maninjau by flushing Microcystis biomass through a natural outlet, publishing regulations for fish culture in the lake, and introducing technology to reduce nutrient load.However, there is limited information about the dynamic of Cyanobacteria related to the water quality as an impact of eutrophication and fish culture activities in Lake Maninjau.During the non-blooming period of Microcystis, the dominant species of Cyanobacteria are represented by Cylindrospermopsis raciborskii, Anabaea affinis, Aphanizomeon sp., Chroococcus sp., Planktolyngbya sp., and Oscillatoria [8].Cyanobacterial species such as Cylindrospermopsis raciborskii, Anabaea affinis, Aphanizomeon sp., Chroococcus sp., and Oscillatoria sp. are known to produce toxins [4].Anthropogenic activities and climate condition can cause significant shifts in Cyanobacteria communities resulting in overdominance in waters [10].Therefore, monitoring Cyanobacteria and water quality is important to recognize the level of water quality status related to Cyanobacteria during eutrophication mitigation and fish culture activities in Lake Maninjau.Monitoring is also important to know the factors that limit Cyanobacterial blooms and to prevent the future blooming in the lake.This information is important to improve the management of the lake.This study aims to monitor Cyanobacteria community and environmental factors which influence their dominance in Lake Maninjau.

study site and sampling
Water sample and Phytoplankton sample were collected in surface (0 m) and subsurface water (0.5 x Secchi depth) in period for controlling Cyanobacteria bloom (May, September October) 2001), periods after controlling Cyanobacteria bloom ( May) 2005), periods with high level of fish culture activity (April 2009, July 2009, April 2014, August 2015, March 2016), period of Cyanobacteria blooms occurred in Lake Maninjau (April ) 2018 and periods after Cyanobacteria bloom (July to November) 2018 then continued in (February, April, and May) 2019.
In this study, nine (9) sampling sites were surveyed (Figure 1).Description of the sampling sites was divided based on the distribution of fish culture activity and surrounding are condition.There were area packed with fish culture and around area was settlement and agriculture (Bayur, Sigiran, Sungai Batang), area with a few of fish culture and surrounding area was agriculture (Koto Kadang and Pandan), area with a few of fish culture near out let of lake (Muko2) and area no fish culture activity represented in middle part of lake (DM 4 and DM 7).Water temperature, pH, dissolved oxygen (DO) concentration, and conductivity were measured directly on site using a water quality checker (Horiba U-10).
Phytoplankton samples were collected by using Kemmerer water sampler and then 2 L of water sample was filtered through 40 µm mesh size of plankton net.The phytoplankton samples were promptly preserved using Lugol's solution, while the water samples intended for nutrient analysis were stored in 300 ml plastic bottles to be analyzed in the laboratory

Sample and data analysis
Measurement of water quality parameters including nutrient were performed according to standard method of the American Public Health Association (11).Total nitrogen (TN) was measured using persulphate digestion and the liberated nitrate was determined by using brucine method.Total phosphorus (TP) was determined using persulphate digestion and the phosphate was analyzed using ascorbic acid method.Phytoplankton species were identified according to some book references [12,13,14].Cyanobacterial species were counted in a filament or colony based on the morphology of species and phytoplankton abundance was counted with a Sedgwick-Rafter counting chamber under magnifications of x 400.[11].A Canonical Correspondence Analysis (CCA) was conducted to know the responses of cyanobacteria to environmental changes.

Water quality condition.
During observation, temperature showed an insignificant variation, which is commonly found in tropical area (Table 1).Conductivity ranged from 0.08 to 0.140 mS -cm , showing that Lake Maninjau is rich in nutrient.Potential hydrogen (pH) ranged from 7.33 to 8.91, which indicates alkaline condition of lake.DO concentration showed a wide range of values (2.87 to 8.83 mgL -1 ) during the observation.Eutrophication is a factor causing a large variation of DO concentration in the lake.In a eutrophic lake with high density of algae, photosynthesis process and respiration lead to a large variation of DO concentration.High intensity of solar radiation during the day of photosynthesis process increases the DO concentration and inversely, lower intensity of solar radiation causes less photosynthesis to produce oxygen [15].On the other hand, in a eutrophic lake, decomposition process of dead phytoplankton deposited in a tropholytic zone may cause oxygen depletion and decrease aerobic zone and low DO concentration was found in the epilimnion.Concentration, of total nitrogen (TN) and total phosphorous (TP) showed fluctuation in the study period (Table 1).After controlling Microcystis blooms in May 2005, a decrease of TN and TP was observed.Furthermore, fish culture activities continued to increase in April, exceeding the carrying capacity of the lake.High TN and TP concentration was observed, and high Cyanobacteria abundance was recorded in April 2018.After Microcystis bloom, TN and TP concentration decreased which is probably used for Microcystis growth.TP depletion was also recorded in high precipitation periods as in October and November 2018.Low TP concentration in this period could be related to precipitation dilution, while TN concentration increased in February to May 2019, could also because of precipitation effect which increase TN load from runoffs.The fluctuation of nutrient concentration (TN and TP) in the lake apparently gives an effect on nutrient limitation and Cyanobacteria abundance (Table 1).TN/TP ratio showed a wide range of value from 4.7 to 1015.The value of TN/TP ratio < 21.5-24.7 indicate N limitation, while the value of TN/TP ratio > 21.5-24.7 indicate P limitation [16].Based on the TN/TP ratio value, mostly Lake Maninjau showed N limitation condition.The lowest TN/TP ratio (4.7) was indicated by the highest Cyanobacteria abundance or Cyanobacterial blooms.However, low TN/TP ratio in this lake was not always followed by the higher abundance of Cyanobacteria.It might have been related to factors such as non-uniform species composition of phytoplankton, in which each species needed a different nutrient requirement.The other factor is the nutrient availability, such as phosphorus bound in particles, may not be entirely available for phytoplankton [17]

Cyanobacteria abundance
Cyanobacteria abundance is presented in Table 1.Cyanobacteria abundance showed a wide range value (0.734 x 10 3 to 4,180.87 x 10 3 individual L -1 ).The variation of Cyanobacteria abundance could be related with environmental factors such as nutrient, precipitation, temperature, and lake stratification [18].The lowest Cyanobacteria abundance in May 2005 coincided with the water quality condition (Table 1).The lowest Cyanobacteria abundance, conductivity, nitrogen, and phosphorus concentration indicated a good condition during the observation.Inversely, highest abundance of Cyanobacteria was indicated by high TN and TP concentration (Table 1).High abundance of Cyanobacteria (4,180.87x 10 3 individual L -1 ) characterized algae blooms in this lake.Nutrients (TN and TP) are the main factors influence of Cyanobacterial blooms [19].The highest of concentration of TN and TP characterized by Cyanobacterial blooms.It showed that concentration of TN (1.117 mg L -1 ) and TP concentration (0.229 mg L -1 ) is limiting nutrient for Cyanobacteria bloom in Lake Mannjau.Other study reported to limit Microcystis blooms, nutrient concentration should below 0.80 mg -1 for TN and 0.05 mg L -1 for TP [20].In Lake Maninjau, higher concentration of TN and TP was not always followed by high abundance of Cyanobacteria (Table 1).It may have been correlated with the dominant species of Cyanobacteria in each period which may had a difference in the environmental parameter for their growth.Each species has a different environmental requirement for the phytoplankton growth [21].Relative abundance of Cyanobacteria (Cyanophyta) showed a wide range of value (Figure 3).Cyanobacteria contributed to total phytoplankton abundance ranging from 2.9 % to 95.32% during the period of study (Figure 3).A similar phenomenon was recorded in the other groups of Bacillariophyta, Chlorophyta, and Pyrrophyta, contributing 1.75% to 88.43%; 0.37% to 93.34%; and 0.44% to 57.79% respectively.Relative abundance of Euglenophyta was exceptionally low compared to the other groups of phytoplankton.A wide range of relative abundance of Cyanobacteria and the other groups of phytoplankton showed an unstable condition of Lake Maninjau.Compared to the other groups of phytoplankton, high relative abundance of Cyanobacteria occurred several times during the observation (Figure 3).The changes of hydro-climatological such as precipitation, nitrogen and phosphorus concentration could influence phytoplankton composition [34].CCA analysis also showed that in general, TP influenced the relative abundance of Cyanobacteria while TN concentration and TN/TP ratio influence relative abundance of Pyrrophyta (Figure 4).As reported, the dominance of Peridinium spp. is related to the sufficient supply of nitrogen [22].

Relative Abundance of Major Species
There are nine major species of planktonic Cyanobacteria in Lake Maninjau, namely Aphanocapsa sp., Aphanomizon gracile, Anabaena sp., Cylindeospermopsis raciborskii, Chroococcus sp., Microcystis aeruginosa, Merismopedia sp., and Oscillatoria formosa.The high relative abundance of major species changed during the observation (Figure 5).Although cyanotoxin has not been evaluated in Lake Maninjau, most of Cyanobacterial species are capable of producing potent toxins [23,24,25].Aphanocapsa sp.contributed 76.2% to the total abundance of phytoplankton recorded in May 2001, while Chroococcus sp. and Microcystis, which contributed 86.4% and 94.37%, were recorded in March 2016 and April 2018, respectively.The of Aphanocapsa was related to water temperature.High abundance of Microcystis in April 2018 was characterized by highly visible scums in the surface waters.In Lake Maninjau, it was recorded that Aphanizomenon sp.contributed 72.43% in November 2018, while Oscillatoria contributed 50.94% in August 2018.Cylindrospermopsis raciborskii did not show high percentage of abundance, but this species was often found during the observation.As reported, Cyanobacterial responses to environmental conditions can be specified based on taxon [26].Canonical Correspondence Analysis (CCA) showed that TN and TP concentration and TN/TP ratio were associated with Microcystis abundance, while Chroococcus sp. and Cylindrospermopsis were likely to prefer an environmental condition with high temperature and pH (Figure 6).Others studies reported that cyanobacteria blooms especially Microcystis was occur in a condition with low TN/TP ratio [27,28].High TN/TP ratio influenced high relative abundance of Aphanizomizon and Merismopedia sp.It indicates that Aphanizomenon could grow vigorously under rich nitrogen concentration and phosphorous deficiency.As reported, lakes rich in nitrogen can support the growth of diazotrophic species such as Aphanizomenon [29].The growth of Aphanizomenon under phosphorus deficiency is probably related to their ability to use organic P from enzymatic process which takes from either intracellular or extracellular sources [30,31].A study also reported that Merismopedia, which is non-nitrogen-fixing Cyanobacteria, dominates in water with high nitrogen concentration [32].

Cyanobacteria Composition and Species Distribution
Cyanobacteria composition consists of three orders, namely Chroococales, Oscillatoriales and Nostococales (Figure 7).Chroococales was more diverse with twelve species, then followed by Nostococales and Oscillatoriales with seven and six species, respectively.There were twenty-five species of Cyanobacteria found in Lake Maninjau (Table 2).Spatially, some species of cyanobacteria such as Microcystis sp., Chroococccus sp., Cylindrospermopsis raciborskii showed a wide range distribution as recorded in all site observation.Those three species are commonly recorded in eutrophic or rich of nutrient [34,35] such as in Lake Maninjau.Microcystis aeruginosa is abundance in water ecosystem with the high concentration of nutrient in waters [36].Cylindrospermopsis raciborskii is also known as a cosmopolitan species which is tolerance to nutrient deficiency could adapted to the wide range of temperature and light regime [34,37].During observation, low species number of Cyanobacteria was found in Koto Gadang (K.Gadang) station and Pandan station, while the high number species of cyanobacteria was found in Muko2 station and Sungai Batang (S.Batang) station (Table 2).Koto Gadang is a station with a few of fish culture in floating cage which probably low input of organic material from fish culture activity as nutrient source for cyanobacteria growth.Similar environmental condition was also found in Pandan station.Inversely, Sungai Batang is a station which used for fish culture with surrounding area is agriculture could receive more nutrient source and increase cyanobacteria growth.Muko2 is a station near outlet of lake, therefore many species of phytoplankton flow out from the lake through this station.
Aphanocapsa sp.Chroococcus sp., Microcysis aeruginosa, and Merismopedia spp.are major species belong to Chrocooccales order while Oscillatoriales was represented by Oscillatoria spp.(Figure 7).The major species of Nostocales was represented by Anabaena spp., Cylindrospermoposis raciborskii, and Aphanaizomenon gracile.There was a shift in Cyanobacteria composition from Chroococales to Oscillatoriales and then Nostococales.Temporally, there was also a shift dominant species (Table 3).Aphanocapsa sp., Microcyatis, Aphanizomezon gracile and Merismopedia sp. were abundance in May 2001, April 2018, November 2018 and in April 2019 respectively.It apparently that the changes of water quality condition such nutrient, temperature, hydrological and climate also influenced species composition and of Cyanobacterial in Lake Maninjau.Low number of species in April 2019 could be related with high abundance of Merismopedia sp. and Cylindrospermopsis raciborskii.It indicates that only these two species were able to adapt to the environmental condition in this period, which was characterized by higher temperature, TN, and lower pH.Microcystis aeruginosa was always found in Lake Maninjau and formed blooms in April 2018.In this study, high concentration of TN and TP was apparently the factors control Microcystis bloom.Therefore, nutrient limitation is important to prevent Microcystis blooms in Lake Maninjau.Cylindropermopsis raciborskii was often recorded in Lake Maninjau, but this species did not show high relative abundance during the study period.A study reported that high biomass of Cylindrospermopsis is related to high temperature and shallow depth of a lake [33].
Aphanizomenon was often recorded in Lake Maninjau and reached high relative abundance in November 2018.This species has a number of adaptations and life strategies to compete successfully against other phytoplankton species.Among the adaptations is that Aphanizomenon is able to grow rapidly in conditions of TP depletion and low light intensity [23,29,34].Although cyanotoxin has not been assessed, most of Cyanobacterial species in Lake Maninjau are toxigenic [23,24,25].

Conclusion
Cyanobacteria composition was represented by twenty-four species belonging to three orders: Chroococales, Oscillatoriales and Nostococales.There was a shift in Cyanobacteria composition from Chroococales to Oscillatoriales then Nostococales and fluctuation of Cyanobacteria abundance.The shifting of Cyanobacteria composition and abundance was apparently related to the dynamic of water quality.The lowest Cyanobacteria abundance was characterized by the lowest TN, TP, and conductivity concentration which indicated a good condition of Lake Maninjau.Inversely, the highest Cyanobacteria abundance was characterized by high TN and TP concentration or indicated Microcystis bloom condition.These results can subsequently be used as the basis for water quality management to prevent Microcystis blooms in Lake Maninjau.

Figure 1 .
Figure 1.Location map of research area and sampling site (indicated by blue circle) in Lake Maninjau, Indonesia.

Figure 2 .
Figure 2. Recorded precipitation in the research area from 2018 to 2019.

Figure 3 .
Figure 3.The relative abundance (%) of Cyanobacteria and other phytoplankton divisions.

Table 1 .
Average Physical and Chemical Conditions and Cyanobacteria Abundance of Lake Maninjau.

Table 2 .
Spatial distribution of cyanobacterial species in Lake Maninjau.

Table 3 .
Temporal Distribution of Cyanobacterial Species in Lake Maninjau.

Table 3 .
Distribution of Cyanobacterial Species in Lake Maninjau.