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All issues Volume 56 (2020) Ann. Limnol. - Int. J. Lim., 56 (2020) 18 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 56, 2020
Article Number 18
Number of page(s) 10
DOI https://doi.org/10.1051/limn/2020015
Published online 24 July 2020

© EDP Sciences, 2020

1 Introduction

Cyanobacteria are photosynthetic aquatic or terrestrial prokaryotes that are small, unicellular, often found in colonies and are also known as “blue-green algae” (Shestakov and Karbysheva, 2017). They are the most genetically diverse group and can exist in various habitats like freshwater, marine water and even extreme environment like frozen lakes, salt works and hot springs (Whitton, 1992). Eutrophication has led to the availability of excessive nutrients that leads to algal blooms causing negative impacts on animals and humans. Increased input of nitrogen and phosphorous from various anthropogenic activities into the water bodies substantially favours frequent algal blooms. Frequency and occurrence of harmful cyanobacterial blooms (CyanoHABs) have increased globally in recent years and has been attributed to climate change and eutrophication. Apart from eutrophication, climate change and spread of invasive species has led to variations in aquatic species compositions and alterations in the food web (Paerl and Huisman, 2009; O'Neil et al., 2012; Knoll et al., 2015). One of the characteristic that makes cyanobacteria prevalent during summer blooms when compared to other species of algae is their ability to proliferate at high temperature (Litchman et al., 2010). Temperature increase could minimise vertical mixing, intensifies and prolongs vertical stratification and could make the environment more stable for Microcystis (Livingstone, 2003; Paerl and Huisman, 2009).

M. aeruginosa is considered as one of the main ecologically detrimental species due to its abundance in freshwater bodies that have varying nutrient loading and its degree of toxicity towards the terrestrial as well the aquatic organisms (Carmichael, 1992; Chorus and Bartram, 1999). Since they are capable of producing cyanotoxin named microcystin they are a major concern to the environment and public health. Microcystin is a hepatotoxin and various cases of human poisoning and mortality of fishes and mammals have been reported (Miller et al., 2010; Tanabe et al., 2018). Microcystin toxins are very stable in nature and are not affected by proteolytic or any hydrolytic attack. They can persist in filter feeders and can finally end up in humans via the food chain (Yu et al., 2009; Chen et al., 2009). These harmful algal blooms could pollute the water bodies with the toxin thereby causing the death of livestock and aquatic animals. M. aeruginosa is usually present in freshwater but their presence has also been reported in brackish water ecosystems. Their invasion from the freshwater to brackish water bodies has been less investigated (Tanabe et al., 2018). Since the potentially toxic Microcystis species are capable of producing microcystin and can have adverse effects on the aquatic ecosystems as well as to humans and other mammals, a detailed study in these aspect stands significant. The present study investigates on the prevalence of Microcystis species as well as their development as blooms in the freshwater ecosystems of central Kerala, south India.

2 Materials and methods

As a part of monitoring cyanobacterial blooms, a preliminary survey of various aquatic ecosystems along central Kerala was carried out. Two freshwater ponds at Ernakulam district of Kerala, Station 1 (Lat. 9°58′6.7″N; Long. 76°16′56.8″E) and Station 2 (Lat. 9°57ʹ34ʺN; Long. 76°17ʹ32ʺE) with Microcystis bloom were selected for monitoring from May 2019 to February 2020 (Figs. 1 and 2).

Quantitative and qualitative analysis of water samples were carried out under a Leica DM 2000 light microscope. Identification of algal species was done with the help of existing literature and standard identification keys (Desikachary, 1959; Rosen and Amand, 2015). Quantitative estimation of algal cells was carried out using Sedgewick- Rafter counting cell. Algal bloom was collected from the ponds by filtering using 63 μm sieve for isolation using BG-11 media and storage for further studies. Isolation was done by single-cell isolation and serial dilution followed by agar plating method (Andersen, 2005). SEM images of Microcystis were also captured for detailed taxonomic analysis. Physico-chemical parameters like temperature, salinity, pH were measured with a digital thermometer, refractometer and pH meter respectively. Dissolved oxygen was estimated by Winkler's method (Winkler, 1888). Major nutrients such as nitrate, phosphate and silicate were estimated by following Grasshoff et al. (1983). Chlorophyll a was determined using 90% acetone extraction method using Hitachi UV-VIS spectrophotometer (Parson et al., 1984). Toxicity studies were conducted by exposing seeds of Oreochromis mossambicus to Microcystis aeruginosa bloom. Tissue samples like gills, liver and heart of exposed fish were collected, fixed in 10% neutral buffered formalin for 24 hours, dehydrated and paraffin-embedded. Fine sections of tissues were mounted on a clean glass slide and stained with hematoxylin and eosin stains (Sanad et al., 2015; Abdel-Latif and Khashaba, 2017). These sections were viewed under the microscope to study the histological changes due to the toxin.

thumbnail Fig. 1

Study area. Red star represents the location in Kochi (Kerala) from where M. aeruginosa bloom was recorded.
thumbnail Fig. 2

M. aeruginosa bloom with green scum floating in the surface. (A) Station-1 (B) Station-2.

3 Results

The analysis of surface water samples of station 1 and 2 showed the persistent presence of cyanobacteria M. aeruginosa. The occasional bloom of M. aeruginosa was observed from the study areas as green free-floating scums formed of densely packed colonies and some dried benthic colonies of the species with an unpleasant odour. There was no sign of mortality of any aquatic species from the bloom area.

Massive blooms of M. aeruginosa (Figs. 2 and 3) was observed during the period prior to summer monsoon (May) with an abundance of 1.17 × 106 cells L‑1 (Station 1) and during the early summer monsoon (February) at station 2, later being more thick scum (2 × 108 cells L‑1). A decline in the cell density was noted at both the stations during monsoon season. In station 2, the coexistence of M. aeruginosa with Anabaena sp., was observed during the monsoon season which later got dominated by Microcystis sp. Light microscopic and SEM images of the species observed from the study area are shown in Figures 3 and 4. Other microalgae present along with the M. aeruginosa bloom at station 1 included Pediastrum sp., Scenedesmus sp., Chlorella sp., Spirulina sp., Woronichinia and diatoms but were found very meagre in cell number.

Seasonal variations in the physicochemical parameters obtained during the monthly monitoring of the study areas are depicted in Figures 5–10. Higher surface water temperature (31 °C) was recorded from both stations prior to monsoon. However, the temperature dropped to an average value of 27.2 °C during the monsoon season. The pH values at station 1 varied between 8.1 and 10.9 with peak value recorded during the end phase of the summer monsoon. At Station 2, the values ranged from 7.4 to 11.5 with higher values during the monsoon season. Dissolved oxygen estimated from station 1 varied between 3.41 ml L‑1 and 7.56 ml L1. Station 2 had dissolved oxygen ranging from 4.31 ml L‑1 to 11.08 ml L‑1. A noticeable decrease in dissolved oxygen was observed in both stations during the winter season. The salinity measured from both stations were zero. Chlorophyll a estimated was higher at station 1 (82.08 mg m‑3) prior to summer monsoon when the cell density was at its peak, which gradually decreased during the monsoon period to 20.42 mg m‑3. At station 2, chlorophyll a ranged from 38 mg m‑3 to 267.13 mg m‑3 with higher value observed during the monsoon season.

Moderate to high levels of nutrient concentrations were observed during the study period. Nitrate concentrations were high in the surface water (Station 1: 96.78 μmol L‑1 and Station 2: 43.149 μmol L‑1) prior to summer monsoon. Both the stations showed higher phosphate concentrations (Station 1: 19.889 μmol L‑1 and Station 2: 5.388 μmol L‑1) during the monsoon season. The peak concentration of silicate was observed during the monsoon season at Station 1 (194.105 μmol L‑1) and post summer monsoon at Station 2 (190.88 μmol L‑1).

Investigation on the stress response of candidate fish species (Oreochromis mossambicus) to exposure of M. aeruginosa bloom showed 100% mortality within 15 days of exposure. Tissues of control fishes retained the normal structure whereas moderate to severe histopathological changes were observed in the gills, liver and heart of fishes exposed to Microcystis bloom (Figs. 11–13) Structural changes in gills were noticed with the degeneration of primary and secondary lamella. Mild necrosis along with an increase in interlamellar space was also recorded. Liver of the test fish showed complete structural disruption. Vacuolar degeneration was observed in the hepatocytes. Severe necrosis of hepatocytes with inflammatory cells was present in the liver exposed to Microcystis bloom. Cardiac muscle cells showed fibrolysis and increased intercellular edema.

thumbnail Fig. 3

Microphotographs (LM) of Microcystis aeruginosa cells from bloom samples.
thumbnail Fig. 4

SEM images of (A) M. aeruginosa colony (B) M. aeruginosa single.
thumbnail Fig. 5

Variations in temperature, pH and dissolved oxygen in Station-1 during the study period.
thumbnail Fig. 6

Variations in temperature, pH and dissolved oxygen in Station-2 during the study period.
thumbnail Fig. 7

Variations in M. aeruginosa cell density (×105 Cells L−1) and chlorophyll a in station-1 during the study period.
thumbnail Fig. 8

Variations in M. aeruginosa cell density (×105 Cells L−1) and chlorophyll a in station-2 during the study period.
thumbnail Fig. 9

Variations in nutrient concentrations in Station-1 during the study period.
thumbnail Fig. 10

Variations in nutrient concentrations in Station-2 during the study period.
thumbnail Fig. 11

(A) Control gills-normal structure with well-arranged primary lamella (PL) and secondary lamella (SL). (B) Test gills-degeneration of the primary and secondary lamella (arrow heads), increase in inter lamellar space (IS).
thumbnail Fig. 12

(A) Control heart-normal structure with no histological changes (CM − Cardiac muscle, E − epicardium). (B) Test heart-Fibrillation of cardiac muscle cells and increased intercellular edema (arrows heads).
thumbnail Fig. 13

(A) Normal liver-normal architecture with no histological abnormalities was observed in liver of control fish. Normal hepatocytes can be seen (GV − Glycogen vacuole, H − Hepatocytes, CV − Central vein, PV − Portal vein). (B) Test liver − Complete structural disruption, severe necrosis of hepatocytes (arrow heads) with inflammatory cells were observed.

4 Discussion

Microcystis is a common bloom-forming cyanobacterium that is known to produce toxins. Microcystis cells are generally of 5–7 µm in diameter with different colony morphology (Baker and Fabbro, 2002). Eutrophic conditions with elevated temperature favour the occurrence of Microcystis blooms in aquatic ecosystems (Davis et al., 2009). Various studies regarding diversity and cyanobacterial bloom occurrences has been reported from several countries (Codd et al., 2005), including India (Agrawal et al., 2006). Microcystis aeruginosa blooms reported from south west coast of India (Padmakumar et al., 2008), estuaries (Santhosh Kumar et al., 2010; Prasath et al., 2014) and ponds (Muthukumar et al., 2007) in Tamil Nadu, temple ponds of Varanasi city, Uttar Pradesh (Prakash et al., 2009) are few among them from the Indian waters. However, reports regarding the occurrence of microcystin in India and toxicity studies from South Indian water bodies is particularly scarce (Sangolkar et al., 2006; Prakash et al., 2009). Detailed studies on Microcystis aeruginosa blooms from south India particularly freshwater ponds along Kerala are fewer.

From the analysis, the bloom of freshwater cyanobacteria was observed in two ponds which were dominated by 90–95% Microcystis aeruginosa. Green free-floating scums were present on the surface of the water which was due to the formation of colonies by Microcystis aeruginosa. Microcystis strains that contain gas vesicles can change their cell density and corresponding buoyancy which enables them to form blooms at different depths in the water column (Reynolds, 2006). Like the other buoyant cyanobacteria, Microcystis also prefers calm water columns, in which they will be able to adjust their buoyancy and thus regulate their vertical position (Reynolds and Walsby, 1975; Chorus and Bartram, 1999; Huisman et al., 2004).

The cell densities in both stations were higher prior to monsoon with comparatively high surface water temperature (∼31 °C). The temperature may well influence not just bloom dynamics, but also influence the preferred production of the toxic fraction of any given cyanobacterial population (Davis et al., 2009; Dziallas and Grossart, 2011). Microcystis species is found to predominate during summer season favoured with high surface water temperatures and thereby conducive for bloom formation (Van der Westhuizen and Eloff, 1985; Imai et al., 2009). During peak monsoon season with lower surface water temperature (27 °C) Microcystis cells were observed in fewer cell densities but in healthy cell conditions. Intense summer monsoon had reduced the surface water temperature and the dilution with rainwater might have caused the decline in cell density.

Microcystis showed coexistence of with Cyanobacteria Anabaena sp. at Station 2. A similar coexistence was reported in Finnish freshwater lakes (Ekebom et al., 1992; Sivonen et al., 1989). Coexistence of Microcystis with Anabaena observed in the study during the monsoon period was later dominated by Microcystis. The shift of dominance from Nostoc and Anabaena to Microcystis has been noted in an early Microcystis-dominated summer bloom in Harsha lake (Lu et al., 2019). This shift was explained by the nitrogen fixation process and the subsequent production of nitrogen along with the phosphate scavenging activity that favoured the succession of Microcystis. Chia et al. (2018) investigated the allelopathic interactions between Microcystis and Anabaena sp., based on nutrient levels.

During the bloom of Microcystis ambient water pH was more on an alkaline range (Station 1: 10.2 and Station 2: 8.5). Neutral to alkaline pH conditions were found to be most favourable for the Microcystis growth and also favours their succession over the other phytoplankton (Yang et al., 2018).

Chlorophyll a concentration was at peak with higher cell density in both the stations prior to monsoon and was found to decrease with the decline in cell density. The maximum concentration of chlorophyll a observed at station 1 was 82.08 mg m‑3. Chlorophyll a data showed a positive correlation with the Microcystis cell density at station 1. While at station 2, a noticeable increase in chlorophyll a concentration (267.13 mg m‑3) was observed during monsoon season when the cell density was at moderate range. This might be due to the coexistence of Microcystis with Anabaena which was found during the monsoon period, where both the microalgae might have contributed to the chlorophyll a concentration. Microcystis bloom with chlorophyll a varying between 13.3 and 216 µg L‑1 was reported by Albay et al. (2005). Almanza et al. (2016) have reported chlorophyll a value of 163.3 µg L‑1 from Lo Galindo urban lake during their study. Yuan et al. (2014) in their analysis suggested that total nitrogen and chlorophyll a was found to have the strongest association with microcystin. World Health Organization have proposed related advisory levels for cyanobacteria abundance and chlorophyll a. The chlorophyll a concentrations <10 µg L‑1 have low, values between 10 and 50 µg L‑1 have moderate, values between 50 and 5000 µg L‑1 have high and values >5000 µg L‑1 have a very high risk (Chorus and Batram, 1999).

Dissolved oxygen present in water can depict the water quality during algal blooms. Increase in dissolved oxygen could be due to active photosynthesis and reaeration along with sufficient sunlight. Oxygen depletion is rendered by the decomposition of algae creating an anoxic condition leading to the dysfunctioning of the whole aquatic ecosystem (Huang and Chen, 2013; Garnier et al., 1999a, 1999b). Dissolved oxygen in the present study ranged from 3.41 mg L‑1 to 11.08 mg L‑1. Increased dissolved oxygen was observed at both stations during intense Microcystis bloom owing to the active growth of algal cells which slightly declined subsequently during the post-bloom period as a result of degeneration stage. Lowest values were observed during the month of January 2020 at both stations when the cell density declined. Hence, the result implies that variations in the dissolved oxygen observed during the study were as a result of algal bloom and eutrophication (Huang and Chen, 2013).

Moderate to increased levels of nutrients observed in both the stations could have greatly contributed to the formation of Microcystis bloom throughout the study period. An increased concentration of phosphorous (P) is considered as an important factor responsible for promoting eutrophication and cyanobacterial blooms. High phosphorous concentrations in lakes could lead to high biomasses of phytoplankton community that mainly consists of cyanobacteria. Nitrogen availability could influence the production of microcystin, in Microcystis thereby impacting the bloom toxicity (Davis et al., 2010; Gobler et al., 2016; Chaffin et al., 2018). The effects of phosphorous, nitrogen and ammonia on the growth of Microcystis were previously studied (Kim et al., 2017). Phosphorus can stimulate the growth of Microcystis by supplying nutrient element and has complex interactions with other “environmental factors". They play major roles in the growth of Microcystis (Jin et al., 2005). Silicate concentrations were also found to be higher during post summer monsoon at station2 and monsoon at station1. Higher silicate concentrations have been reported during Microcystis bloom from backwaters of the southeast coast of India (Prasath et al., 2014). Nitrate concentration was high prior to monsoon whereas a peak concentration of phosphate was observed during monsoon season. The ponds were mainly used for domestic use like washing clothes and bathing. Use of soaps and detergents which could likely increase the phosphate content might have favoured the development of Microcystis bloom in these freshwater ecosystems. Fertilizer runoff could elevate the nitrate content in water. Since the water is stagnant and high temperature along with higher nutrient conditions together builds a favourable environment for the proliferation of M. aeruginosa (Dhanya et al., 2012; Somek et al., 2008; Levy, 2017). Even though eutrophication and climate change are the key drivers of algal blooms, their combined influence on microcystin concentration is less investigated. Lürling et al. (2017) hypothesized that warming could promote the cyanobacterial blooms and eutrophication could enhance the biomass and microcystin concentration. This represents the vulnerability of eutrophic waters to future climate changes that might provoke more cyanobacterial nuisance. Increased incidents of eutrophication caused by the use of fertilizers, detergents, due to sewage discharge and other effluents from chemical industries containing nitrate and phosphate have been inducing algal blooms in the aquatic ecosystem.

Reports on the occurrence of toxic M. aeruginosa bloom from Indian waters are less. Since the species is known to produce hepatotoxin called microcystin, it can cause a potential threat to humans and the environment. Microcystis species is of both economic and ecological importance. They produce hepatotoxin that affects the health of humans as well as other livestock's. Besides, they pollute the water bodies making it unsuitable for use.

Bloom associated toxicity studies are of significant scientific value especially for providing an overall understanding of the occurrence of cyanotoxin to enhance risk management and risk assessment strategies (Metcalf and Codd, 2014). During the toxicity study, 100% mortality was observed in the fish exposed to Microcystis bloom within 15 days of exposure. The most affected organ was liver which has been previously reported as the target organ of Microcystin (Hermansky and Stoh's, 1991; Tencalla et al., 1994). Histological changes were also observed in gills and heart. The important histological findings included structural alterations, necrosis and vacuolization. Concomitant histological alterations were reported elsewhere in connection with Microcystis blooms (Atencio et al., 2008; Preeti et al., 2016; Abdel-Latif & Khashba, 2017; Sanad et al., 2015; Ahmed et al., 2017).

M. aeruginosa blooms are well studied and documented in the temperate and subtropical aquatic ecosystems. However such studies particularly toxicity examinations of Microcystis blooms are least attempted from Indian aquatic systems (Sangolkar et al., 2006). Hence the study addresses the occurrence of cyanobacteria Microcystis, their bloom formation and possible toxicological effects from the freshwater lentic ecosystem. Variations in the hydrobiological conditions of the systems during bloom and non-bloom conditions are addressed.

5 Conclusion

M. aeruginosa bloom along two selected freshwater ponds of central Kerala was monitored with the changes in the water quality, bloom characteristics and toxic effects. The species is known to produce potent toxin microcystin that has an adverse effect on various aquatic organisms. Huge scum formation and depletion of dissolved oxygen following the bloom occurs in the study sites. M. aeruginosa was observed in both the study sites throughout the period however they developed to bloom during post-monsoon and pre-monsoon period with decreased cell densities during monsoon. High surface water temperature with stable water column and alkaline water pH was observed to be conducive for M. aeruginosa blooms. Coexistence of M. aeruginosa with Anabaena sp. was observed during the non-bloom conditions. Exposure of the M. aeruginosa bloom to fish (Oreochromis mossambicus) observed high mortality at ∼15 days. Histological examination of the fish revealed that the liver was most effected followed by gills and heart indicating the hepatotoxicity of microcystin. Therefore, regular monitoring of the freshwater ecosystem is necessary to address the occurrence of freshwater toxic algal bloom and their ecological impacts. This can help in the development of eco-friendly control and mitigation techniques.

Variations in physicochemical parameters like temperature, pH and nutrient concentration might be the reason for the emergence of M. aeruginosa bloom. These blooms could affect the water quality as well as a threat to the health of humans, pets and aquatic organisms. Therefore, regular monitoring of the freshwater ecosystem is necessary to preserve and maintain the aquatic systems. Due to the impacts and toxicity of blooms, the development of eco-friendly control and mitigation techniques to reduce the occurrence of blooms is necessary. An awareness regarding the harmful algal blooms and its effect should be created among the people. Further studies should be carried out to determine the extent of toxicity.

References

  • Abdel-Latif HMR, Khashaba AMA. 2017. Subchronic toxicity of Nile tilapia with different exposure routes to Microcystis aeruginosa: histopathology, liver functions, and oxidative stress biomarkers. Veterinary World 10: 955–963. [CrossRef] [PubMed] [Google Scholar]
  • Agrawal MK, Ghosh SK, Bagchi D, Weckesser J, Erhard M, Bagchi SN. 2006. Occurrence of microcystin–containing toxic water blooms in Central India. J Microbiol Biotechnol 16: 212–218. [Google Scholar]
  • Ahmed S, Giese B, Schulz V, Ahmed SMd. 2017. Effects of toxic Microcystis aeruginosa bloom on liver of nile tilapia (Oreochromis niloticus). Bangladesh J Zool 45: 1–10. [CrossRef] [Google Scholar]
  • Albay M, Matthiensen A, Codd GA. 2005. Occurrence of toxic blue-green algae in the Kucukcekmece lagoon (Istanbul, Turkey). Environ Toxicol 20: 277–284. [CrossRef] [PubMed] [Google Scholar]
  • Almanza V, Parra O, Bicudo CD, Baeza C, Beltran J, Figueroa R, Urrutia R. 2016. Occurrence of toxic blooms of Microcystis aeruginosa in a central Chilean (36° Lat. S) urban lake. Rev Chilena Historia Natur 89: 8. [CrossRef] [Google Scholar]
  • Andersen RA. 2005. Algal Culturing Techniques. New York: Elsevier Academic Press, 578 p. [Google Scholar]
  • Atencio L, Moreno I, Prieto AI, Moyano R, Molina AM, Cameán AM. 2008. Acute effects of microcystins MC-LR and MC-RR on acid and alkaline phosphatase activities and pathological changes in intraperitoneally exposed tilapia fish (Oreochromis sp.). Toxicol Pathol 36: 449–458. [CrossRef] [PubMed] [Google Scholar]
  • Baker PD, Fabbro LD. 2002. A guide to the identification of common blue-green algae (Cyanoprokaryotes) in Australian freshwaters, 8–14 p. [Google Scholar]
  • Carmichael WW. 1992. Cyanobacterial secondary metabolites-the Cyanotoxins. J Appl Bacteriol 72: 445–459. [Google Scholar]
  • Chaffin JD, Davis TW, Smith DJ, Baer MM, Dick GJ. 2018. Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production. Harmful Algae 73: 84–97. [Google Scholar]
  • Chen J, Xie P, Li L, Xu J. 2009. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicolog Sci 108: 81–89. [CrossRef] [Google Scholar]
  • Chia MA, Jankowiak JG, Kramer BJ, Goleski JA, Huang IS, Zimba PV, Gobler CJ. 2018. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions. Harmful Algae 74: 67–77. [Google Scholar]
  • Chorus I, Bartram J. 1999. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management, 42–46 p. [Google Scholar]
  • Codd GA, Azevedo SMFO, Bagchi MD, Burch MD, Carmichael WW, Harding WR, Utkilen HC. 2005. CYANONET: a global network for cyanobacterial bloom and toxin risk management: initial situation assessment and recommendations, 21–47 p. [Google Scholar]
  • Davis TW, Berry DL, Boyer GL, Gobler CJ. 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8: 715–725. [Google Scholar]
  • Davis TW, Harke M, Marcoval MA, Goleski JA, Orano-Dawson C, Berry DL, Gobler CJ. 2010. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquatic Microb Ecol 61: 149–162. [CrossRef] [Google Scholar]
  • Desikachary TV. 1959. Cyanophyta, Indian Council of Agricultural Research. New Delhi. 81–99 p. [Google Scholar]
  • Dhanya S, Sebastian S, Joseph A. 2012. A survey of algal blooms in the ponds of Pallippuram, Kerala, India. Int J Environ Sci 3: 1185–1193. [Google Scholar]
  • Dziallas C, Grossart HP. 2011. Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS ONE 6. [Google Scholar]
  • Ekman-Ekebom M, Kauppi M, Sivonen K, Niemi M, Lepistö L. 1992. Toxic cyanobacteria in some Finnish lakes. Environ Toxicol Water Quality 7: 201–213. [CrossRef] [Google Scholar]
  • Garnier J, Leporcq B, Sanchez N, Philippon X. 1999b. Biogeochemical budgets in three large reservoirs of the seine basin (Marne, Seine and Aube reservoirs). Biogeochemistry 47: 119–146. [Google Scholar]
  • Garnier J, Billen G, Palfner L. 1999a. Understanding the oxygen budget of the Mosel drainage network with the concept of heterotrophic/autotrophic sequences: the River Strahler approach. Hydrobiologia 410: 151–166. [Google Scholar]
  • Gobler CJ, Burkholder JM, Davis TW, Harke MJ, Johengen T, Stow CA, Van de Waal DB. 2016. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54: 87–97. [Google Scholar]
  • Grasshoff K. 1983. Determination of nitrate. In: Grasshoff K, Ehrhardt M, Kremling K (Eds.). Methods of Seawater Analysis. Weinheim: Verlag Chemie, p. 143. [Google Scholar]
  • Hermansky SJ, Stohs SJ. 1991. Effect of microcystin-LR (MCLR) on hepatic microsomal membrane fluidity. Res Commun Chem Pathol Pharmacol 72: 213–222. [PubMed] [Google Scholar]
  • Huang Y, Chen M. 2013. Variation of dissolved oxygen in the experiments of occurrence & disappearance for Microcystis bloom. Proc Environ Sci 18: 559–566. [CrossRef] [Google Scholar]
  • Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JM, Sommeijer B. 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960–2970. [Google Scholar]
  • Imai H, Chang KH, Nakano SI. 2009. Growth responses of harmful algal species Microcystis (Cyanophyceae) under various environmental conditions. Interdisciplinary Stud Environ Chem 269–275. [Google Scholar]
  • Jin XC, Chu ZS, Yi WL, Hu XZ. 2005. Influence of phosphorus on Microcystis growth and the changes of other environmental factors. J Environ Sci 17: 937–941. [Google Scholar]
  • Kim H, Jo BY, Kim BY. 2017. Effect of different concentrations and ratios of ammonium, nitrate, and phosphate on growth of the blue-green algae (cyanobacterium) Microcystis aeruginosa isolated from the Nakdong River, Korea. Algae 32: 275–284. [CrossRef] [Google Scholar]
  • Knoll LB, Hagenbuch EJ, Stevens MH, Vanni MJ, Renwick WH, Denlinger JC, Hale RS, González MJ. 2015. Predicting eutrophication status in reservoirs at large spatial scales using landscape and morphometric variables. Inland Waters 5: 203–214. [Google Scholar]
  • Levy S. 2017. Microcystis rising: why phosphorus reduction isn't enough to stop cyanoHABs. Environ Health Perspect 125: A34–A39. [PubMed] [Google Scholar]
  • Litchman E, de Tezanos Pinto P, Klausmeier CA, Thomas MK, Yoshiyama K, 2010. Linking traits to species diversity and community structure in phytoplankton. In Fifty years after the “Homage to Santa Rosalia”: Old and new paradigms on biodiversity in aquatic ecosystems, 15–28. [CrossRef] [Google Scholar]
  • Livingstone DM. 2003. Impact of secular climate change on the thermal structure of a large temperate central European lake. Climatic Change 57: 205–225. [Google Scholar]
  • Lu J, Zhu B, Struewing I, Xu N, Duan S. 2019. Nitrogen–phosphorus-associated metabolic activities during the development of a cyanobacterial bloom revealed by metatranscriptomics. Sci Rep 9: 1–11. [CrossRef] [Google Scholar]
  • Lürling M, Oosterhout FV, Faassen E. 2017. Eutrophication and warming boost cyanobacterial biomass and Microcystins. Toxins 9: 64. [Google Scholar]
  • Metcalf JS, Codd GA. 2014. A review of current knowledge, cyanobacterial toxins (Cyanotoxins) in water. Found Water Res 47. [Google Scholar]
  • Miller MA, Kudela RM, Mekebri A, Crane D, Oates SC, Tinker MT, Staedler M, Miller WA, Choutka ST, Dominik C, Hardin D, Langlois G, Murray M, Ward K, Jessup DA. 2010. Evidence for a novel marine harmful algal bloom: cyanotoxin (Microcystin) transfer from land to sea otters. PLoS ONE 5: e12576. [CrossRef] [PubMed] [Google Scholar]
  • Muthukumar C, Muralitharan G, Vijayakumar R, Panneerselvam A, Thajuddin N, 2007. Cyanobacterial biodiversity from different freshwater ponds of Thanjavur, Tamilnadu (India), 17–25 p. [Google Scholar]
  • O'Neil JM, Davis TW, Burford MA, Gobler CJ. 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334. [Google Scholar]
  • Padmakumar KB, Sanilkumar MG, Saramma AV, Sajeevan VN, Menon NR. 2008. Microcystis aeruginosa bloom on Southwest coast of India. Harmful Algae News 37: 11–12. [Google Scholar]
  • Paerl HW, Huisman J. 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1: 27–37. [CrossRef] [PubMed] [Google Scholar]
  • Parsons TR, Maita Y, Lalli CM. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Oxford: Pergamon Press, 173 p. [Google Scholar]
  • Prakash S, Lawton LA, Edwards C. 2009. Stability of toxigenic Microcystis blooms. Harmful Algae 8: 377–384. [Google Scholar]
  • Prasath B, Nandakumar R, Jayalakshmi T, Santhanam P. 2014. First report on the intense cyanobacteria Microcystis aeruginosa Kützing, 1846 bloom at Muttukkadu Backwater, Southeast coast of India. Indian J Geo-Mar Sci 43: 258–262. [Google Scholar]
  • Preeti T, Hariharan G, Rajarajeswari GR. 2016. Histopathological and biochemical effects of cyanobacterial cells containing microcystin-LR on Tilapia fish. Water Environ J 30: 135–142. [Google Scholar]
  • Reynolds CS. 2006. Ecology of phytoplankton. Cambridge University Press, 145–236 p. [CrossRef] [Google Scholar]
  • Reynolds CS, Walsby AE. 1975. Water-blooms. Biol Rev Cambr Philos Soc 50: 437–481. [CrossRef] [Google Scholar]
  • Rosen BH, St. Amand A. 2015. Field and laboratory guide to freshwater cyanobacteria harmful algal blooms for Native American and Alaska Native Communities: U.S. Geological Survey Open-File Report 2015–1164, 26–28 p. [Google Scholar]
  • Sanad SM, Al-Gamaal MA, Hemmaid DK. 2015. Histopathological changes in the liver of the Nile fish Oreochromis niloticus fed on the blue-green algae Microcystis aeruginosa under laboratory conditions. In International Conference on Biological, Civil and Environmental Engineering (BCEE-2015), Bali (Indonesia). [Google Scholar]
  • Sangolkar LN, Maske SS, Chakrabarti T. 2006. Methods for determining Microcystins (peptide hepatotoxins) and microcystins producing cyanobacteria. Water Res 40: 3485. [CrossRef] [PubMed] [Google Scholar]
  • Santhosh Kumar C, Ashok Prabu V, Sampathkumar P, Anantharaman P. 2010. Occurrence of algal bloom Microcystis aeruginosa in the Vellar estuary, South-East coast of India. Int J Curr Res 5: 52–55. [Google Scholar]
  • Shestakov SV, Karbysheva EA. 2017. The origin and evolution of cyanobacteria. Biol Bull Rev 7: 259. [CrossRef] [Google Scholar]
  • Sivonen K, Himberg K, Luukkainen R, Niemelä SI, Poon GK, Codd GA. 1989. Preliminary characterization of neurotoxic cyanobacteria blooms and strains from Finland. Toxic Assess 4: 339–352. [CrossRef] [Google Scholar]
  • Somek H, Ustaoğl MR, Yağci M. 2008. A case report: algal bloom of Microcystis aeruginosa in a drinking-water body, Eğirdir Lake, Turkey. Turk J Fish Aquat Sci 8: 177–179. [Google Scholar]
  • Tanabe Y, Hodoki Y, Sano T, Tada K, Watanabe MM. 2018. Adaptation of the freshwater bloom-forming cyanobacterium Microcystis aeruginosa to brackish water is driven by recent horizontal transfer of sucrose genes. Front Microbiol https://doi.org/10.3389/fmicb.2018.01150. [Google Scholar]
  • Tencalla FG, Dietrich DR, Schlatter C. 1994. Toxicity of Microcystis aeruginosa peptide toxin to yearling rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 30: 215–224. [Google Scholar]
  • Van der Westhuizen AJ, Eloff JN. 1985. Effect of temperature and light on the toxicity and growth of the blue-green algae Microcystis aeruginosa (UV-006). Planta 163: 55–59. [CrossRef] [PubMed] [Google Scholar]
  • Whitton BA. 1992. Diversity, ecology, and taxonomy of the cyanobacteria. In: Mann NH, Carr NG (eds) Photosynthetic Prokaryotes. Biotechnology Handbooks 6, 1–51. [Google Scholar]
  • Winkler LW. 1888. Die Bestimmung des im Wassergelosten Sauerstoffes. Chem Ber 21: 2843–2855. [Google Scholar]
  • Yang J, Tang H, Zhang X, Zhu X, Huang Y, Yang Z. 2018. High temperature and pH favor Microcystis aeruginosa to outcompete Scenedesmus obliquus . Environ Sci Pollut Res 25: 4794–4802. [CrossRef] [Google Scholar]
  • Yu T, Xie P, Dai M, Liang G. 2009. Determinations of MC-LR and [Dha (7)] MC-LR concentrations and physicochemical properties by liquid chromatography-tandem mass spectrometry. Bull Environ Contamin Toxicol 83: 757–760. [CrossRef] [Google Scholar]
  • Yuan LL, Pollard AI, Pather S, Oliver JL, D'Anglada L. 2014. Managing microcystin: identifying national-scale thresholds for total nitrogen and chlorophylla. Freshw Biol 59: 1970–1981. [Google Scholar]

Cite this article as: Mohan R, Sathish T, Padmakumar KB. 2020. Occurrence of potentially toxic cyanobacteria Microcystis aeruginosa in aquatic ecosystems of central Kerala (south India). Ann. Limnol. - Int. J. Lim. 56: 18

All Figures

thumbnail Fig. 1

Study area. Red star represents the location in Kochi (Kerala) from where M. aeruginosa bloom was recorded.
In the text
thumbnail Fig. 2

M. aeruginosa bloom with green scum floating in the surface. (A) Station-1 (B) Station-2.
In the text
thumbnail Fig. 3

Microphotographs (LM) of Microcystis aeruginosa cells from bloom samples.
In the text
thumbnail Fig. 4

SEM images of (A) M. aeruginosa colony (B) M. aeruginosa single.
In the text
thumbnail Fig. 5

Variations in temperature, pH and dissolved oxygen in Station-1 during the study period.
In the text
thumbnail Fig. 6

Variations in temperature, pH and dissolved oxygen in Station-2 during the study period.
In the text
thumbnail Fig. 7

Variations in M. aeruginosa cell density (×105 Cells L−1) and chlorophyll a in station-1 during the study period.
In the text
thumbnail Fig. 8

Variations in M. aeruginosa cell density (×105 Cells L−1) and chlorophyll a in station-2 during the study period.
In the text
thumbnail Fig. 9

Variations in nutrient concentrations in Station-1 during the study period.
In the text
thumbnail Fig. 10

Variations in nutrient concentrations in Station-2 during the study period.
In the text
thumbnail Fig. 11

(A) Control gills-normal structure with well-arranged primary lamella (PL) and secondary lamella (SL). (B) Test gills-degeneration of the primary and secondary lamella (arrow heads), increase in inter lamellar space (IS).
In the text
thumbnail Fig. 12

(A) Control heart-normal structure with no histological changes (CM − Cardiac muscle, E − epicardium). (B) Test heart-Fibrillation of cardiac muscle cells and increased intercellular edema (arrows heads).
In the text
thumbnail Fig. 13

(A) Normal liver-normal architecture with no histological abnormalities was observed in liver of control fish. Normal hepatocytes can be seen (GV − Glycogen vacuole, H − Hepatocytes, CV − Central vein, PV − Portal vein). (B) Test liver − Complete structural disruption, severe necrosis of hepatocytes (arrow heads) with inflammatory cells were observed.
In the text

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