JES-00691; No of Pages 9

J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX

Available online at www.sciencedirect.com

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1 Spatial and temporal distribution of cyanobacteria in

2 Batticaloa Lagoon

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Jalaldeen Mohamed Harris1,⁎, Periyathamby Vinobaba1 ,

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4 Ranil Kavindra Asela Kularatne2,3 , Ellawala Kankanamge Champika4

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5 1. Department of Zoology, Eastern University, Vantharumoolai, Chenkaladi, Sri Lanka. E-mail: harriseusl@gmail.com
6 2. MAS Capital (Private) Limited, 10th Floor, Aitken Spence Tower II, 315, Vauxhall Street, Colombo 2, Sri Lanka

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7 3. MAS Active Trading (Pvt) Limited, No. 231, D.M. Colombage Mawatha, Nawala, Sri Lanka
8 4. Department of Civil and Environmental Engineering, Faculty of Engineering, University of Ruhuna, Hapugala, Galle, Sri Lanka
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11 AR TIC LE I NFO ABSTR ACT

13 Article history:
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The necessity to understand the relationship between cyanobacterial species abundance 18
14 Received 11 August 2015 and water quality variations in coastal lagoons is crucial to develop strategies to prevent 19
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15 Revised 23 December 2015 further cyanobacterial proliferation. This paper evaluates the relationship between water 20
16 Accepted 4 January 2016 quality variations on the distribution of cyanobacteria during a 12-month period in 21
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17 Available online xxxx Batticaloa Lagoon (Sri Lanka) using Redundancy analysis and Pearson correlations. Drastic 22
variations in pH, temperature, salinity, dissolved oxygen (DO) and total phosphorus (TP) 23
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31 Keywords: levels were reported, but not turbidity and NO−3. This brackish waterbody is hypereutrophic 24
32 Batticaloa Lagoon (TP levels > 0.1 mg/L). The cyanobacterial community contained 13 genera and 22 species. 25
33 NO−3, TP and turbidity levels positively influenced cyanobacterial abundance during all 26
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Cyanobacteria
34 Nitrates (NO−3) seasons indicating that nutrient (largely phosphorus) and sediment entry control is highly 27
35 Turbidity 28
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crucial along with periodic monitoring of cyanobacterial growth.

36 Total phosphorous (TP) © 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. 29
37 Water quality Published by Elsevier B.V. 30
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38
41
40
39
42
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44
43 Introduction dumping of Municipal Solid Waste (MSW) by the local 56
community and some local government authorities (e.g., 57
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45 Batticaloa Lagoon (located between 7°58′N and 81°29′E to Kattankudy Urban Council), disposal of untreated sewage, 58
46 7°20′N and 81°52′E) is the third largest brackish water body rice mill effluents, shrimp farm effluents and slaughter- 59
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47 in Sri Lanka with more than 90% of the area located in the houses effluents (e.g., in Urani area) tends to pollute the 60
48 Batticaloa District in the Eastern Province. The lagoon sup- lagoon (Kularatne, 2014). Significant Pb contamination has 61
49 ports diverse ecosystems including marine habitats such as been already reported by Kularatne (2014). Also occurrence of 62
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50 mangroves. However, due to poorly planned infrastructure cyanobacteria (blue-green algae) (e.g., Microcystis aeruginosa, 63
51 development, aquaculture ponds and government security Oscillatoria sp., Lyngbya sp., Cylindrospermopsis sp., Nostoc sp. 64
52 clearances the original mangrove cover of 1490 ha has been and Anabaena sp., etc.) has been reported by Harris and 65
53 reduced to 321 ha at present during a 20 year period (IUCN Vinobaba (2012a) indicating that there is some nutrient 66
54 Sri Lanka and the Central Environmental Authority, 2006; enrichment and further lagoon pollution is expected due 67
55 NECCDEP, 2010; Kularatne, 2014). Moreover, indiscriminate to considerable anticipated unplanned developments in the 68

⁎ Corresponding author.

http://dx.doi.org/10.1016/j.jes.2016.01.020
1001-0742/© 2016 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 2 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

69 Batticaloa area since the cessation of the ethnic conflict in 93703 C turbidity meter for turbidity) as per standard methods 124
70 May, 2009 (Kularatne, 2014). (APHA, AWWA and WEF, 2005). 125
71 Cyanobacteria secrete various cyanotoxins that are harmful Water samples were kept in a cool, dark environment and 126
72 to the biota. For example, M. aeruginosa, Oscillatoria sp., Nostoc sp. carried to the laboratory for analysis of nutrients. Prior to 127
73 and Anabaena sp. secrete microcystins (which are cyclic peptide nutrient analysis, water samples were filtered through GF/C 128
74 hepatotoxins) that could cause death in mammals in acute filter papers to remove any green color interference of algae. 129
75 doses by hypovolaemic shock (Codd et al., 1999; Falconer, 1999; Nitrates (NO−3) and phosphates as total phosphorous (TP) were 130
76 Sathishkumar et al., 2010; Metcalf and Codd, 2012). Anabaena measured within 48 hr using the Molybdate Blue method and 131
77 sp. as well as Lyngbya sp. and Cylindrospermopsis sp. secretes UV screening method, respectively (APHA, AWWA and WEF, 132
78 saxitoxins which are a group of about 30 neurotoxic carbamate 2005). Separate water samples were collected for dissolved 133
79 alkaloids (Falconer, 1999; Metcalf and Codd, 2012). More- oxygen (DO) analysis within 48 h using modified Winkler's 134
80 over, odor attributed to the secretion of metabolites (example, Method (APHA, AWWA and WEF, 2005). 135

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81 2-methyl isoborneol and geosmin/trans-1,10-dimethyl-trans-9
82 decalol) is esthetically unpleasing since tourism is an im- 1.3. Collection of cyanobacterial samples, identification and 136

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83 portant commercial activity in the Batticaloa Lagoon. Also some enumeration 137
84 species secrete skin irritants such as the phenolic bislactones

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85 aplysiatoxins (e.g., Oscillatoria sp. and Lyngbya sp.) and indole Cyanobacterial samples were also taken at each sampling 138
86 alkaloid lyngbyatoxins-A, -B and -C (e.g., Lyngbya sp.) (Falconer, point (5 samples per location) using a plankton net 139
87 1999; Metcalf and Codd, 2012) which could be a concern to (Hydro-bios, Germany) with the end of the net having a 140

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88 bathers in the lagoon. collecting bottle with a capacity of 250 mL. Cyanobacterial 141
89 There is a need to analyze cyanobacterial species and samples were collected slowly by horizontal hauling without 142

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90 abundance variability in relation to water quality variations causing disturbances to the cyanobacteria (at a distance of 143
91 so that this information can be used to develop strategies to 10 m from the sampling vessel). The samples were immedi- 144
92 prevent further cyanobacterial growth. Redundancy analysis ately preserved using Lugol's solution (ratio is 1 mL of Lugol's
D 145
93 (RDA), a constrained linear ordination method has been used solution to 100 mL of water sample) in order to settle the 146
94 to evaluate the effects of environmental variables on fresh- cyanobacteria and to get a clear view. The samples were then 147
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95 water cyanobacterial communities (Tian et al., 2012; Lu et al., reduced to 10 mL by decanting the supernatant aliquot and 148
96 2013). In this study, we use RDA to evaluate the impact of centrifuged (Bench model D2230, Brand — Gallenkamp, UK) 149
97 150
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seasonal variations of selected water quality parameters on for 20 min at 4000 r/min. One drop of concentrated sample
98 the distribution of cyanobacteria in Batticaloa Lagoon. was investigated under a trinocular bright field research 151
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microscope (Labomed LX400, USA). Identification was done 152

using standard keys (Prescott, 1970; Lee, 2008; Bellinger and 153
100
99 1. Materials and methods Sigee, 2010) at 400 × magnification to lowest taxonomic level. 154
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The quantity of cyanobacteria was determined using 1 mL 155

101 1.1. Study area of sedimented sample through a Sedgewick-Rafter counting 156
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chamber (Pyser-SGI S50, UK) comprising a plastic cover glass 157

102 The 16 sampling points were previously defined based on the (Pyser-SGI S51, UK) and then the number of individual species 158
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103 different biotypes in the lagoon (Fig. 1) and characteristics was counted as described in other reports (Littleford et al., 159
104 such as bottom substrate, surface, topography, depth, salinity 1940; Gilbert, 1942; Serfling, 1949). 160
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105 and human impact level. The precise location of each station The above processes were repeated 5 times and the mean 161
106 was determined using a portable GPS meter (Garmin, USA) was used to determine the sample abundance. 162
107 (Table 1).
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1.4. Statistical analysis 163

108 1.2. Sampling and water quality analysis
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One-way ANOVA (unstacked) in Minitab Version 14 was used 164

109 Water sampling was carried out during the period of March 2012 to evaluate any significant differences between the different 165
110 166
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to February 2013 (i.e., twice a month) between 9 am and 11 am seasons with reference to the mean levels of the different
111 covering the different seasons. Period of November–February is parameters analyzed. 167
112 the heaviest north-east monsoonal rainy period with intermit- All multivariate and ordination analyses were performed 168
113 tent or few showers occurring in the first inter-monsoonal using CANOCO version 4.5. Firstly, detrended correspondence 169
114 period (March–April) and second inter-monsoonal period analysis (DCA) was carried out and the first gradient length 170
115 (September–October). South-west monsoonal period (May– was used to select the appropriate model (ordination proce- 171
116 August) is the driest period in Batticaloa. dure) for the constrained ordinations. Redundancy analysis 172
117 Samples were collected in triplicate by dipping well labeled (RDA) was chosen as an appropriate tool for the analysis 173
118 sterilized plastic containers of 1000 mL to about 50 cm below because the length of the ordination axes in DCA was less 174
119 the surface film. pH, surface temperature, salinity and tur- than 3 (Lepš and Šmilauer, 2003). The effects of environmental 175
120 bidity were analyzed in-situ using calibrated instruments variables (i.e., pH, temperature, salinity, turbidity, DO, NO−3 and 176
121 (Hanna, Romania portable HI 98128 water proof pH meter for TP) on cyanobacteria were analyzed and the environmental 177
122 pH and temperature, Portable ATAGO, Japan, S/MillE Hand variables were taken up as the explanatory variables. All of 178
123 Refractometer for salinity and Hanna, Romania portable HI these environmental variables were log (X + 1) transformed 179

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 3

Batticaloa Lagoon

Sri Lanka

Batticaloa District

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Fig. 1 – Map of the study area showing the sampling locations. Locations 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15 and 16
denotes Palameenmadu, Kallady, Kottamunai, Eravur, Sathurukkondan, Thiruperumthurai, Urani, Valayaravu, Vavunativu,
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Kattankudy, Kaluthawalai, Chettipalayam, Kallaru, Kallaru stream, Pattiruppu and Kokkaticholai, respectively.
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180 before analysis (Tian et al., 2012; Lu et al., 2013). Co-variable, Pearson correlation analysis between cyanobacteria abun- 195
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181 monsoon period was an ordinal variable introduced as dance and environmental factors was carried out. Levels 196
182 the north-east monsoonal period = 1, 1st inter-monsoonal of significance used were 5% (significant) and 1% (highly 197
183 period = 2, south-west monsoonal period = 3 and 2nd inter- significant). Statistical analysis was carried out using the SPSS 198
184 monsoonal period = 4 in the model. Monsoonal periods were 16.0 statistical package. 199
185 assigned the number in the order of the monsoon periods
186 occurring during the year. Twenty two cyanobacterial species
187 were encountered in the lagoon. All species were incorporated 2. Results and discussion 201
200
188 into RDA. RDA was carried out on the data for all periods
189 encountered during the study period. The results of RDA 2.1. Water quality of the study area 202
190 were visualized in the form of ordination diagrams in the Fig. 2 shows the temporal variations of the selected water 203
191 Canodraw for Windows program. Species scores are repre- quality parameters in Batticaloa Lagoon. Spatial variations of 204
192 sented as light colored arrows. Environmental variables are the selected water quality parameters are shown in Table S1. 205
193 represented by dark bold arrows, pointing in the direction of Mean pH and temperature values reported in this study are 206
194 maximal variation. in agreement with previous studies (GreenTec Consultants, 207

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 4 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

t1:1 Table 1 – Brief description of the study area with the GPS coordinates.
t1:3
t1:2
t1:4 Location GPS Remarks
Coordinates

t1:5 1 Palameenmadu 7°45′29.58N81°41′ Located close to the bar mouth and opens to the Indian Ocean when breached during rainy periods.
14.39″E Characterized by a muddy substrate.
t1:6 2 Kallady 7°43′23.42″N Fairly high saline water with suitable spawning ground for Sea bass.
81°42′29.93″E
t1:7 3 Kottamunai 7°42′58.15″N Freshwater area that is highly organically enriched. Substratum profile is characterized by fine muddy
t1:8 81°41′48.64″E silt with abundance of aquatic vegetation. Located near a sewage outfall.
t1:9 4 Eravur 7°45′14.81″N Located near a sewage outfall. Highest levels of industrial pollution are likely.
81°35′51.45″E
t1:10 5 Sathurukkondan 7°44′31.96″N Pristine mangrove areas that have been recommended to be declared as a sanctuary as these marshy
81°38′50.23″E lands provides habitats for several species of birds including migrant waders and rare species such as

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Q1 Lesser Adjutant Stork Leptoptilus javanicus and Spot Billed Pelican Pelecanus philippensis (NECCDEP, 2009).
t1:11 6 Thiruperumthurai 7°43′12.39″N Located near a shrimp farming site on the northern sector with sandy substrate.

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81°42′16.24″E
t1:12 7 Urani 7°43′07.22″N Highest levels of industrial pollution are likely. Contaminated with shrimp farm effluents and
81°41′20.27″E slaughterhouses effluents.

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t1:13 8 Valayaravu 7°42′48.07″N Highest levels of industrial pollution are likely. Freshwater area that is highly organically enriched.
81°39′24.88″E Substratum profile is characterized by fine muddy silt with abundance of aquatic vegetation.

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t1:14 9 Vavunativu 7°41′45.15″N Muddy bottom with aquatic moss.
81°39′36.73″E
t1:15 10 Kattankudy 7°39′38.64″N Sandy bottom near to sewage disposal.

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81°43′59.98″E
t1:16 11 Kaluthawalai 7°32′39.57″N Subjected to fertilizer and pesticide runoff from nearby crop lands.
81°46′29.62″E
t1:17 12 Chettipalayam 7°43′07.22″N Located near a sewage outfall.
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81°41′20.27″E
t1:18 13 Kallaru 7°29′47.36″N Located close to the bar mouth and opens to the Indian Ocean when breached during rainy periods.
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81°48′27.36″E Characterized by a muddy substrate.
t1:19 14 Kallaru stream 7°28′19.08″N Located near a sewage outfall.
81°47′30.81″E
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t1:20 15 Pattiruppu 7°30′32.08″N Completely fresh water area and highly turbid with the abundance of Eichhornia crassipes (water hyacinth).
81°46′15.29″E
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t1:21 16 Kokkaticholai 7°38′01.17″N Subjected to agricultural runoff with muddy bottom.

81°43′59.98″E
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208 2009; Harris and Vinobaba, 2012b; Kularatne, 2014). pH was (IUCN Sri Lanka and the Central Environmental Authority, 234
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209 within the range of 6.0–8.5 to support estuarine and marine 2006). 235
210 ecosystems (Svobodova et al., 1993; Harris and Vinobaba, In contrast to previous reports (JUGAS Ltd., 2010), statisti- 236
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211 2012a, 2012b). However, significant pH and temperature vari- cally there was no significant variation in the turbidity levels 237
212 ations (p < 0.005) were evident between the different seasons considering the different seasons (p > 0.005). Currently, in the 238
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213 with the lowest temperature and pH conditions reported Sri Lankan legislation, there is no ambient standard enacted 239
214 during the heavy rainy periods of the north-east monsoon or proposed for turbidity levels in inland waters and coastal 240
215 due to dilution effects (Harris and Vinobaba, 2012a; Jalal et al., waters. 241
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216 2012). The present study revealed that the mean NO−3 levels were 242
217 Mean salinity levels showed a significant seasonal varia- less than 5 mg/L which is the threshold limit for aquatic life 243
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218 tion (p < 0.005) with the lowest salinity scenarios reported (GreenTec Consultants, 2009) and there was no significant 244
219 during the north-east monsoonal period due to considerable seasonal variation (p > 0.005). In contrast, mean TP levels 245
220 246
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dilution of the lagoonal waters by heavy surface and sub-
221 surface runoff from the mainland (Coelho et al., 2007; Harris
222 and Vinobaba, 2012b; Uzukwu et al., 2013; O'Neill et al., 2015).
223 Highest salinity was evident at location 1 (Palameenmadu;
224 northern bar mouth which is frequently breached by the
225 fishermen to gain access to the Indian Ocean) and the lowest
226 salinity levels were recorded at locations 11, 12 and 15. The
227 entire lagoon including the southernmost sections could
228 be described as a brackish water body (as salinity is between
229 0.5 g/L and 30 g/L), though recent studies revealed that the
230 northern basin becomes more saline with salinity levels
231 exceeding 30 g/L during the driest spells (JUGAS Ltd., 2010;
232 Kularatne, 2014) while other reports showed that the south-
233 ernmost section is relatively fresh due to freshwater inflows
showed a significant seasonal variation (p < 0.005) with most
of the locations (i.e., locations 1, 2, 4, 5, 6, 9, 10, 12, 15 and 16) 247
showing elevated levels during the second inter-monsoonal 248
season and then during the north-east monsoonal period. 249
This is possibly due to runoff entry from agricultural lands, 250
urban areas and shrimp farms, etc. TP levels were in excess of 251
0.010 mg/L to favor the growth of cyanobacteria and the fact 252
that the TP levels have well exceeded 0.1 mg/L, indicates that 253
Batticaloa Lagoon is hypereutrophic (OECD, 1982; Masters, 254
2000; Weiner and Matthews, 2012; Mallick, 2014). 255
All the locations reported DO values higher than 4.5 mg/L, 256
which is sufficient for the survival of fish and other lagoonal 257
biota (GreenTec Consultants, 2009). Almost all the locations 258
reported the lowest DO levels during the north-east monsoonal 259

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 5

34.0 8.60 35.00 18.00

33.0 a 8.40
8.20
30.00
25.00
b 16.00
14.00

Turbidity (NTU)
32.0 8.00
Temperature (°C)

20.00 12.00

Salinity (g/L)
31.0 7.80
15.00 10.00

pH
7.60
30.0 10.00 8.00
7.40
5.00 6.00
29.0 7.20
0.00 4.00
7.00
28.0 -5.00 2.00
Temperature pH 6.80 Turbidity Salinity
27.0 6.60 -10.00 0.00

4.00 0.80 10.00

3.50 c 0.70 9.00

8.00
d
3.00 0.60
7.00
Nitrate (mg/L)

2.50 0.50

TP (mg/L)
6.00

DO (mg/L)
2.00 0.40 5.00

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1.50 0.30 4.00
3.00
1.00 0.20
2.00

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0.50 0.10
Nitrate TP 1.00 DO
0.00 0.00 0.00

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Fig. 2 – Temporal variation of (a) temperature and pH, (b) turbidity and salinity, (c) Nitrate and TP and (d) DO in Batticaloa Lagoon

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during the study period (March 2012 to February 2013). Each data point represents the mean value of 16 sampling locations. TP:
total phosphorus; DO: dissolved oxygen.

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260 period (p < 0.005), possibly due to the low photosynthetic filamentous genera Cylindrospermopsis and Oscillatoria. Among
D 269
261 activities of the cyanobacteria during the cloudy rainy periods these cyanobacteria genera, M. aeruginosa, Spirulina major, 270
262 (Uzukwu et al., 2013). Anabaena oscillarioides, Cylindrospermopsis sp., Lyngbya sp. and 271
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Oscillatoria sancta lacked seasonality in all seasons and were 272
263 2.2. Cyanobacterial species composition the main representatives of the cyanobacterial community. 273
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Throughout the study period, A. oscillarioides seemed to be more 274

264 A total of 60 species of phytoplankton were reported (data not dominant (17.1%), followed by O. sancta (13%), M. aeruginosa 275
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265 shown) out of which there were 22 species of cyanobacteria (11%) and then S. major (10.2%). Chroococcales peak density 276
266 from 5 different orders (Table 2). The most abundant was observed during the north-east monsoon period while 277
267 cyanobacteria in this lagoon were bloom or colony-forming Glaucocystales and Nostocales during the first inter-monsoon. 278
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268 genera (Microcystis and Anabaena) as well as the solitary Oscillatoriales and Synechococcales were predominant during 279
the south-west monsoonal period. M. aeruginosa and Anabaena 280
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sp. are bloom-forming species (Tian et al., 2012; Lu et al., 281

2013) and both these species along with Oscillatoria sp. secrete 282
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t2:1 Table 2 – List of cyanobacterial species recorded from the microcystins (Rapala et al., 1997; Codd et al., 1999; Falconer, 283
t2:2 Batticaloa Lagoon. 1999; Sathishkumar et al., 2010; Metcalf and Codd, 2012). 284
t2:3
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t2:4 Order Genera Species Anabaena sp. also secretes saxitoxins and Oscillatoria sp. produce 285
phenolic bislactones aplysiatoxins (Falconer, 1999; Metcalf 286
t2:5 Chroococcales Aphanothece Aphanothece sp.
t2:6 and Codd, 2012). Studies conducted by Lu et al. (2013) for 287
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Chroococcus Chroococcus sp.

t2:7 Microcystis Microcystis aeruginosa freshwater lakes have revealed that Anabaena sp., Oscillatoria 288
t2:8 Microcystis sp2. sp. and Cylindrospermopsis sp. have the ability to fix atmospheric 289
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t2:9 Spirulina Spirulina major N2. 290

t2:10 Spirulina princeps
t2:11 Spirulina subsalsa
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2.3. Variations in abundance and species composition 291

t2:12 Glaucocystales Glaucocystis Glaucocystis sp.
t2:13 Nostocales Anabaena Anabaena oscillarioides
t2:14 Anabaena sp2. Fig. 3 shows the spatial variation and the temporal varia- 292
t2:15 Anabaenopsis Anabaenopsis arnoldii tion of cyanobacterial composition in Batticaloa Lagoon, 293
t2:16 Anabaenopsis sp1. respectively. 294
t2:17 Anabaenopsis sp2. Cyanobacterial abundance in Batticaloa Lagoon exhibited 295
t2:18 Cylindrospermopsis Cylindrospermopsis sp. distinct spatial distribution. Highest abundance was recorded 296
t2:19 Nostoc Nostoc sp.
during the 1st inter-monsoonal period (March to April) and 297
t2:20 Oscillatoriales Arthrospira Arthrospira maxima
low values during the 2nd inter-monsoon period (September 298
t2:21 Arthrospira sp2.
t2:22 Lyngbya Lyngbya sp. to October). The maximum individual cyanobacteria cell was 299
t2:23 Oscillatoria Oscillatoria sancta observed in the month of April 2013 (7.86 × 106 cells/L), the 300
t2:24 Oscillatoria sp2. lowest density occurred in September 2013 (3.29 × 106 cells/L). 301
t2:25 Synechococcales Merismopedia Merismopedia glauca Spatial variation of cyanobacterial composition showed het- 302
t2:26 Merismopedia sp2.
erogeneity among the sampling sites. During the study period 303

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 6 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

Chroococcales Glaucocystales Nostocales

a Oscillatoriales Synechococcales b

Abundance of cyanobacteria (×106 cells/L)

100% 160 1
90% 2
140 3
80% 4
Relative abundance

120 5
70% 6
60% 100 7
8
50% 80 9
10
40% 60 11
30% 12
40 13
20% 14
20 15
10% 16

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0 0 Average
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 SW NE IM1 IM2
Sampling location Monsoon period

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Fig. 3 – Spatial (a) and temporal (b) variation of cyanobacterial composition in Batticaloa Lagoon. SW, NE, IM1 and IM2 denote

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south-west monsoon, north-east monsoon, 1st inter-monsoon and 2nd inter-monsoon, respectively.

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304 only location 11 had all five orders while sites 9 and 13 were 2.4. Impact of water quality variations on cyanobacterial 316
305 solely represented by O. sancta. species and their abundance 317
306 Peak numerical abundance of M. aeruginosa population
307 reached during the north-east monsoonal period with a cell
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Fig. 4 shows the first two axes of RDA for the selected water 318
308 density of 1.07 × 106 cells/L. However, this organism again quality parameters associated with the cyanobacteria varia- 319
309 became prevalent during late March in the first inter-monsoon tion in all periods investigated and during the different 320
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310 period. During mid-April conditions became optimal for the seasons. Table 3 shows the summary of RDA between the 321
311 growth of the Microcystis and a very rapid development towards selected water quality parameters and cyanobacterial abun- 322
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312 the latter part of the month. Cylindrospermopsis sp. reached dance in Batticaloa Lagoon. 323
313 maximum in April (first inter-monsoon) with a density of When all periods in the year are analyzed, the eigen values 324
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314 0.52 × 106 cells/L while during the other seasons abundance (λ) for RDA axis 1 (λ: 0.212) and RDA axis 2 (λ: 0.035) explained 325
315 was more or less the same. 24.7% of variance in the species data. Variables such as 326
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salinity (r = − 0.7543), DO (r = − 0.2506), turbidity (r = 0.3299) 327

and NO−3 (r = 0.3556), related to axis 1 while turbidity (r = 328
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0.2388), TP (r = 0.2618), temperature (r = − 0.3275) and pH 329

(r = − 0.3647) associated with axis 2. The RDA ordination 330
0.6
331
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diagram clearly shows that different cyanobacterial species

have correlations with different water quality parameters. 332
Almost all cyanobacterial species observed in Batticaloa 333
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Lagoon negatively correlated with salinity and DO while 334

Ana.
Nitrate

they positively correlated with NO−3, TP, turbidity and tem-

Art.

335
C

Aph.
Mic. perature. Microcystis, Arthrospira, Nostoc, Anabaena, Lyngbya 336
Mer.
N

Table 3 – Summary of RDA between environmental factors t3:1

and cyanobacterial abundance in Batticaloa Lagoon during t3:2
U

the entire period of study (monsoon periods have been t3:3

considered as a covariate in the analysis). t3:4
t3:5
-0.8 Axis 1 2 t3:6
-1.0 1.0
Eigen values 0.212 0.035 t3:7
Species-environment correlations 0.809 0.613 t3:8
Fig. 4 – The first two axes of RDA for environmental factors
Cumulative percentage variance of species data 21.9 25.5 t3:9
associated with the cyanobacteria variation during the study
Cumulative percentage variance of species– 72.3 84.3 t3:10
period at Batticaloa Lagoon (monsoon period is considered environment relation
as a co-variable in the analysis). Aph.: Aphanothece sp., Sum of all unconstrained Eigen values 0.971 t3:11
Chr.: Chroococcus sp., Mic.: Microcystis sp., Spi.: Spirulina sp., Sum of all canonical Eigen values 0.294 t3:12
Gla.: Glaucocystis sp., Ana.: Anabaena sp., Anab.:
In the model, 1: monsoon period was coded as the north-east monsoon t3:13
Anabaenopsis sp., Cyl.: Cylindrospermopsis sp., Nostoc: Nostoc period, 2: 1st inter-monsoonal period, 3: south-west monsoon period t3:14
sp., Art.: Arthrospira sp., Lyn.: Lyngbya sp., Osc.: Oscillatoria and 4: 2nd inter-monsoonal period. RDA: redundancy analysis. t3:16
t3:15
sp., Mer.: Merismopedia sp. RDA: redundancy analysis.

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 6 ) XX X–XXX 7

337 and Aphanothece sp. strongly positively correlated with via particle ingestion or by the uptake of DOC (Anderson et al., 370
338 turbidity, NO−3 and TP. General water quality and purity of 2002). It has also been documented that some cyanobacteria 371
339 water is affected by the abundance of that group. Oscillatoria (example, Microcystis sp.) could make vertical movements to 372
340 strongly positively correlated with pH. During the north-east the water surface by regulating their buoyancy within the 373
341 monsoonal period (wettest period) among the 22 species water column through intracellular gas vacuoles; in this way 374
342 found in the lagoon only 12 species were abundant. During such cyanobacterial species can thrive by obtaining enough 375
343 the south-west monsoonal period (driest period) abundance light under high turbidity or low light penetration conditions 376
344 of cyanobacterial species were high compared with the other while enhancing their dominance by inhibiting the growth 377
345 periods. Monsoonal period accounted for 2.9% of the varia- of other algae (Reynolds et al., 1987; Anderson et al., 2002; Su 378
346 tions observed in the species data. et al., 2014). 379
347 Generally, temperature is a limiting factor for cyanobacterial All species negatively correlated with salinity, but posi- 380
348 growth (Hansson, 1996; Lu et al., 2013). Temperature beyond tively correlated with NO−3 and TP levels. Generally, higher 381

F
349 15°C is considered as the threshold value (Hansson, 1996; Lu phosphorous (P) levels are known to favor cyanobacteria (Fong 382
350 et al., 2013). However, in Sri Lanka temperature throughout et al., 1993; Kuffner and Paul, 2001; Anderson et al., 2002). 383

O
351 the year is far exceeding 15°C. Therefore, temperature is not In analyzing Pearson correlations the same trends were 384
352 a limiting factor for cyanobacterial growth in countries such observed in RDA ordination diagrams. However, it should be 385

O
353 as Sri Lanka; Batticaloa District occurs within the Dry Zone of noted that Pearson correlations between any species and NO−3, 386
354 Sri Lanka and the total annual mean rainfall is 1704.7 mm, TP and pH is not significant (Table 4). 387
355 annual mean daily maximum and minimum temperatures are

R
356 30.6 and 24.3°C, respectively. 2.5. Implications of this study in the management of the 388
357 Although high turbidity levels are known to suppress lagoon 389

P
358 cyanobacterial growth by decreasing light penetration for
359 photosynthesis, this study showed a positive relationship Since this study elucidates a positive relationship be- 390
360 between cyanobacterial abundance and turbidity during all tween nutrient levels (NO−3 and TP levels), turbidity and
D 391
361 periods of investigation. Turbidity is mostly governed by the cyanobacterial abundance in brackish waterbodies such as 392
362 amount of total suspended solids in the water, but algae and Batticaloa Lagoon, development and implementation of 393
E
363 organic detritus particles derived from bloom decay together a comprehensive nutrient management strategy (largely 394
364 with co-occurring bacteria can cause further increase in water focusing on P) and sediment entry control is of paramount 395
turbidity (Lu et al., 2013). It is likely that phosphates and NH+4
T

365 importance. Controlling internal loading of P requires consid- 396

366 ions adsorbed to suspended sediments and nutrients and erable attention since many cyanobacteria such as Anabaena 397
C

367 dissolved organic carbon (DOC) released during algae and sp., Oscillatoria sp. and Cylindrospermopsis sp. have the ability to 398
368 detritus decay may favor cyanobacterial proliferation. Some fix atmospheric N2 (Lu et al., 2013) and hence NO−3 or any other 399
369 cyanobacterial species have an ability to acquire both N and C nitrogenous material is not a limiting factor for cyanobacterial 400
E
R

t4:1 Table 4 – Pearson correlation coefficients between the selected parameters during all periods investigated.
R

t4:3
t4:2
t4:4 Cyanobacterial species Salinity DO Turbidity Nitrates TP Temperature pH

t4:5 −0.650⁎⁎ −0.451 0.761⁎⁎

O

Aphanothece sp. 0.42 0.429 0.586 0.102

t4:6 Chroococcus sp. −0.184 0.062 −0.142 −0.063 −0.113 −0.031 −0.041
t4:7 Microcystis aeruginosa −0.41 −0.446⁎ 0.628⁎⁎ 0.197 0.395 0.483⁎ −0.095
−0.510⁎ 0.486⁎ 0.459⁎
C

t4:8 Microcystis sp2 −0.281 0.218 0.086 −0.25

t4:9 Spirulina major −0.666⁎⁎ −0.439 0.701⁎⁎ 0.418 0.378 0.442 0.076
t4:10 Spirulina princeps −0.392 −0.074 0.327 0.369 0.01 0.212 −0.178
N

t4:11 Spirulina subsalsa −0.283 0.029 −0.066 −0.359 −0.18 0.3 0.005
t4:12 Glaucocystis sp. −0.691⁎⁎ −0.543⁎⁎ 0.730⁎⁎ 0.610⁎⁎ 0.450⁎ 0.458⁎ 0.144
t4:13 Anabaena oscillarioides −0.617⁎⁎ −0.385 0.533⁎⁎ 0.305 0.203 0.279 −0.276
U

t4:14 Anabaena sp2 0.09 0.016 −0.038 −0.247 −0.348 −0.485⁎ −0.534⁎
t4:15 Anabaenopsis arnoldii −0.498⁎ −0.358 0.569⁎⁎ 0.205 0.035 0.338 −0.394
t4:16 Anabaenopsis sp2 0.119 −0.059 0.047 −0.155 −0.329 −0.351 −0.483⁎
t4:17 Cylindrospermopsis sp. −0.499 −0.238 0.342 0.134 0.003 0.122 −0.336
t4:18 Nostoc sp. −0.673⁎⁎ −0.531⁎⁎ 0.753⁎⁎ 0.515⁎ 0.386 0.461 0.004
t4:19 Arthrospira maxima −0.415 −0.279 0.072 0.525⁎ 0.08 −0.172 0.064
t4:20 Arthrospira sp2 −0.281 −0.208 −0.083 0.562⁎ 0.009 −0.087 0.086
t4:21 Lyngbya sp. −0.544⁎ −0.176 0.404 0.297 0.066 0.239 −0.275
t4:22 Oscillatoria sancta −0.512⁎ −0.365 0.49 0.349 0.132 0.389 −0.257
t4:23 Oscillatoria sp2 −0.049 0.363 −0.368 0.304 −0.163 −0.318 0.154
t4:24 Merismopedia glauca −0.184 −0.127 0.253 0.109 0.234 −0.043 −0.304
t4:25 Merismopedia sp2 0.171 −0.18 0.115 0.093 0.263 −0.017 0.095

t4:26 ⁎⁎p < 0.01 and ⁎p < 0.05 show significant correlations between the parameters and respective cyanobacterial species; for example Aphanothece
t4:27
t4:28 sp. abundance significantly (p < 0.01) correlated with salinity and turbidity. DO: dissolved oxygen; TP: total phosphorus.

Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020
 8 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 6 ) XXX –XXX

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Please cite this article as: Harris, J.M., et al., Spatial and temporal distribution of cyanobacteria in Batticaloa Lagoon, J. Environ. Sci.
(2016), http://dx.doi.org/10.1016/j.jes.2016.01.020