J. Subtrop. Agric. Res. Dev. 7(3): 645-652, June 2009, www.gscience.

net

CYANOBACTERIAL ABUNDANCE AND BLOOM DYNAMICS IN TWO URBAN WASTEFED FISH POND OF BANGLADESH R. SHARMEEN1, M. A. S. JEWEL1 and M. BELAL HOSSAIN2*
ABSTRACT Cyanobacteria abundance and nutrient dynamics was studied in two urban wastefed fish ponds of Rajshahi City Corporation from January to December, 2006. Twenty three species of cyanophyceae under 8 genera were identified. Cyanophyceae was highest (90.15x10 6cells/L) in August, 2006 in pond-1 and 156.0x106cells/L in pond-2 in September, 2006. Lowest cell density (2.16x10 6cells/L and 3.97x10 6cells/L) was observed in January in both the ponds. Cyanophyceae was also abundant in March (spring) when temperature started to rise. Four species of Microcystis were also identified, among which M. aeroginosa formed a bloom in August (81.64% of total cyanophyceae ) and September (83.24% of total cyanophyceae) in pond-1 and pond-2 respectively. Further, 3 species of Anabaena: (A. circinalis, A. spiroides and A. flosaquae), 2 species of Planktothrix (P. agardhii and P. rubescens) were most commonly encountered. Environmental factors like surface water temperature, transparency, pH, Dissolve Oxygen, free Carbon dioxide, Biological Oxygen Demand (BOD5), NO2 -N, NH3 -N, NH4+, Oxidation Reduction Index (rH2) and their relationship with cyanophyceaewere studied. Cyanophyceae.showed positive correlation with temperature, pH, free carbon dioxide, NO 2 -N, NH3-N, and NH4+. Nutrients were high during peak periods of cyanophyceae. Oxidation Reduction Index (rH 2) was low during cyanophyceae dominance in August and September indicating high organic load in water. This condition of eutrophication in urban fish ponds is one of the major causes of noxious cyanophyceae bloom. Cyanophyceae showed negative correlation with Chlorophyceae, Euglenophyceae, Bacillariophyceae.

Keywords: Cyanophyceae, Water quality, Bloom, Wastefed pond and Pollution.

INTRODUCTION Eutrophication is the result of uncontrolled human population growth and the discharge of urban, industrial and agricultural effluents into the aquatic ecosystem (Tundisi and Matsumura Tundisi, 1992). One of the most severe problems associated with eutrophication of urban freshwater ecosystem is the occurrence of frequent blooms of toxic cyanobacteria. Urban run-off can contain high concentrations of nutrients, oxygen-consuming wastes, pathogens and toxic substances such as pesticides, heavy metals and oils (Peterson et al., 1985). Eutrophication is mostly caused by sewage discharge into lakes and ponds. Environmental pollution from wastes induces changes to the structure and function of biological systems (Odiete, 1999). There are over 30 species of cyanobacteria that can be associated with toxic blooms (Skulberg et al., 1993). The species responsible for most of the poisonous outbreaks are Microcystis aeruginosa Kutz, Anabaena flos-aquae (Lyngb.) Breb and Aphanizomenon flosaquae (L.) Ralfs (Carmichael and Bent,1981). Massive growth (bloom) of cyanobacteria (blue-green) in ponds, lakes, reservoirs or other freshwater systems has become serious water quality problem for human and animal health (WHO, 2003). Occurrences of cyanobacterial bloom typically appear in eutrophic lakes, which either has encountered anthropogenic nutrient loading or are naturally nutrient rich (Vaitomaa, 2006). Cyanobacterial blooms can cause a variety of water quality problems, including dissolved oxygen depletion and subsequent fish kills, aesthetic nuisances and unpalatable, possibly even unsafe drinking water (Carmichael, 2001). Rabergh et al., (1991) reported that the damage of liver, kidney, heart, gills, skin, and spleen of fish were associated with toxic cyanobacterial blooms. Studies of the seasonal cycle and bloom dynamics of cyanobacteria in urban wastefed fish ponds is very scarce. During the summer and monsoon season there is continuous flushing of drains in to the urban ponds. As a result the confined waters of the pond become eutrophicated due to sedimentation of nutrients and decomposition of
1

Department of Fisheries, University of Rajshahi, Rajshahi-6205, Bangladesh, 2Department of Fisheries and Marine Science, Noakhali Science and Technology University, Sonapur-3802, Bangladesh, *Corresponding author: Email:belalhossain@yahoo.com

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organic matter that induce toxic and noxious blooms of cyanobacteria. Therefore, present study was done on seasonal abundance and bloom dynamics of cyanobacteria in eutrophic wastefed urban fish ponds. MATERIALS AND METHODS Study area: The study was conducted in two urban fish culture ponds for a period of 12 months from January to December 2006. Pond-1 is situated in Baliapukur and pond-2 in Hadirmor under Rajshahi City Corporation. Pond-1 receives domestic wastes and decomposed organic nutrients through 2 drains and pond-2 from 5 drains. Analysis of water quality: Surface water samples were collected once a month from 10 to11 am. Water samples were collected in black plastic bottles for estimation of different chemical parameters. Plankton samples were collected by German plankton net of 55m mesh size and preserved in 5% formalin. Surface water temperature and transparency was measured using a Celsius thermometer and a secchi disk. pH, NO2-N, NH3-N, NH4+ was measured using a HACH kit (Model FF-2). Dissolved Oxygen (DO) and Biological Oxygen Demand (BOD) were estimated by Winklers titration method (APHA, 1976). Oxidation Reduction Index (rH2) was calculated by using the formula given by Mukherjee (1996). Phytoplankton Study: For species identification samples were gently shaken to resuspend all materials and allowed to settle for one minute. Then 2-3 drops were removed from the middle of the sample and kept on a glass slide. Taxonomic determination of phytoplankton was done with an Olympus (Japan) phase contrast light Microscope at 100 to 400 x with bright field and phase contrast illumination on (Anagnostidis and Komarek, 1985; Skulberg et al., 1993 and Bellinger, 1992). Quantitative estimation of phytoplankton was done on Sedgewick-Rafter counting chamber (S-R cell) following the method described by Stirling (1985). The results were summarized as cells per liter. Seasons were divided as summer (June through August), autumn (September through November), winter (December through February) and spring (March through May). RESULTS AND DISCUSSION During the study period, 23 species of cyanophyceae identified were Microcystis aeruginosa, M. flosaquae, M. viridis, M. wesenbergii, M. botrys, M. natans, Anabaena circinalis, A. spiroides, A. flosaquae, Planktothrix agardhii, P. rubescens, Aphanocapsa delicatissima, A. muscicola, A. crassa, A. koordersi, Anabaenopsis arnoldii, Merismopedia elegans, M. minima, M. tenuissima, Gleocapsa granosa, G. calcarea, G. magma, Arthrospira platensis (Table 1). Cyanophyceae cell density varied from 2.16106 to 90.15106 cells/l and 3.97106 to 156.0106 cells/l in pond-1 and pond-2 respectively. Highest cell density (156.0x106 cells/l) of cyanobacteria was observed in September in pond-2 while lowest (2.16x 106 cells/l) was observed in January, 2006 in pond-1. Vardaka et al. (2005) observed that cyanobacteria comprised 90% of total phytoplankton and identified Microcystis aeruginosa, M. flosaquae, M. ichthyoblabe, M. novacekii, M. viridis and M. wesenbergii. According to them M. aeruginosa was the most dominant species in the Greek waterbodies. Cyanophyceae cell density was relatively high in pond-2 than in pond-1, because pond-2 received sewage waste from 5 drains located at different sides compared to the 2 drains in pond-1. These drains are continuously flushing decomposed organic waste, domestic or kitchen wastes from the neighboring households, surface runoff from the surrounding area and household washing. Jewel (2004) and Affan et al. (2005) reported that in summer months more nutrient accumulated from surface run-off due to rainfall and from the drains of three residential halls of the university students into the Isha kha lake which created favourable condition for the maximum growth of Cyanobacteria.Blooms of toxic cyanobacteria in lakes, reservoirs and rivers are associated with enrichment by nutrients (Fergunson, 1997). Municipal and industrial discharges, urban storm water and agricultural drainage can transport in trace metals, nutrients, pesticides and organic wastes into aquatic ecosystems (Bryan and Langston, 1992). May (1981) reported that bloom of Microcystis aeruginosa and Anabaena circinalis were increasing due to increasing pollution of the water. 2

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Cyanophyceae abundance in August and September may be attributed to higher concentration of NO 2-N (0.3 mg/l and 0.5 mg/l), NH3-N (2.0 mg/ml and 3.0 mg/l), NH4+ (1.65 mg/l and 2.47 mg/l), high temperature (33.21C and 33.50C), alkaline pH (8.8 and 8.8 in pond-1 in August and in pond-2 in September) and bright sunlight which created favourable condition for better propagation of this group of phytoplankton (Fig 1). Tilman et al. (1986) reported that cyanobacteria show dominance at temperature higher than 20C which agrees with the present study. Highest NH4+ concentrations (2.03 mg/l and 3.02 mg/l) occurred in March when cyanophyceae was second highest. According to Siddiqa (2002), higher values of cyanobacterial concentration were found in August and September, which may be due to less rainfall and higher rate of decomposition of organic matter and high temperature. Dissolved oxygen (DO) was low (0.62 mg/l and 0.46 mg/l) during cyanobacterial dominance (August and September) in the studied ponds. Dahl et al. (1989) reported that oxygen deficits resulting from decomposition of algal matter, with the ensuring death of fish and other animal, constitute a regular environmental problem in the southern Kattegat between Denmark and Southern Sweden. In the present study, BOD values were decreased with increased growth of cyanobacteria. Chowdhury et al. (1996) reported higher abundance of phytoplankton with poor BOD values during their study period. Kolte and Goyal (1989) reported that blue-green algal cell density increased with the increase of nitrogen in the media. Lowest values of rH2 were observed in August and September, which indicates organic loads are higher in the aquatic ecosystem. Again according to Mukherjee (1996) anaerobic forms were found in the bottom with a low oxidation reduction index. Alkaline nature of water with a hypolimnion oxygen deficit and an occurrence of Cyanophyceae plankton, especially Microcystis sp. are indicative of a eutrophic or highly productive nature of a body of water (Hasan, 2000).

Pond 1

Pond 2

Temperature ( C), Transparency (cm)

Total Cyanophyceae (x10 cells/l)

100 90 80 70 60 50 40 30 20 10 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

70 60 50 40 30 20 10 0

180 160 140 120 100 80 60 40 20 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

40 35 30 25 20 15 10 5 0

Temperature ( C), Transparency (cm)

Total Cyanophyceae Transparency

Temperature pH

Total Cyanophyceae Transparency

Temperature pH

Total Cyanophyceae (x10 cells/l)

and pH

Total Cyanophyceae (x10 cells/l)

Total Cyanophyceae 100 80 60 40 20 0

BOD

DO 3.5
DO and BOD (mg/l)

Total Cyanophyceae (x10 cells/l)

Total Cyanophyceae 200 150 100 50 0

BOD

DO 3.5 3 2.5 2 1.5 1 0.5 0

DO and BOD (mg/l)

3 2.5 2 1.5 1 0.5 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

and pH

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Total Cyanophyceae NH3-N(mg/l) 100

(x10 cells/l)

NH4 (mg/l) NO2-N (mg/l)

NH3-N (mg/l), NO2-N (mg/l) and NH4 (mg/l)

Total Cyanophyceae NH3-N(mg/l) 180 160 140 120 100 80 60 40 20 0

NH4 (mg/l) NO2-N (mg/l)

(mg/l) (mg/l) and NH 4
+

3.5 3 2.5 2 1.5 1 0.5 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months
NH3 -N (mg/l), NO -N 2

Total Cyanophyceae

2.5 2 1.5 1 0.5 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

Total Cyanophyceae

80 60 40 20 0

(x10 cells/l)

Total Cyanophyceae 100 90 80 70 60 50 40 30 20 10 0

rH2
Total Cyanophyceae (x 10 cells/l)

Total Cyanophyceae

rH2 35 30 25
rH2

Total Cyanophyceae (x 10 cells/l)

30 29 28 27 26 25 24 23 22 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

180 160 140 120 100 80 60 40 20 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

20 15 10 5 0

Fig. 1. Effect of physicochemical parameters on the abundance of total cyanophyceae in pond 1 and pond 2. Table 1. The list of Cyanophyceae species observed among the two urban wastefed fish ponds during the study period.
Division Class Order Hormogonales Family Nostocaceae Genus Anabaena Bory Species Anabaena circinalis Rabenh. Anabaena flosaquae Breb. Anabaena spiroides Kleb. Anabaenopsis arnoldii Aptekarj

Anabaenopsis Morren Aphanocapsa delicatissima West and G.S.West Aphanocapsa muscicola Mengh Aphanocapsa Ngeli Aphanocapsa crassa Ghose Aphanocapsa koordersi Strom

Cyanophyceae

Cyanophyta

Chroococcaceae

Chroococcales

rH2

Oscillatoriaceae

Oscillatoriales

Microcystis Lemmermann

Gleocapsa Kutzing Merimopedia Ngli

Microcystis aeruginosa(Ktzing)Lemmermann Microcystis flosaquae (Wittrock) Kirchner Microcystis botrys Teiling Microcystis viridis (Braun) Lemmermann Microcystis natans Lemmermann Microcystis wesenbergii (Komarek) Starmach Gleocapsa calcarea Tilden Gleocapsa magma (Breb) Ktz Gleocapsa granosa (Breb) Ktz Merismopedia elegans A.Br. Merismopedia elegans A.Br.

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Planktothrix Anagnostidis and Komrek Arthrospira Stizenberge

Merismopedia minima Beck. Merismopedia tenuissima Lemmermann Planktothrix agardhii Anagn et. Kom. Planktothrix rubescens Anagn et. Kom Arthrospira platensis (Nordst) Gomont

Twenty three species of cyanophyceae under 8 genera were identified of which Microcystis sp., Anabaena sp., Planktothrix sp., were the most dominant genera. Microcystis aeruginosa was the bloom forming species in August and September. Microcystis aeruginosa was the most dominant species among the other species of Microcystis. M. aeruginosa cell density was highest (129.85x106 cells/l) in September (Table 2) which was 83.24% of total cyanophyceae (Fig 2) and lowest (0.02x10 6 cells/l) in January in pond-1. A. circinalis was highest among the Anabaena species, highest (17.72 x106 cells/l) was observed in March which was 13.16% of total cyanophyceae in pond-2 and lowest (0.59x106 cells/l) in January in pond-1. P. agardhii was highest (2.73x 106 cells/l) in March which was 13.42% of total cyanophyceae and lowest (0.08x 106 cells/l) in August in pond-2.
Pond-1 Microcystis aeruginosa 100%
Relative abundance (%) of different species among total cynophyceae

Pond-2
Planktothrix agardhii

Anabaena circinalis

Microcystis aeruginosa 100%

Relative abundance (%) of different species among total cynophyceae

Anabaena circinalis

Planktothrix agardhii

90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Months

Fig 2. Showing relative abundance (%) of Microcystis aeruginosa, Anabaena circinalis and Planktothrix agardhii in pond-1 and pond-2 from January to December, 2006.

Table 2. Monthly variation of different Cyanophyceae species in pond 1 and pond 2 (January to June).
January P1 P2 M. aeruginosa 0.02 0.04 M. flosaquae 0.05 0.08 M. viridis 0.49 0.92 M. wesenbergii 0.53 1.02 Anabaena circinalis 0.59 1.13 Anabaena spiroides 0.16 0.29 Anabaena flosaquae 0.08 0.13 Planktothrix agardhii 0.19 0.18 Planktothrix rubescens 0.03 0.11 Aphanocapsa 0.004 0.02 Anabaenopsis 0.004 0.02 Merismopedia 0.004 0.01 Gleocapsa 0.004 0.01 Arthrospira 0.004 0.01 February P1 P2 0.67 2.61 0.55 2.17 1.66 4.76 1.66 4.42 1.03 3.24 0.09 0.67 0.09 0.45 0.55 0.84 0.10 0.12 0.03 0.03 0.02 0.03 0.02 0.02 0.01 0.02 0.01 0.01 March P1 P2 60.18 103.83 5.23 7.19 0.62 1.98 0.26 1.69 8.55 17.72 0.65 0.31 0.36 0.42 2.73 1.06 0.33 0.17 0.19 0.07 0.19 0.07 0.19 0.07 0.16 0.05 0.16 0.05 April P1 P2 0.02 0.04 0.05 0.08 0.49 0.92 0.53 1.02 0.59 1.13 0.16 0.29 0.08 0.13 0.19 0.18 0.03 0.11 0.004 0.02 0.004 0.02 0.004 0.01 0.004 0.01 0.004 0.01 May P1 P2 0.67 2.61 0.55 2.17 1.66 4.76 1.66 4.42 1.03 3.24 0.09 0.67 0.09 0.45 0.55 0.84 0.10 0.12 0.03 0.03 0.02 0.03 0.02 0.02 0.01 0.02 0.01 0.01 June P1 P2 60.18 103.83 5.23 7.19 0.62 1.98 0.26 1.69 8.55 17.72 0.65 0.31 0.36 0.42 2.73 1.06 0.33 0.17 0.19 0.07 0.19 0.07 0.19 0.07 0.16 0.05 0.16 0.05

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Table 2. Monthly variation of different Cyanophyceae species in pond 1 and pond 2 (July to December).
July M. aeruginosa M. flosaquae M. viridis M. wesenbergii Anabaena circinalis Anabaena spiroides Anabaena flosaquae Planktothrix agardhii Planktothrix rubescens Aphanocapsa Anabaenopsis Merismopedia Gleocapsa Arthrospira P1 6.94 2.22 0.67 0.36 2.63 0.15 0.15 0.26 0.08 0.02 0.02 0.01 0.01 0.01 P2 14.79 5.03 1.11 1.11 5.14 0.52 0.37 0.27 0.07 0.03 0.03 0.02 0.02 0.01 August September P1 P2 P1 P2 73.06 33.16 21.44 129.85 2.50 4.64 2.91 4.55 0.38 2.39 0.78 0.90 0.23 1.3 0.77 0.65 8.05 8.69 4.78 17.67 1.34 0.42 0.83 1.39 1.05 0.22 0.62 0.60 1.89 0.08 0.60 0.21 0.33 0.05 0.13 0.06 0.19 0.03 0.04 0.03 0.19 0.03 0.04 0.03 0.19 0.02 0.04 0.03 0.11 0.02 0.02 0.02 0.1 0.02 0.02 0.01 October P1 P2 7.81 11.59 3.82 5.74 0.84 1.09 0.82 0.88 3.16 5.55 0.65 0.62 0.54 0.56 0.85 0.25 0.09 0.08 0.04 0.01 0.05 0.02 0.05 0.02 0.04 0.02 0.03 0.02 November P1 P2 3.72 6.13 2.04 3.50 0.89 2.04 0.97 1.39 2.47 3.29 0.36 1.14 0.28 0.39 0.36 0.15 0.10 0.13 0.02 0.005 0.03 0.006 0.03 0.007 0.02 0.006 0.01 0.006 December P1 P2 0.04 0.13 0.31 1.01 0.62 2.02 0.77 2.52 0.74 2.81 0.12 0.59 0.12 0.15 0.24 0.61 0.15 0.15 0.02 0.01 0.02 0.01 0.02 0.01 0.02 0.02 0.01 0.01

Cyanobacteria showed negative correlation with Chlorophyceae (r= -0.322; pond-1 and r = -0.304; pond-2), Euglenophyceae (r= -0.135; pond-1 and r = -0.351; pond-2) and Bacillariophyceae (r= -0.055; pond-1 and r = -0.449; pond-2) (Table 3). Table 3. Correlation co-efficient between Cyanophyceae and other groups of phytoplankton.
Correlation Pond-1 Pond-2 -0.322 -0.304 -0.135 -0.351 -0.055 -0.449 Calculated t Pond-1 Pond-2 2.152 2.134 2.137 2.132 1.918 1.867 Tabulated t Pond-1 Pond-2 2.23 2.23 2.23 2.37 2.45 2.45

Cyanophyceae vs Chlorophyceae Cyanophyceae vs Euglenophyceae Cyanophyceae vs Bacillariophyceae

In pond-1, Microcystis was abundant throughout the study period, with maximum (82.76%) in summer, second highest in spring (78.76%) and lowest in winter. Anabaena and Planktothrix were highest (25.92% and 10.81% respectively) in the winter and lowest in summer. In pond-2, Microcystis was most dominant in autumn (83.99%) and second highest in spring (80.57%). Similar to pond-1, Anabaena and Planktothrix showed dominance in winter (28.52% and 6.06% respectively) but was lowest in autumn in pond-2 (Fig. 3). Pond 1
Relative abundance (%) of different species of cyanophyceae

Pond 2
Planktothrix
Relative abundance (%) of different species of cyanophyceae

Microcystis
90 80 70 60 50 40 30 20 10 0 Summer

Anabaena

Microcystis 90 80 70 60 50 40 30 20 10 0 Summer

Anabaena

Planktothrix

Autumn Seasons

Winter

Spring

Autumn

Winter

Spring

Seasons

Fig.3. Showing seasonal relative abundance values of the three most common Cyanophyceae species (Microcystis, Anabaena and Planktothrix) in pond-1 and pond-2. Summer (Jun-Aug), autumn (Sep-Nov), winter (Dec-Feb), spring (Mar-May). 6

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Microcystis aeruginosa was the most dominant species representing 81.64% (August) and 83.24% (September) of total Cyanophyceae in the two ponds. Oudra et al. (1998) recorded 95% of M. aeruginosa in a cyanobacterial bloom in eutrophic Lalla Takerkousta reservoir in Morocco. In pond-1 a bloom of M. aeruginosa was observed in summer while a bloom of M. aeruginosa developed in autumn in pond-2. Watson et al. (1997) also found cyanobacterial bloom in warmer months in eutrophic lakes with lowest average biomass in nutrient poor systems. Seasonal variation of different cyanophyceae species showed that Anabaena and Planktothrix showed dominance in both ponds in winter when Microcystis was lowest. Jewel et al. (2006) Microcystis aeruginosa might have some growth inhibitory substance which may suppresse the growth of other species. Cyanophyceae showed negative correlation with chlorophyceae, euglenophyceae and bacillariophyceae. Negative correlation of cyanophyceae with chlorophyceae indicated the growth inhibitory effect of cyanobacteria with chlorophyceae which agrees with the findings of Lam and Silvester (1979). A gradual elimination of the members of chlorophyceae and bacillariophyceae was probably due to the presence of the members of cyanophyceae earlier found by Naz (1999). In the study pond fish farmers reported that the people who bathed in the studied ponds suffered from skin rashes and eye and ear irritation during the bloom of cyanophyceae. The owner of the fish mortality pond in Mymensingh reported that people who used the pond water for bathing were affected by skin rashes and eye inflammation Jewel et al. (2003). In the present study, Cyanophyceae was characterized by summer and autumn domination of Microcystis aeruginosa. Temperature, pH and Nutrient concentration were found high during peak period of cyanobacterial bloom. rH2 factor was found low during cyanobacterial dominance in both ponds indicating high organic load in pond water. Hence further study will have to be taken to determine heavy metals and toxicity test of cyanobacteria in waste fed fish pond in other parts of Bangladesh. REFERENCES
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