Cyanobacterial community patterns as water quality bioindicators

Item Type article

Authors Soltani, N.; Khodaei, K.; Alnajar, N.; Shahsavari, A.; Ashja Ardalan, A.

Download date 01/10/2021 23:18:40

Link to Item http://hdl.handle.net/1834/37329 Iranian Journal of Fisheries Sciences 11(4) 876-891 2012 Cyanobacterial community patterns as water quality Bioindicators

Soltani N.1; Khodaei K.2, *; Alnajar N.1; Shahsavari A.2; Ashja Ardalan A.3

Received: March 2012 Accepted: July 2012

Abstract The main goal of this study was to examine the use of for evaluating the quality of running water. Accordingly epilithic cyanobacterial communities were collected in Dez River and Ojeyreb drain in south of Iran. Samples were collected in two seasons: autumn and spring. Effective physical and chemical factors on the structure of cyanobacterial communities and the dispersion of the species in relation with them were determined using PCA and CCA analyses. The Shannon-wiener biodiversity index was used to define the species diversity. The concentration of Nitrate as main nutrient had significant increase in Drain stations. A decline in species richness was observed associated with these increases in nutrient load in both seasons in different cyanobacterial community structure. The results indicated that order had higher proportion of cyanobacteria species at Drain. The species chlorina, Chroococcus minor, Phormidium tenue and Lyngbya kuetzingii S had the most positive correlation with nutrient factor. Species Lyngbya infixa and Lyngbya mesotrichia had the most negative correlation with nitrate. Our results confirm the using of cyanobacteria species as indicators for monitoring eutrophication in rivers and define them as water eutrophication bioindicators.

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 Keywords: Cyanobacteria, Drainage, Eutrophication, River, Water quality, PCA

______1- Research Institute of applied Science, ACECR, Shahid Beheshti University, Tehran, Iran. 2- Dept. Geology, Institute of applied Science, ACECR, Shahid Beheshti University, Evin, Tehran, Iran. 3- Dept. Marine Biology, Islamic Azad University, Tehran-North Branch, Tehran, Iran. *Corresponding Author's email: [email protected]

877 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators Introduction Monitoring of eutrophication in running communities have changed from upstream waters caused by anthropogenic activities to downstream of the rivers with physical in these ecosystems, is the first step to and chemical conditions and nutrient load define an efficient water management in the water (Perona et al., 1998; Aboal et program for preservation of these al., 2002; Douterelo et al., 2004; ecosystems. The analysis of microflora Maldonado et al., 2011). Such community structure and defined investigations led to define the bioindicators of water quality is an cyanobacteria as water quality important tool in environmental bioindicators. monitoring programs. First record of using In this study cyanobacterial biological methods to monitor river water community’s structure in Dez River and quality was introduced by Kolkwitz and Ojeyreb Drain, in Khuzestan province Marsson (1908). Many of methods have (Iran) is described in two seasons: autumn been defined to monitor rivers water and spring. Although the quality of Dez quality include employing algae, river are measured in a few papers bryophytes, macro invertebrates and fishes (Khodaie et al., 2006; Khodaie and (Whitton and Kelly, 1995). However, Shahsavari, 2003) this study is the first more recent investigations have record on Iranian river epilithic demonstrated that water quality and cyanobacterial communities and the nutrient concentration in the river waters relationship between the diversity of had the greater effect on the cyanobacterial species and physical and photosynthetic organisms as algae (Kelly chemical conditions of water to determine and Whitton, 1998). With this respect water quality indicators and compared algae such as diatom communities have with universal patterns. been widely used as bioindicators Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 (Whitton and Rott, 1996; Prygiel et al., Materials and methods 1999), and defined as biotic indices such Sampling sites were selected in order to as IBD index (based on diatoms) in the include locations above and below human rivers water quality monitoring programs. settlements and agricultural centers. The It has been found that in special ecosystem research was carried out on seven sites, of some rivers, cyanobacterial dominance including the first site at Dez river branch and cyanotoxic effect on the studied (Dez108) and the other six sites along communities would have lower values Ojeyreb drain at the end of Dez river to than expected (Aboal et al., 2002). These downstream point of this drain nearby the results highlight the necessity of Persian Gulf (Dez103-Dez107, Fig. 1). incorporating corrections in biotic indices Samples were collected two times in 2009, definitions and monitoring programs and including the end of autumn and the end of also to consider the cyanobacterial spring. Dissolved oxygen, temperature, pH communities. In recent studies it is shown and electric conductivity (EC) were that the structure of cyanobacterial measured in situ in each sampling site Iranian Journal of Fisheries Sciences, 11(4), 2012 878

- - 2- 3- using portable Multi 350i WTW (NO3 , Cl , SO4 , PO4 ) were analyzed (Germany). according to Standard Methods For Water samples were taken in each Examination of Water and Wastewater, station. Two polyethylene bottles of water (APHA) (1995); by chromatography per station were considered for chemical technique methods, respectively. analysis. Nutrient chemical concentrations

Figure 1: Geographical position of sampling sites

For sampling of cyanobacterial number of individual cells) in alternate communities in each sampling sites two transects in 16 cm2 surface on

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 stones were collected from a submerged semipermanent slides by light microscopy. part of the river bank. The attached algae The Shannon-Wiener biodiversity index were removed by brushing in 5 ml of (Margalef, 1957) was used to define the medium. Aliquots were transferred on species diversity of algae inhabiting Petri dishes with different solid culture different types of habitats. media (BBM, BG11 and Chu; Andersen, Data were subjected to multivariate 2006). Another aliquot was fixed with statistical analysis. Environment data were formaldehyde 4% for microscopic ordinated using a correlation - based examination. Cyanobacteria and principal component analysis (PCA). nomenclature is primarily classified based Relationship between cyanobacterial on the methods of Prescott (1962), abundance and environmental variables of Desikachary (1959), John et al. (2003). sampling periods were analyzed with Their abundance in epilithon samples was canonical correspondence analysis (CCA). evaluated by counting the presence of each Statistical analysis performed with Past species (as cells in filament or equal and SPSS 16 software. In addition, cluster 879 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators analysis was carried out by ward's method G.S. West, Homeothrix juliana and at Euclidian scale by PAST software. Oscillatoria annae in Dez 108, 107 and 106 sites, respectively, L.mesotrichia in Results Dez 105, 104, 103 sites and Oscillatoria OD and pH in Dez River are higher than limentica in Dez 109 sampling site. The drain sites water. No significant difference dominant species in the spring changed to between different drain sampling sites was Microcoleus chthonoplastes (Vaucher) found. However, EC had no significant Gomont, Oscillatoria subbrevis Schmidle difference in all sites, but it had higher and L. mesotrichia in Dez 108,107 and level in the autumn. Greater amount of Cl- 106, Lyngbya limnetica Lemmermann in were detected in the river than drain sites Dez 105 and 103, L.infixa in Dez104 and especially in the autumn. Amount of L.mesotrichia in Dez 109 (Fig. 2). In other sulfate at the autumn was same in all sites view the dominant filamentous but in the spring it shows high decrease in cyanobacteria species in two sampling river water. Phosphate had very low seasons were L.mesotrichia, amount in all sampling sites (not shown). P.angustissimum, O.annae, O.limnetica, These results show high variation in O.subbrevis, H.juliana, L.infixa and physical condition and nutrient content in M.chthonoplastese that the dominance of the river water and drain sites (Table 1). two species O.limnetica and L.mesotrichia Table 2 describes the occurance of species were observed in Dez River and the others in different sampling sites. The dominant were in Ojeyreb drain sites, also non- community of cyanobacteria of these filamentous dominant species were stations is created by 35 species belonging Chroococcus turgidus (Kuetz.) Naegeli, to 13 genera. Oscillatoria (7 species), Ch.minor and Dermocarpa sp.. The Lyngbya (5 species), Phormidium (3 dominance of this species just observed in species), Chroococcus (2 species) and Drain sampling sites. The most abundant Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 Anabaena, Aphanocapsa, Merismopedia , filamentous species were observed is Microcoleus, Nostoc, Plectonema each L.mesotrichia in Dez109 in the spring and with one species were present in sampling Dermocarpa sp. as non-filamentous sites. Dominant species in first sampling species in Dez105 at the autumn. were Phormidium angustissimum West et

Table 1: Variation of the chemical and physical variables associated with the quality of waters in two seasons (ANOVA, p<0.001)

- 2- -

Sampling EC T NO SO Cl Coordinates OD pH 3 4 site (µS/cm) (°C) (mg /L) (mg /L) (mg /L)

Spring Autumn Spring Autumn Spring Autumn Spring Autumn Spring Autumn Spring Autumn Spring Autumn

X=256649 Dez109 8.60 a 11.20 a 614 a 820 a 17.1 a 20.5 a 8.00 a 8.40a 5 a 14.0 a 135 a 60.0 a 66 a 89.5 a Y=3588618 Iranian Journal of Fisheries Sciences, 11(4), 2012 2012 11(4), Sciences, ofFisheries IranianJournal

X=263598 Dez108 8.60 a 7.50 a 614 a 868 a 17.1 a 21.0 a 8.00 a 7.60 b 16 a 15.0 a 172 a 50.4 a 66 a 39.0 b Y=3555420

X=263556 Dez107 7.50 b 7.03 a 723 a 917 a 24.2 b 21.5 a 7.60 b 7.70 b 16 a 19.9 a 617 b 49.0 a 69 a 44.7 b Y=3558111

X=262227 Dez106 7.12 b 6.20 b 749 a 920 a 24.3 b 22.0 a 7.55 b 7.80 b 19 a 28.9 a 104 a 71.0 a 69 a 71.5 a Y=3562155

X=262701 Dez105 6.60 b 6.94 b 787 a 937 a 24.3 b 22.6 a 7.54 b 7.70 b 22 a 19.2 a 94 a 50.8 a 77 a 38.8 b Y=3564710

X=262855 Dez104 7.89 b 7.33 a 724 a 888 a 23.4 b 22.6 a 7.43 b 7.60 b 25 a 25.0 a 243 a 49.6 a 51 b 31.6 b Y=3567886

X=262004 Dez103 5.86 b 6.38 b 743 a 904 a 22.7 b 21.1 a 7.38 b 7.45 b 28 a 25.3 a 560 b 49.4 a 48 b 31.9 b Y=3569334

8 80

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 881 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators

------+ + + + + + + A

Dez109

------S + + + + + + +

------+ + + + + + + +

A Dez108

------+ + + S + +

------+ + + + + + +

A Dez107

------S + + + + + + + + + +

------+ + + + +

A

Dez106

------S + + + + +

------+ + +

A Dez105

------S + + + + + +

------

+ + + + + + + A

Dez104

species in differentspecies site sampling ------S + + + +

------

+ + + + A Dez103

cyanobacteria ------+ + S + of

Spring

sp.

sp.

calcuttensis

Occurrence , S: sp.

sp. Species sp. Sampling site Sampling llatoria subbrevis llatoria

Autumn

Table 2: Oscillatoria chlorine Oscillatoria Osci Oscillatoria rubescens Oscillatoria Aphanocapsa greviellii Aphanocapsa Oscillatoria fragile Phormidium Phormidium tenue Phormidium Plectonema notatum Plectonema Oscillatoria subtilisima Oscillatoria Oscillatoria limnetica Oscillatoria Phormidium Phormidium angustissimum Anabaena Anabaena Calothrix Calothrix Chroococcus minor Chroococcus Chroococcus turgidus Chroococcus Dermocarpa Dermocarpa Homeoethrix juliana Homeoethrix Lyngbya cryptovaginata Lyngbya Lyngbya infixa Lyngbya Lyngbya kuetzingii Lyngbya Lyngbya limnetica Lyngbya Lyngbya mesotricha Lyngbya Merismopedia Merismopedia Microcoleus Microcoleus chthonoplastes Oscillatoria annae Oscillatoria Nostoc Nostoc

A:

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Figure2: Variability of the abundunce of dominant cyanobacteria species in two sampling seasons.

Table 3: Shannon-Wiener and Dominance indices Site Shanon-Wiener indices

spring Autumn Dez103 0.346 0.479 Dez104 0.430 0.664 Dez105 0.368 0.185 Dez106 0.964 0.309 Dez107 0.178 0.756 Dez108 0.732 0.322 Dez109 0.221 0.273

Maximum species diversity was observed values. Positive and negative values on

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 - in autumn in Dez 106 and 108 sampling second component were associated to NO3 sites and so the minimum diversity was in and Cl- concentrations, respectively. At the Dez 107 in spring. Increases in the spring sampling as above, the first two diversity Ordination of environmental data components explained 96% of the data by PCA showed a clear pattern. In the variance (pc1=3.9, pc2= 0.08). Positive autumn sampling the first two components values on first component were associated 2- explained 98% of the data variance to EC and SO4 and negative values were - (pc1=3.5, pc 2=0. 03) on component 1, associated to pH, OD and NO3 high positive values were associated to EC concentration. Cl- concentration is 2- (then SO4 ) and pH, OD (then associated to negative values on the temperature) were related to high negative second component (Fig. 3). 883 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators

(a) Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018

(b)

Figure 3: PCA analysis of environmental data obtained in (a) autumn and (b) spring

Iranian Journal of Fisheries Sciences, 11(4), 2012 884

(a) Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018

(b) Figure 4: CCA ordination plot in (a) autumn and spring (b)

885 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators …

(a) Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018

(b) Figure 5: Dendrograms of the Cyanobacterial communities groups based on environmental factors of sampling sites (a) autumn, (b) spring

Iranian Journal of Fisheries Sciences, 11(4), 2012 886

The preliminary cyanobacteria CCA III. Species with direct positive analysis was carried out on the basis of correlation to EC and seven variables in two sampling seasons: temperature autumn and spring, shown in table 1, to IV. species with direct positive -2 show the species- environment correlation. correlation to OD, SO4 and Aphanocapsa greviellii (Hassall) pH Rabenhorst, O.rubescens (de Candol) The dissimilarity between groups was Gomont, O.subbrevis and Ch.minor in higher than -9.6. The CCA analysis results -2 autumn showed the highest direct revealed that EC, OD and SO4 are the correlation to EC and another hand the main factors influencing the species L.mesotrichia, M.sp., H.juliana cyanobacterial species communities in the and O.limnetica have the highest autumn. Three groups of species could be 2- correlation to OD and SO4 , and distinguished from the dendrogram of the L.mesotrichia and H.galiana in the spring cluster analysis the spring sampling: samplings showed the highest direct I. A species with highest positive 2- -2 correlation to OD and SO4 . O.chlorina, correlation to Cl . C.minor, L.kuetzingii, P.tenue have the II. Species with positive direct - -2 highest positive and L.mesotricha, correlation to NO3 , EC and SO4 . C.turgidus and H.juliana have the highest III. Species with highest positive - 2- negative association to NO3 and SO4 as direct correlation to OD. nutrient water ions (Fig. 4). Cluster The dissimilarity between groups analysis was performed to separate the was higher than -8.0 the CCA analysis -2 - Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 species to distinct groups based on results confirmed that EC, SO4 , NO3 and environmental factors, with the help of OD are the main factors influencing the CCA analysis results (Fig. 5).In autumn cyanobacterial species communities in the sampling, 4 groups of species could be spring. distinguished from the dendrogram based on hierarchical cluster: Discussion I. A species with highest direct Our results revealed great difference in correlation just to OD. physical condition and nutrient content II. Species with direct positive between river and Drain water, that led to correlation to EC and negative different cyanobacterial community correlation to temperature. structures in this locations, so we can define two different zones: The fresh water of the river and also second station in the 887 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators … Drain water where subjected to a communities in high level of dissolved particularly wide variety of perturbations oxygen were shown in fresh waters as domestic waters and due to agricultural (Whitton, 1992). Our results showed the practices. In describing of water chemical highest direct correlation between OD and content a distinction can be drawn between abundance of two species L.mesotrichia 2- conservative chemical factors as pH, SO4 and H.juliana. Abundance of some species , Cl-, etc. that closely associated with such as A. greviellii, O.rubbescens, lithological composition of river basin and O.subbrevis and O.limnetica also determine the mineralization of the water correlated with this factor. and non-conservative component such as It has described an increase in nutrient whose concentrations depend on prevalence of cyanobacteria in response to local conditions (Sabater et al., 1990). different types of fluvial pollutions such as There are many records confirmed that the eutrophication (Shaji and Patel, 1991), cyanobacteria community responds to high level of organic pollution (Necchi et changes in fresh water quality and there is al., 1994) and high relative abundance of not always a general response for all filamentous cyanobacteria with increasing cyanobacteria as group, since the fecal coliform concentration or urban responses of single species can be quite wastewater (Vis et al., 1998). At least it different. So changes in cyanobacterial had confirmed that epilithic cyanobacterial communities or single species can be used communities are suitable eutrophication as water quality bioindicators (Douterelo bioindicators in the rivers (Perona et al., et al., 2004). 1998). Our results showed less nitrate level

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 In this study PCA analysis results in the river than drain water, whereas the showed that physical parameters such as phosphate concentration had very low OD, EC and pH have the most important level in both. CCA analysis results showed - effect on describing the patterns of the highest negative correlation with NO3 cyanobacterial species diversity that have concentration and species L.infica and higher level in the river water than drain L.mesotrichia abundance. Also C.turgidus, sites. There are a few results about the L.mesotrichia and H.juliana have effect of physical water conditions on the significant decreases in abundance at sites - cyanobacterial communities. with high level of NO3 . C.minor has the - In previous studies the use of most positive correlation with NO3 - epilithic diatoms as acidity indicators concentration. Increase of NO3 level in the (Coring, 1996) and the negative effect of water has direct effect on the abundance of OD on richness of cyanobacterial O.chlorine, L.kuetzingii and P.tenue Iranian Journal of Fisheries Sciences, 11(4), 2012 888

species. In subsequent reviews polluted water in agreement with previous (Fjerdingstad, 1964; Sladeček, 1973; Rott suggestions (Perona et al., 1999). Results et al., 1997) several species of genera also confirm that cyanabacteria Oscillatoria emerged as organically community responds to changes in fresh polluted waters. However, Oscillatoria water quality and can be used as species such as O.limosa and O.boryana bioindicators in environmental studies of (Rott and Fister, 1988; Aboal, 1989) quality of these ecosystems. became more abundant in enriched waters; The present study clearly species belonging to Oscillatoriales were illustrated the response of cyanobacterial associated with highly eutrophic media. species and structure of their communities Douterelo (2004) defined greater number to fresh water quality and replacement of of Oscillatoria species at the downstream sensitive species in cleaned waters to sites of the rivers that had high trophic resistant species in the drain as polluted levels. Also, our study confirmed the water. In confirmation of previous reports relationship between water entrophication this study showed that most abundant and Oscillatoria abundance. species in eutrophic water of the drain In addition, this study suggested that belonged to Family , C.minor and then O.chlorina, P.tenue and besides in this study the frequent presence L.kuetzingiias can be as indicators of of Chroococcus minor, O. chlorina, eutrophic waters. In the other hand, some P.tenue and L.kuetzingii were reported in genera such as Nostoc (Sabater 1983; the drain water. On the other hand the Aboal, 1988), Chamaespihon (Sabater, abundance of species L.mesotrichia,

Downloaded from jifro.ir at 17:22 +0330 on Wednesday February 14th 2018 1983; Aboal, 1988), Calothrix and L.infixa, H.juliana and Chroococcus Scytonema (Fernandez-pinas et al., 1991) turgidus in the river indicates how are commonly associated with low level influenced or unpolluted waters. So these nutrient waters and upstream sites. Our species can be considered as bioindicators results also suggested the presence of two in the environmental monitoring programs. Lyngbya species L.mesotrichia and The results of such studies could be led to L.infixa and other species H.juliana and define a universal freshwater quality index Chroococcus turgidus as low influenced based on cyanobacterial community environment or unpolluted waters structures. indicators. Totally, these results showed the Acknowledgements replacement of sensitive species in cleaned waters to resistant species in the drain as 889 Soltani et al., Cyanobacterial community patterns as water quality Bioindicators … This work was supported by the grant No. Institüte fur Botanik, Universität 1427-55 from the research council of Innsbruke, Austria. pp. 7-16. ACECR, Tehran, Iran. Desikachary, T. V., 1959. Cyanophyta. Indian council of agricultural research, References New Delhi. Aboal, M., 1988. Aportacio´n al Douterelo, I., Perona, E. and Mateo, P., conocimiento de las algas 2004. Use of cyanobacteria to assess epicontinentales del sudeste de water quality in running waters. Espana. III: Cianoficeas Environmental Pollution, 127, 377- (Cyaniphyceas Schaffner 1909). 384. Anales del Jardin Botanico de Fernandez-piñas, F., Leganés, F., Madrid, 45, 3-46. Mateo, P. and Bonilla, I., 1991. Use Aboal, M., 1989. Epilithic algal of algae for monitoring Rivers. Institut communities from River Saegure fur Botanik, Universitat Innsbruck , Basin, southeastern Spain. Archive für Innsbruck, Austria. pp. 151-156. Hydrobiology, 116, 113-124. Fjerdingstad, E., 1964. Pollution of Aboal, M., Puig, M. A., Mateo, P. and streams estimated by benthal Perona, E., 2002. Implication of phytomicro-organisms. I. A saprobic cyanophyte toxicity on biological system based on communities of monitoring of calcareous streams in organism and ecological factors. north-east Spain. Journal of Applied International Review of Hydrobiology, Phycology, 14, 49-56. 99, 63-131.

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