Short-term changes in phytoplankton assemblages and their potential for heavy metal bioaccumulation – a laboratory study

Abd-Ellatif M. Hussian 1 , Ahmed M. Abd El-Monem 1 , Agnieszka Napiórkowska-Krzebietke 2  and Naser S. Flefil 1
  • 1 National Institute of Oceanography and Fisheries (NIOF), 101 El Kasr El Aini St., Cairo, Egypt
  • 2 Department of Hydrobiology, Inland Fisheries Institute, Oczapowskiego 10, 10-719, Olsztyn, Poland
Abd-Ellatif M. Hussian
  • National Institute of Oceanography and Fisheries (NIOF), 101 El Kasr El Aini St., Cairo, Egypt
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Ahmed M. Abd El-Monem
  • National Institute of Oceanography and Fisheries (NIOF), 101 El Kasr El Aini St., Cairo, Egypt
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Agnieszka Napiórkowska-Krzebietke
  • Corresponding author
  • Department of Hydrobiology, Inland Fisheries Institute, Oczapowskiego 10, 10-719, Olsztyn, Poland
  • Email
  • Search for other articles:
  • degruyter.comGoogle Scholar
and Naser S. Flefil
  • National Institute of Oceanography and Fisheries (NIOF), 101 El Kasr El Aini St., Cairo, Egypt
  • Search for other articles:
  • degruyter.comGoogle Scholar

Abstract

This study focused on phytoplankton changes in polluted waters of Lake Manzala and the assessment of heavy metal bioaccumulation capacity during the 15-day laboratory experiment. Phytoplankton samples were analyzed every day and the concentration of zinc, iron and lead in water, in phytoplankton and in filtrate – every fifth day of the experiment. Significantly higher phytoplankton abundance was recorded in water from the El-Boom station (basin I) compared to the New Bahr El-Baqar drain (basin II), followed by distinct differences in its composition and chlorophyll content. However, the most abundant species were the same in both basins, i.e. Chroococcus minor, Microcystis aeruginosa, Actinoptychus octonarius, Aulacoseira granulata, Pantocsekiella ocellata, Kirchneriella obesa and Nephrocytium limneticum. Water in basin I was more polluted with heavy metals compared to basin II. Basin I was characterized by the dominance of cyanobacteria and high relative abundance of chlorophytes compared to basin II, where either cyanobacteria and/or diatoms dominated in the phytoplankton. In the former basin, the highest uptake factors (UFs) were recorded for iron and zinc and the lowest UF for lead. In basin II, the highest UF was determined for zinc, but relatively high UFs were recorded also for iron and lead. The presented results suggest that phytoplankton can contribute to natural biosorbents of heavy metals in Egyptian lakes.

Introduction

At present, significant changes in lake ecosystems occur worldwide due to the impact of various climatic and anthropogenic factors. This applies also to the Egyptian lakes (El-Shabrawy et al. 2015; Shadrin et al. 2016). The pollution with heavy metals is one of the major environmental problems in recent years (Fu & Wang 2011), which affects i.e. Lake Manzala in Egypt (Zahran et al. 2015), but also other lakes in most countries around the world (Jaishankar et al. 2014). Consequently, water pollution affects the natural balance of aquatic ecosystems (Kosygin et al. 2007), which is largely associated with industrial, sewage or agricultural drainage (Sathware et al. 2007). The Bahr El-Baqar drain, considered as one of the most heavy-metal polluted drains in Egypt (Abdel-Shafy & Aly 2002), receives and carries most of the wastewater (3 billion m3 per year or about 60 m3 s−1 according to Stahl et al. 2009) into Lake Manzala. The drain runs through a very densely populated area of the Eastern Delta, i.e. through Qalyubia, Sharkia, Ismailia and Port Said Governorate. Zahran et al. (2015) demonstrated that Lake Manzala is highly contaminated with iron (Fe), cadmium (Cd), lead (Pb) and chromium (Cr), because of the continuous supply of various pollutants. The highest heavy metal concentrations were recorded in the northeastern and southern parts of the lake near the Bahr El-Baqar drain. Heavy metals, which are directly related to environmental pollution, have a major impact on all organisms (Mason 2002). This applies in particular to the biological toxicity of iron, copper (Cu), lead, cadmium, mercury (Hg), nickel (Ni), zinc (Zn) and manganese (Mn). The above metals tend to bio-accumulate and are ultimately transferred to higher levels of the food chain (Gustav 1974; Jaishankar et al. 2014). Some metals, such as Cu, Mn, Fe, and Zn, are considered essential micronutrients but become toxic when present in higher concentrations than those needed for normal growth (Nies 1999). Other heavy metals (e.g. Cd, Hg, and Pb), which play an unknown role in living organisms, are even toxic at very low concentrations (Wood 1974; Nies 1999).

The non-degradability and toxicity of heavy metals (Kathal et al. 2016) may cause serious damage to the health of organisms inhabiting a given ecosystem or to human health through the food chain (Angelone & Bini 1992; Chan et al. 2003; Tchounwou et al. 2012; Ali et al. 2016). Heavy metals can be directly accumulated by some organisms, e.g. phytoplankton. Such bioaccumulation capacities are often considered good indicators of exposure and risk, and they have been extensively used to assess contamination levels of heavy metals in polluted ecosystems (Phillips & Rainbow 1994). Several studies were undertaken to quantify the use of phytoplankton in either bioindication of environmental changes or heavy metal bioaccumulation (e.g. Hussian et al. 2015; Ali et al. 2016; Goher et al. 2016). Aquatic environments are usually rich in phytoplankton resources, which are relatively inexpensive to process and capable of accumulating high levels of metals, and can also be used as inexpensive biosorption materials in environmentally friendly technologies. The use of living phytoplankton to remove toxic metals from contaminated waters can be widespread, because phytoplankton is ubiquitous in almost all parts of the world. Metals can be removed from the surrounding environment through the accumulation in cells during both nonmetabolic-dependent (adsorption) and metabolic-dependent (absorption) processes (Perez-Rama et al. 2002; Malik 2004; Mehta & Gaur 2005; Perales-Vela et al. 2006; Topperwien et al. 2007; Lavoie et al. 2009). Furthermore, the direct or indirect presence of phytoplankton in the diet of many herbivores and predators contributes significantly to the bio-transfer of heavy metals to higher trophic levels. Thus, the phytoplankton and the assessment of its potential for heavy metal bioaccumulation are of particular concern. The amount of heavy metals in planktonic organisms may depend on their content in water and partly in sediment, as well as several environmental factors (Elmaci et al 2007). According to the findings of Bahnasawy et al. (2011), the concentrations of Cu, Zn, Cd, and Pb were much higher in phytoplankton than in water. This may be related to the active metabolism of planktic microorganisms characterized by rapid adsorption, the high surface-area-to-mass ratio, or even the fact that some microalgal species can also protect themselves by accumulating some pollutants, such as heavy metals, in their polysaccharide walls (Ravera 2001). Furthermore, some factors, including e.g. productivity and physicochemical properties of water bodies, quantitative and qualitative features of planktic assemblages, absorption capacity of heavy metals or even the seasons can affect the content of heavy metals in phytoplankton (Elmaci et al 2007).

The objective of this study was to describe the abundance and structure of phytoplankton in the polluted waters and to assess its ability to accumulate the selected heavy metals, primarily zinc, iron and lead regarded as the main pollutants in Lake Manzala.

Materials and methods

Water sampling and experiment setting

Water samples were collected from two sites: the El-Boom station (1) and the New Bahr El-Baqar drain (2) in Lake Manzala in Egypt (Fig. 1), in spring 2017. Lake Manzala is a coastal lake of the northern Nile Delta, surrounded with wetlands. It is one of the most important lakes with high fish production (about 30% of the total catch in Egypt). The Bahr El-Baqar drain is located in the eastern part of the Nile Delta (Abdel-Fattah & Helmy 2015). It runs for about 170 km from Cairo to Lake Manzala (Abdel-Shafy & Aly 2002), discharging approximately 1122 million m3 of drainage waters with a salinity of 1237 g m−3 into the lake. Furthermore, the Bahr El-Baqar drain is considered as one of the most polluted drains with industrial and urban sewage, and with water unsuitable for reuse (Soleiman et al. 1994). Bahr El-Baqar with coordinates of 31°7′0″N and 32°6′0″E is divided into the new and old Bahr El-Baqar drains, which are connected with the lake in the south-eastern part. The El Boom station is located at the main west channel of the Bahr El-Baqar drain.

Figure 1
Figure 1

Water sampling sites: 1 – El-Boom station, 2 – New Bahr El-Baqar drain in Lake Manzala in Egypt

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Both sampling sites were polluted with heavy metals (Stahl et al. 2009). Furthermore, they differed in terms of physicochemical parameters, primarily nutrients (Table 1). The concentrations of mineral nitrogen and phosphorus were generally higher at the New Bahr El-Baqar drain, while salinity lower than at the El-Boom station. The highest differences were related to ammonium (30 times), nitrates (7 times) and nitrites (3 times), and only about 1.5 times in the case of phosphorus. However, nutrient enrichment and low Secchi disk depth also indicated the hypertrophic conditions at both sampling sites.

Table 1

Physicochemical parameters of waters at two sampling sites in Lake Manzala in spring 2017

ParametersUnitsSampling sites
El-BoomNew Bahr El-Baqar Drain
Temperature°C26.426.2
Secchi disk depthm0.30.2
Total solidsg l−13.713.03
Total dissolved solids3.462.65
Total suspended solids0.250.39
Electrical conductivitymS cm−15.414.12
pH7.987.78
Dissolved oxygenmg l−114.21.2
Biological oxygen demand31.547.5
Chemical oxygen demand2.88.8
Nitritesμg l−121.1268.57
Nitrates15.17110.1
Ammonium325.379862.26
Orthophosphates324.53445.08
Total phosphorus331.94480.38
Silicon dioxidemg l−110.9810.67
SalinityPSU2.662.12
TSI (Trophic State Index)a82.7 (hypertrophy)86.7 (hypertrophy)

Each 500 l water sample was transported to the aquarium. Basin I contained a water sample from the El-Boom station and basin II – a water sample from the New Bahr El-Baqar drain. Each basin was additionally divided into two 250 l glass subbasins to get more replications. The experiment was carried out without any additional treatments, supported only with air pumps and neon light, and then incubated at a laboratory temperature of 25°C for 15 days.

To follow up quantitative and qualitative changes in phytoplankton in the two basins during the experiment, daily water samples were collected to measure the total chlorophyll as a phytoplankton biomass proxy. Other samples were preserved to investigate the species composition and its density.

To evaluate the uptake for some heavy metals, the interval water sampling (on the 1st, 5th, 10th and 15th day) starting from the beginning to the end of the experiment was applied to each basin. The three kinds of samples for measurements of the total heavy metals: (1) in water – before the filtration process, (2) in phytoplankton (fresh weight) and (3) in filtrate – after filtration through GF/F filter paper, were collected. The samples were preserved with 15% nitric acid (HNO3) and placed into a freezer (at −20°C). They were stored in a refrigerator for atomic absorption measurements.

Analyses of chlorophyll, phytoplankton and heavy metals

A known volume of water samples was filtered in situ through a glass microfiber filter GF/F. The filter paper with filtrate was wrapped in aluminum foil and preserved in a dark ice box. In the laboratory, chlorophyll was extracted by soaking the filter in 5 ml acetone (90%) and preserved in dark at 20°C overnight. The samples were shaken thoroughly and centrifuged. The clear acetone extract was siphoned carefully and then measured spectrophotometrically to estimate chlorophyll a, b and c, using 90% acetone as blank. To measure pheophytins, the extract was acidified with 2 drops of 4N HCl and re-measured to calculate pheophytins. The concentrations of chlorophyll a, b, c and pheophytins were calculated according to APHA (1992).

For quantitative and qualitative analysis of phytoplankton, 250 ml of water samples was preserved with 4% neutral formalin and Lugol’s iodine solution, which was then transferred into a glass cylinder with extra Lugol’s iodine solution added to faint tea color, covered with aluminum foil and allowed for 5 days to settle (APHA 2012). Ninety percent of the supernatant fluid was siphoned off, the sample volume was adjusted to fixed volume (25 ml) and transferred to a small plastic vial for microscopic examination. The drop method was applied for counting and identification of phytoplankton species (APHA 2012) and triplicate samples (2 or 5 μl) were collected and examined under an inverted microscope ZEISS IM 4738, with a magnification of 400× and 1000× (with oil immersion). Results of phytoplankton density were presented as a number of cell per liter (cell l−1). The main references used in the identification included: Krammer & Lange-Bertalot (1991), Popovsky & Pfiester (1990), Ettl & Gärtner (1988), Tikkanen (1986), Prescott (1978), Starmach (1974), Deskachary (1959), Hannford & Britton (1952) and Huber & Pestalozzi (1942). Taxonomic names of species were compared with Guiry & Guiry (2017) and currently accepted names are given in this study.

Analysis of heavy metals was carried out according to APHA (2012), using atomic spectrometry: inductively coupled plasma optical emission (ICP-OES), model Agilent 5100 Synchronous Vertical Dual View (SVDV) in water and quality control samples from National Institute Standards and Technology (NIST).

Numerical and Statistical analyses

Trophic conditions in Lake Manzala were assessed according to the Trophic State Index (TSI), which was calculated from the Secchi disk depth and concentrations of chlorophyll a and total phosphorus (Carlson & Simpson 1996). The uptake factor (expressed in %) was used to assess the bioaccumulation of heavy metals by phytoplankton as follows:

UF=CPhCW×100%

where: Cph – concentration of heavy metals in phytoplankton (fresh weight) after filtration, CW – concentration of heavy metals in water before filtration.

Significant changes in chlorophyll and phytoplankton abundance in the two experimental basins were tested using the U Mann-Whitney test, which is used to compare two independent groups. Furthermore, multiple comparisons of mean ranks for all samples (ANOVA, Kruskal-Wallis test) were applied to chlorophyll concentration. The statistical analyses were provided at the 0.05 significance level (StatSoft, Inc. v. 12). A cluster analysis based on the percentage similarity of taxonomic groups and the Unweighted Pair Group Method with Arithmetic Mean (UPGMA) was applied to determine the similarity of phytoplankton assemblages’ structure on each day of the experiment in both basins (Multi-Variate Statistical Package, MVSP, Kov. Comp. Serv. 1985-2009). The existence of any relationships between the features of phytoplankton and its capacity for heavy metal bioaccumulation were additionally tested using principal component analysis (PCA) and canonical correspondence analysis CCA.

Results and discussion

Chlorophyll, phytoplankton abundance and structure during the experimental period

Changes in the chlorophyll content (as a phytoplankton biomass proxy), phytoplankton density/abundance and structure in each experimental basin were analyzed on a daily basis. The concentration of chlorophyll ranged from 126.5 μg l−1 to 557.6 μg l−1 and from 130.3 μg l−1 to 785.3 μg l−1 in basin I and basin II, respectively (Fig. 2), during the whole experimental period, with no treatments and supported only with aeration, neon light and temperature of 25°C. The larger range of concentration in water of basin II from the New Bahr El-Baqar drain corresponded also to higher levels of mineral nitrogen and phosphorus. Nonetheless, general changes in the chlorophyll concentration in both experimental basins were not statistically significant, because of similar average chlorophyll concentrations of approximately 272.4 μg l−1 in both basins. Whereas different medians and coefficients of variation suggested a variable phytoplankton growth pattern for both experimental basins. The multiple comparisons for each day of the experiment confirmed the significant differences (p < 0.05) between the 1st, 3rd, 5th and 10th, 12th, 15th, and between the 2nd, 4th, 6th, and 14th, 15th day of the experiment in basin I and basin II, respectively.

Figure 2
Figure 2

Chlorophyll content (mean ± SE, min.−max) in basin I (El-Boom station) and basin II (New Bahr El-Baqar drain) during the experimental period

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

During the experiment, phytoplankton density changed from 190 × 104 cell l−1 to 780 × 104 cell l−1 and from 215 × 104 cell l−1 to 705 × 104 cell l−1 in basin I with the water sample from the Fig. 3). The maximum phytoplankton abundance was recorded on the 10th (basin I) and 11th (basin II) day of the experiment, whereas the minimum abundance almost at the end of the experiment. The mean and median values of the total abundance were higher and the coefficient of variation was lower in basin I compared to basin II (Table 2). The differences in the phytoplankton abundance changes in both experimental basins were statistically significant (the Mann-Whitney U test, U = 54.00, p = 0.016), indicating different growth patterns of phytoplankton.

Figure 3
Figure 3

Phytoplankton abundance in basin I (El-Boom station) and basin II (New Bahr El-Baqar drain) during the experimental period; dotted lines indicate the abundance output levels of the experiment in each basin

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Table 2

General features of phytoplankton (total abundance and abundance of dominant groups, No.× 104 cell l−1) in both experimental basins

AbundanceBasin I
TotalCyanophyceaeChlorophyceaeBaccillariophyceae
Minimum190903540
Maximum780345270205
Median52525017590
Mean507.3242.3163.794.3
Standard deviation157.169.075.347.8
Coefficient of variation (%)31284651
AbundanceBasin II
TotalCyanophyceaeChlorophyceaeBaccillariophyceae
Minimum215753525
Maximum705380165260
Median32514570105
Mean361.3181.371.3105.0
Standard deviation132.191.230.364.3
Coefficient of variation (%)37504361

The phytoplankton structure was primarily due to the high contribution of three main groups, i.e. Cyanophyceae, Chlorophyceae and Bacillariophyceae (Fig. 4). Cyanobacteria were always the most dominant group in basin I, accounting for 42–57% of the total abundance. The next group, chlorophytes, accounted for 13–47% and the last group, diatoms, accounted for 8–34% of the total abundance. In basin II, on the other hand, the structure of phytoplankton varied. In the first seven days of the experiment, phytoplankton was dominated by cyanobacteria (41–73%), while later (on the 8th, 10th, 12th, 14th and 15th day) – mainly by diatoms (36–46%) or cyanobacteria (on the 9th, 11th and 13th day – 43–57%). Chlorophytes played then a less important role in phytoplankton, with an average contribution of 21% in basin II and 31% in basin I. The representatives of the remaining phytoplankton groups were noted sporadically in both basins and their contribution was up to 4%. All this may indicate that the dominance of cyanobacteria in Egyptian lakes is a persistent problem of global eutrophication and health. Furthermore, the high abundance of cyanobacteria in Lake Manzala is significantly above the WHO’s moderate risk threshold (Chorus & Bartram 1999) or even higher thresholds (Napiórkowska-Krzebietke et al. 2015) with cyanotoxin hazard.

Figure 4
Figure 4

Phytoplankton structure in basin I – El-Boom station (A) and basin II – New Bahr El-Baqar drain (B) during the experimental period

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

In general, phytoplankton assemblages in basin I were represented by a total of 68 species, belonging to 6 classes (Table 3). The highest species richness was determined for the Chlorophyceae class (25 species) with the highest abundance of Kirchneriella obesa (West) West & G.S. West and Nephrocytium limneticum (G.M. Smith) G.M. Smith. Next, the Bacillariophyceae class was represented by 18 species with the most abundant: Actinoptychus octonarius (Ehrenberg) Kützing, Aulacoseira granulata (Ehrenberg) Simonsen and Pantocsekiella ocellata (Pantocsek) K.T.Kiss & E.Ács. The Cyanophyceae class was represented by 16 species, and Chroococcus minor (Kützing) Nägeli and Microcystis aeruginosa (Kützing) Kützing were the most abundant. Furthermore, 7 species represented Euglenophyceae, whereas the lowest species richness was recorded for Dinophyceae and Conjugatophyceae, i.e. only one species for each group.

Table 3

List of phytoplankton species investigated both in basin I (El-Boom) and basin II (New Bahr El-Baqar drain) during the experimental period (dominant species are in bold)

No.SpeciesEl-BoomNew Bahr El-Baqar drain
CHLOROPHYCEAE
1Acutodesmus acuminatus (Lagerheim) P.M. Tsarenko++
2Ankistrodesmus falcatus (Corda) Ralfs++
3Ankistrodesmus fractus (West & G.S.West) Collins++
4Chlorella vulgaris Beyerinck++
5Coelastrum microporum Nägeli++
6Crucigenia tetrapedia (Kirchner) Kuntze++
7Desmodesmus bicaudatus (Dedusenko) P.M. Tsarenko+
8Desmodesmus maximus (West & G.S.West) Hegewald+
9Elakatothrix gelatinosa Wille++
10Franceia ovalis (Francé) Lemmermann++
11Fusola viridis J.W. Snow++
12Golenkinia radiata Chodat+
13Kirchneriella aperta Teiling++
14Kirchneriella major C. Bernard++
15Kirchneriella obesa (West) West & G.S. West++
16Monoraphidium convolutum (Corda) Komárková-Legnerová++
17Nephrocytium limneticum (G.M. Smith) G.M. Smith++
18Oedogonium americanum Transeau++
19Oocystis pyriformis Prescott++
20Pseudopediastrum boryanum var. longicorne (Reinsch) Tsarenko+
21Pseudokirchneriella elongata (G.M.Smith) F.Hindák+
22Quadrigula chodatii (Tanner-Füllemann) G.M. Smith+
23Scenedesmus armatus (Chodat) Chodat+
24Scenedesmus bijugus (Turpin) Lagerheim+
25Scenedesmus obtusus Meyen++
26Schroederia jadayi G.M. Smith+
27Selenastrum bibraianum Reinsch++
28Tetradesmus dimorphus (Turpin) M.J. Wynne++
29Tetraëdron minimum (A. Braun) Hansgirg++
30Tetraëdron trigonum (Nägeli) Hansgirg++
31Tetraselmis suecica (Kylin) Butcher++
BACILLARIOPHYCEAE
1Actinoptychus octonarius (Ehrenberg) Kützing++
2Aulacoseira granulata (Ehrenberg) Simonsen++
3Biddulphia biddulphiana (J.E. Smith) Boyer++
4Ceratoneis closterium Ehrenberg++
5Chaetoceros lorenzianus Grunow+
6Cocconeis neodiminuta Krammer++
7Cyclotella meneghiniana Kützing++
8Cymbella tumida (Brébisson) van Heurck+
9Entomoneis alata (Ehrenberg) Ehrenberg++
10Fragilaria vaucheriae (Kützing) J.B. Petersen++
11Lyrella lyra (Ehrenberg) Karajeva++
12Nitzschia acicularis (Kützing) W. Smith++
13Nitzschia frustulum var. perpusillum (Rabenhorst) van Heurck+
14Nitzschia linearis W. Smith++
15Nitzschia palea (Kützing) W. Smith++
16Pantocsekiella ocellata (Pantocsek) K.T. Kiss & E.Ács++
17Pinnularia major (Kützing) Rabenhorst+
18Pleurosigma elongatum W. Smith+
19Triceratium favus Ehrenberg+
20Triceratium grande var. septangulata (Kitton) Schmidt+
21Ulnaria ulna (Nitzsch) Compère++
CYANOPHYCEAE
1Anabaena wisconsinensis Prescott++
2Anabaenopsis circularis (G.S. West) Woloszynska & V. Miller++
3Aphanocapsa grevillei (Berkeley) Rabenhorst++
4Chroococcus minor (Kützing) Nägeli++
5Chroococcus minutus (Kützing) Nägeli++
6Chroococcus pallidus Nägeli++
7Dactylococcopsis raphidioides Hansgirg++
8Glaucospira laxissima (G.S. West) Simic, Komárek & Dordevic+
9Gloeobacter violaceus Rippka, J.B. Waterbury & Cohen-Bazire++
10Gloeocapsa punctata Nägeli++
11Gomphosphaeria aponina Kützing++
12Leptolyngbya tenuis (Gomont) Anagnostidis & Komárek++
13Merismopedia tenuissima Lemmermann++
14Microcystis aeruginosa (Kützing) Kützing++
15Oscillatoria tenuis C. Agardh ex Gomont++
16Phormidium inundatum Kützing ex Gomont++
17Rhabdoderma lineare Schmidle & Lauterborn++
EUGLENOPHYCEAE
1Euglena minuta Prescott++
2Lepocinclis buetschlii Lemmermann+
3Lepocinclis ovum (Ehrenberg) Lemmermann++
4Phacus longicauda (Ehrenberg) Dujardin+
5Trachelomonas armata (Ehrenberg) F. Stein++
6Trachelomonas hispida (Perty) F. Stein++
7Trachelomonas cylindracea (Playfair) T.G. Popova+
CONJUGATOPHYCEAE
1Euastrum binale var. gutwinskii (Schmidle) Homfeld+
2Cosmarium laeve Rabenhorst+
DINOPHYCEAE
1Prorocentrum tsawwassenense Hoppenrath & B.S. Leander++

+ present, - absent

The species richness of phytoplankton in the second basin was similar to that in the first basin: 67 phytoplankton species belonging to 6 classes. However, the Chlorophyceae class was represented by a larger number of species (28), while Bacillariophyceae and Euglenophyceae classes by a smaller number of species (17 and 4, respectively) compared to basin I. The two other classes were represented by only one species. Furthermore, the same species of chlorophytes, cyanobacteria and diatoms were the most abundant as in basin I.

The cluster analysis by the UPGMA method based on the percentage similarity showed considerable differences in the daily phytoplankton structure and between both experimental basins (Fig. 5A, B). Three different groups were distinguished in basin I, starting from the 4th and 9th, 2nd and 8th, 3rd and 5th experimental day with the highest phytoplankton similarity of over 95% (Fig. 5A). Samples collected on other experimental days: the 1st and 11th, 12th and 10th, 6th, 7th and 14th day with 87–94% similarity were then included among these three groups, respectively. The least similar (77%) were samples collected on the 13th and 15th day, forming the fourth group. In basin II, three groups could be distinguished (Fig. 5B). In contrast to basin I, the highest similarity of 97% was found between samples collected on the 10th and 15th day of the experiment. The most similar phytoplankton assemblages developed also on the 8th, 14th, 12th and 13th day, co-forming together the first group with the overall similarity of 85%. The “center of the aggregation” of the second group were samples collected on the 5th and 7th day of the experiment with similarity of 95%, followed by a high similarity with samples from the 9th and from the 3rd and 4th day of the experiment. The remaining samples, i.e. from the 1st, 2nd and 11th day, comprised the last group.

Figure 5
Figure 5

Cluster analysis based on similarity of phytoplankton taxonomic structure in basin I (A – water from El-Boom station) and basin II (B – water from New Bahr El-Baqar drain) during the 15-day experimental period; 1-15 consecutive days of the experiment

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Bioaccumulation of heavy metals by phytoplankton

During the experiment, the three kinds of samples, i.e. one before filtration (water samples) and two after filtration (phytoplankton fresh weight samples and filtrate samples) were collected at 5-day intervals (the 1st, 5th, 10th and 15th day) and analyzed separately for heavy metals. The highest concentration of zinc (39.3–49.0 μg l−1) and approximately 4 times lower concentration of iron (7.5–13.1 μg l−1) were recorded in water of both basins during the whole experiment period (Fig. 6). Lead was then characterized by the lowest concentrations, i.e. 0.18–0.47 μg l−1 and 0.09–0.18 μg l−1 in basin I and II, respectively. The average concentrations of Zn, Fe and Pb in water usually reached 43.5 μg l−1, 10.7 μg l−1 and 0.2 μg l−1, respectively. These concentrations did not exceed their permissible limits according to the World Health Organization (WHO 2003a,b,c). Furthermore, their mean concentrations in a sequence of Zn > Fe > Pb were ranked in a different way compared to the results from 31 sampling sites in Lake Manzala [Fe (29.6 μg l−1) > Zn (5.2 μg l−1) > Pb (4.7 μg l−1)] acquired during the previous studies (Zahran et al. 2015). In general, the water from the El-Boom station in basin I with its higher phytoplankton abundance and significantly varying chlorophyll content (on the 1st, 3rd, 5th and 10th, 12th, 15th day) was more polluted with heavy metals compared to water from the New Bahr El-Baqar drain in basin II, characterized by higher content of nutrients. Furthermore, only the concentrations of Zn and Fe statistically significantly varied (zinc p = 0.043; iron p = 0.030) in both basins.

Figure 6
Figure 6

Uptake of heavy metals: lead (a), iron (b) and zinc (c) by phytoplankton in basins I and II during the experimental period

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

General trends included the gradual decrease in the content of heavy metals in water and their rapid (especially at the beginning) increase in phytoplankton throughout the experimental period. Clear differences in bioaccumulation are reflected in the uptake factor (UF) of heavy metals in phytoplankton, including ach day of the experiment and each basin. In basin I, zinc and iron had the highest UF starting from the 5th day up to the end of the experiment (90–92% and 81–99%, respectively) (Fig. 7) along with the increase in the total phytoplankton abundance up to the 10th day. The bioaccumulation of lead in phytoplankton was the lowest up to the 10th day (16–32%), and it reached 83% only on the last day of the experiment, i.e. on the 15th day when the total abundance dropped below its initial value. Cyanobacteria dominated in phytoplankton and their abundance was approximately two times higher compared to diatoms and chlorophytes every fifth day of the experiment. The process of bioaccumulation was clearly different during the 15-day experiment in basin II. This may be due to the differences in phytoplankton abundance and structure, i.e. the lower total abundance and abundance of cyanobacteria and chlorophytes and the higher abundance of diatoms in basin II compared to basin I. Starting from the 5th day to the end of the experiment, the uptake factors were higher in the case of zinc (89–98%) and lead (63–89%), and lower in the case of iron (53–87%). Cyanobacteria dominated in phytoplankton only on the 5th day, followed by the dominance of diatoms (on the 10th and 15th day) and chlorophytes (on the 15th day). Furthermore, the total phytoplankton abundance gradually decreased up to the 10th day of the experiment along with the rapid increase in the uptake of all heavy metals. Such a different course of the bioaccumulation process due to differences in phytoplankton is consistent with findings of Elmaci et al. (2007). On the other hand, the different bioaccumulation degree can also results from the existence of two stages: the first stage of initial passive and rapid uptake of heavy metals and the second stage of active and slow uptake (Shanab et al. 2012). The present results did not show such sensitivity of cyanobacteria to heavy metals as that found by Shanab et al. (2012), maybe because the phytoplankton in Lake Manzala was dominated by chroococcalean and not by nostocalean cyanobacteria.

Figure 7
Figure 7

Uptake factor (%) used to assess the rate of heavy metal bioaccumulation by phytoplankton in basin I (A) and basin II (B)

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Furthermore, the PCA revealed the existence of correlation between the total abundance of phytoplankton and its taxonomic groups, and the content of heavy metals and bioaccumulation potential (Fig. 8A). The first two factors (PC1 and PC2) explained 73% of the total variability. The total phytoplankton abundance and the abundance of Cyanophyceae, Dinophyceae and Chlorophyceae were strongly and positively correlated with PC1, which explained 53% of the total variability. Similar relationships were recorded for the content of heavy metals in water which, in turn, was closely related to phytoplankton. The uptake factors of heavy metals were strongly and negatively-correlated with PC1, whereas such relations with PC2, which explained only 20% of the total variability, were weaker. Furthermore, the relations between phytoplankton and heavy metals were additionally checked for the samples collected on the 1st, 5th, 10th and 15th day of the experiment (Fig. 8B). It was possible to distinguish two groups, one group with samples from basin I and the other group with samples from basin II, except for samples 1 (BII) and 15(BI). CCA analysis revealed also some relationship between the dominant species and the taxonomic class of phytoplankton and bioaccumulation of heavy metals (Fig. 9). The eigenvalues were 0.037 and 0.015 for the first and the second axis, respectively. The cumulative percentage reached 40.2% of the total variation for both axes. The species-environment correlations were 0.925 and 0.795 for the 1st and 2nd axis, respectively. The grouping of the samples was very similar to that obtained with PCA.

Figure 8
Figure 8

PCA-based relationships between phytoplankton and heavy metal bioaccumulation (A) and ordination of samples (B) during the 15-day experiment in basin I (BI) and basin II (BII)

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Figure 9
Figure 9

CCA joint plot of relationships between dominant phytoplankton species and classes and iron, zinc and lead bioaccumulation capacity on the 1st, 5th, 10th and 15th day of the experiment in basin I (BI) and basin II (BII) based on Canonical Correspondence Analysis. Kirch – Kirchneriella obesa, Nephr – Nephrocytium limneticum, Actin – Actinoptychus octonarius, Aulac – Aulacoseira granulata, Pantoc – Pantocsekiella ocellata, Chrooc – Chroococcus minor, Micr – Microcystis aeruginosa, CHL – Chlorophyceae, BAC – Bacillariophyceae, CYA – Cyanophyceae

Citation: Oceanological and Hydrobiological Studies 47, 3; 10.1515/ohs-2018-0025

Cyanobacteria with Chroococcus minor and Microcystis aeruginosa, chlorophytes with Kirchneriella obesa and Nephrocytium limneticum and diatoms with Actinoptychus octonarius, Aulacoseira granulata and Pantocsekiella ocellata played the main role in the bioaccumulation of heavy metals in Lake Manzala as the most abundant species in phytoplankton. In basin I, the dominant cyanobacteria contributed primarily to the very high bioaccumulation level of iron and zinc and the reduced bioaccumulation level of lead. Chlorophytes also played an important role. In basin II, initially cyanobacteria and then diatoms primarily contributed to a similarly high UF of iron and lead and the accelerated UF of zinc.

Lake Manzala is one of the most important resources for fishing in Egypt, but it receives treated and untreated wastewaters of municipal, industrial and agricultural origin (Zahran et al. 2015). The results of the present experimental studies suggest that high cyanobacteria abundance can contribute to either nuisance problems or natural biosorbents of heavy metals in Egyptian lakes. The applicable and effective technologies including bioremediation or biosorption for removal of heavy metals (e.g. Champagne 2009; Baskaran et al. 2010; Mann & Mandal 2014; Goher et al. 2016) are still needed. Therefore, studies that have been conducted to investigate the levels of heavy metals in aquatic environments, their bioaccumulation level in organisms and factors that affect the bioaccumulation process by various organisms (Machiwa 1992; 2000; Ferletta et al. 1996; Engdahl et al. 1998) should be continued.

Conclusions

Nutrient-rich water contaminated with heavy metals delivered with wastewaters of municipal, industrial and agricultural origin was collected for further studies from two selected sites in Lake Manzala. The 15-day experiment with no additional treatments, supported only with aeration, neon light and temperature of 25°C was aimed at describing the abundance and structure of phytoplankton, and assessing the bioaccumulation potential. The water sample from the El-Boom station (basin I) was characterized by significantly higher phytoplankton abundance compared to water sample from the New Bahr El-Baqar drain (basin II) throughout the experiment period. The main phytoplankton groups were dominant Cyanophyceae and co-dominant Bacillariophyceae and Chlorophyceae. Considering the day-to-day changes in the chlorophyll content, the significant differences were recorded between selected days (the 1st, 3rd, 5th and 10th, 12th, 15th day of the experiment in basin I and the 2nd, 4th, 6th, and 14th, 15th day of the experiment in basin II). The concentrations of Zn, Fe and Pb were usually higher in basin I than in basin II. The differences were also related to the degree of bioaccumulation (expressed as an uptake factor) in phytoplankton which, in turn, was connected with clearly different structures in both basins. The dominance of Cyanobacteria with a high contribution of chlorophytes contributed to the highest bioaccumulation of iron and zinc in basin I, whereas cyanobacteria with/or primarily diatoms had an important contribution to the highest UF of zinc and similarly high UF of iron and lead in basin II.

References

  • Abdel-Fattah, M.K. & Helmy, A.M. (2015). Assessment of Water Quality of Wastewaters of Bahr El-Baqar, Bilbies and El-Qalyubia Drains in East Delta, Egypt for Irrigation Purposes. Egypt. J. Soil Sci. 55(3): 287–302.

    • Crossref
    • Export Citation
  • Abdel-Shafy, H.I. & Aly, R.O. (2002). Water issue in Egypt: Resources, pollution and protection endeavors. CEJOEM 8(1): 3–21.

  • Ali M.H.H., Hussian A.M., Abdel Satar, A.M., Goher, M.E., Napiórkowska-Krzebietke A. et al. (2016). The isotherm and kinetic studies of heavy metals biosorption by nonliving cells of Chlorella vulgaris. J. Elem. 21(4): 1263–1276. .

    • Crossref
    • Export Citation
  • Angelone, M. & Bini, C. (1992). Trace elements concentrations in soils and plants of Western Europe. In D.C. Adriano (Ed.), Biogeochemistry of Trace Metals (pp. 19–60). Lewis Publishers, Boca Raton, FL.

  • APHA (American Public Health Association) (1992). Standard methods of the examination of water and waste water. 17th edition (pp. 1–1015). AWWA, WPCF.

  • APHA (American Public Health Association) (2012). Standard Methods for the examination of water and wastewater. 22nd edition (pp. 1–1360). Washington, ISBN 978-087553-013-0.

  • Bahnasawy, M.H., Khidr, A.A. & Dheina, N.A. (2011). Assessment of heavy metals concentrations in water, plankton and fish of Lake Manzala, Egypt. Turk. J. Zool. 35(2): 271–280. .

    • Crossref
    • Export Citation
  • Baskaran, P.K., Venkatraman, B.R., Hema, M. & Arivoli, S. (2010). Adsorption studies of copper ion by low cost activated carbon. J. Chem. Pharm. Res. 2(5): 642–655.

  • Carlson, R.E. & Simpson, J. (1996). A Coordinator’s Guide to Volunteer Lake Monitoring Methods (pp. 1–96). North American Lake Management Society.

  • Champagne, P. (2009). Fixed-bed column study for the removal of cadmium (II) and nickel (II) ions from aqueous solutions using peat and mollusk shells. J. Hazard. Mater. 171(1–3): 872–878. .

    • Crossref
    • Export Citation
  • Chan, S.M., Wang, W. & Ni, I. (2003). The uptake of Cd, Cr, and Zn by the macroalga Enteromorpha crinita and subsequent transfer to the marine herbivorous rabbitfish, Sigunus canaliculatus. Arch. Environ. Contam. Toxicol. 44: 298–306.

    • Crossref
    • PubMed
    • Export Citation
  • Chorus, I. & Bartram, J. (1999). Toxic Cyanobacteria in water: A guide to their public health consequences, monitoring and management. WHO Publ., E & FN Spon, London and New York.

  • Deskachary, T.V. (1959). Cyanophyta. 1st edition (pp. 1–686). Indian Council of Agricultural Research, New Delhi.

  • Elmaci, A., Teksoy, A., Olcay Topaç, F., Özengin, N., Kurtoglu, S. et al. (2007). Assessment of heavy metals in Lake Uluabat, Turkey. Afr. J. Biotech. 6: 2236–2244.

    • Crossref
    • Export Citation
  • El-Shabrawy, G.M., Anufriieva, E.V., Germoush, M.O., Goher, M.E. & Shadrin, N.V. (2015). Does salinity change determine zooplankton variability in the saline Qarun Lake (Egypt)? Chin. J. Oceanol. Limn. 33(6): 1368–1377.

    • Crossref
    • Export Citation
  • Engdahl, S., Mamboya, F.A., Mtolera, M., Semesi, A.K. & Björk, M. (1998). The brown macroalgae Padina boergesenii as an indicator of heavy metal contamination in the Zanzibar Channel. Ambio 27 (8): 694–700.

  • Ettl, H., & Gärtner, J. (1988). Chlorophyta. II Tetrasporales, Chlorococcales, Gloeodendrales. In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßwasserflora von Mitteleuropa Band 10 (pp. 1–436). Gustav Fischer Verlag, Stuttgart, New. York.

  • Ferletta, M., Bråmer, P., Semesi, A.K. & Björk, M. (1996). Heavy metal contents in macroalgae in the Zanzibar channel – an initial study. In M. Björk, A.K. Semesi, M. Pedersén & B. Bergman (Eds.), Current trends in Marine Botanical Research in the East African Region (pp. 332–346). Proceedings of the Symposium on the Biology of Microalgae, Macroalgae and Seagrasses in the Western Indian Ocean. Stockholm: Sida.

  • Fu, F. & Wang, Q. (2011). Removal of heavy metal ions from wastewaters: A review. J. Environ. Manage. 92: 407–418.

    • Crossref
    • PubMed
    • Export Citation
  • Goher, M.E., Abd El-Monem, A.M., Abdel Satar, A.M., Ali, M.H.H., Hussian A.M. et al. (2016). Biosorption of some toxic metals from aqueous solution using non-living cells of Chlorella vulgaris. J. Elem. 21(3): 703–714. .

    • Crossref
    • Export Citation
  • Gustav, R (1974). Hazardous heavy metals: cadmium, mercury, lead and arsenic. WHO International Reference Centre for Waste Disposal (pp. 1–11), IRCWD News, Switzerland.

  • Guiry, M.D. & Guiry, G.M. (2017). AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org; searched on 16 November 2017.

  • Hannford, L.T. & Britton, M.E. (1952). The algae of Illinois (pp. 1–407). The Univ. of Chicago Press, Chicago, Illinois, U.S.A.

  • Huber-Pestalozzi, G. (1942). Das Phytoplankton des Süßwassers. 2. Teil, 2. Häfte. In A. Thienemann (Ed.) Die Binnengewasser. Band XVI (pp. 1–549). Schweizerbart’she Verlagsbuchhandlung, Stuttgart.

  • Hussian, A.M., Napiórkowska-Krzebietke, A., Toufeek, M.E.F., Abd El-Monem, A.M. & Morsi H.H. (2015). Phytoplankton response to changes of physicochemical variables in Lake Nasser, Egypt. J. Elem. 20(4): 855–871. .

    • Crossref
    • Export Citation
  • Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B. & Beeregowda, K.N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology 7(2): 60–72. .

    • Crossref
    • PubMed
    • Export Citation
  • Kathal, R., Malhotra, P. & Chaudhary, V. (2016). Phytoremediation of Cadmium from Polluted Soil. J. Bioremediat. Biodegrad. 7(6): 376–378. .

    • Crossref
    • Export Citation
  • Kosygin, L., Dhamendra, H. & Gyaneshwari, R. (2007). Pollution status and conservation strategies of Moirang river, Manipur with a note on its aquatic bio-resources. J. Environ. Biol. 28: 669–673.

    • PubMed
    • Export Citation
  • Krammer, K. & Lange-Bertalot, H. (1991). Bacillariophyceae 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßwasserflora von Mitteleuropa. Band 2/3 (pp. 1–576). Gustav Fischer Verlag, Stuttgart, Jena.

  • Lavoie, M., Le Faucheur, S., Fortin, C. & Campbell, P.G.C. (2009). Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aquat. Toxicol. 92: 65–75.

    • Crossref
    • PubMed
    • Export Citation
  • Machiwa, J.F. (1992). The anthropogenic pollution in the Dar es Salaam Harbour area. Tanz. Mar. Pollut. Bullet. 24: 562–567.

    • Crossref
    • Export Citation
  • Machiwa, J.F. (2000). Heavy metals and organic pollutants in sediments of Dar es Salaam Harbour prior to dredging in 1999. Tanz. J. Sci. 26: 29–46.

  • Malik, A. (2004). Metal bioremediation through growing cells. Environ. Int. 30: 261–278.

    • Crossref
    • PubMed
    • Export Citation
  • Mann, S. & Mandal, A. (2014). Removal of fluoride from drinking water using sawdust. Int. J. Eng. Res. Appl. 4(7): 116–123.

  • Mason, C.F. (2002). Biology of freshwater pollution. 4th edition (pp. 1–387). Essex Univ. England.

  • Mehta, S.K. & Gaur, J.P. (2005). Use of alga for removing heavy metal ions from wastewater: progress and prospects. Crit. Rev. Biotechnol. 25: 113–152.

    • Crossref
    • Export Citation
  • Napiórkowska-Krzebietke, A., Dunalska, J., Grochowska, J., Łopata, M. & Brzozowska, R. (2015). Intensity and thresholds of cyanobacterial blooms an approach to determine the necessity to restore urban lakes. Carpath. J. Earth Env. 10(2): 123–132.

  • Nies, D.H. (1999). Microbial heavy metal resistance. Appl. Micreobial. Biotechnol. 51: 730–750.

    • Crossref
    • Export Citation
  • Perales-Vela, H.V., Peña-Castro, J.M. & Cañizares-Villanueva, R.O. (2006). Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64: 1–10.

    • Crossref
    • PubMed
    • Export Citation
  • Perez-Rama, M., Alonso, J.A., Lopez, C.H. & Vaamonde, E.T. (2002). Cadmium removal by living cells of the marine microalga Tetraselmis suecica. Bioresour. Technol. 84: 265–270.

    • Crossref
    • PubMed
    • Export Citation
  • Phillips, D.J.H. & Rainbow, P.S. (1994). Biomonitoring of Trace Aquatic Contaminants. 2nd edition (pp. 1–371). London: Chapman and Hall.

  • Popovsky, J. & Pfiester, L.A. (1990). Dinophyceae (Dinoflagellitida). In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßiwasserflora von Mitteleuropa. Band 6 (pp. 1–272). Gustav Fischer Verlag, Jena, Stuttgart.

  • Prescott, A.G.W (1978). How to know the freshwater algae. The 3rd edition (pp. 1–293). WCB / McGraw, Hill.

  • Ravera, O. (2001). Monitoring of the aquatic environment by species accumulator of pollutants: a review. J. Limnol. 60: 63–78.

    • Crossref
    • Export Citation
  • Sathware, N.G., Paterl, K.G., Vyas, J.B., Patel, S., Trivedi, M.R. et al. (2007). Chromium exposure study in chemical based industry. J. Environ. Biol. 28: 405–408.

    • PubMed
    • Export Citation
  • Shadrin, N.V., El-Shabrawy, G.M., Anufriieva, E.V., Goher, M.E. & Ragab, E. (2016). Long-term changes of physicochemical parameters and benthos in Lake Qarun (Egypt): Can we make a correct forecast of ecosystem future? Knowl. Manag. Aquat. Ecosyst. 417: 18. .

    • Crossref
    • Export Citation
  • Shanab, S., Essa, A. & Shalaby, E. (2012). Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal. Behav. 7(3): 392–399. .

    • Crossref
    • PubMed
    • Export Citation
  • Soleiman, A.A., Morsy, A.M. & Kamel, G.A. (1994). Drainage water in the Nile Delta. Report 38. Drainage Research Institute Kanater, Cairo, Egypt.

  • Stahl, R., Ramadan, A.B. & Pimpl, M. (2009). Bahr El-Baqar Drain System /Egypt Environmental Studies on Water Quality. Part I: Bilbeis Drain / Bahr El-Baqar Drain. Forschungszentrum Karlsruhe in der Helmholtz-Gemeinschaft, Wissenschaftliche Berichte FZKA 7505, Germany.

  • Starmach, K. (1974). Flora Słodkowodna Polski. Tom 4. Cryptophyceae, Dinophyceae, Raphidophyceae (pp. 1–519). Kraków.

  • Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., & Sutton, D.J. (2012). Heavy Metals Toxicity and the Environment. EXS 101: 133–164. .

    • Crossref
    • PubMed
    • Export Citation
  • Tikkanen, T. (1986). Kasviplanktonopas (pp. 1–278). Helsinki. Topperwien, S., Xue, H., Behra, R. & Sigg, L. (2007). Cadmium accumulation in Scenedesmus vacuolatus under freshwater conditions. Environ. Sci. Technol. 41: 5383–5388.

  • WHO (2003a). Iron in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/8).

  • WHO (2003b). Lead in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/9).

  • WHO (2003c). Zinc in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/ WSH/03.04/17).

  • Wood, J.M. (1974). Biological cycles for toxic elements in the environment. Science 183: 1049–1052.

    • Crossref
    • PubMed
    • Export Citation
  • Zahran, M.A., El-Amier, Y.A., Elnaggar, A.A., Abd El-Azim, H. & El-Alfy, M.A. (2015). Assessment and Distribution of Heavy Metals Pollutants in Manzala Lake, Egypt. J. Geosci. Environ. Protect. 3: 107–122. .

    • Crossref
    • Export Citation

Footnotes

a

TSI calculations according to Carlson, Simpson (1996)

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Abdel-Fattah, M.K. & Helmy, A.M. (2015). Assessment of Water Quality of Wastewaters of Bahr El-Baqar, Bilbies and El-Qalyubia Drains in East Delta, Egypt for Irrigation Purposes. Egypt. J. Soil Sci. 55(3): 287–302.

    • Crossref
    • Export Citation
  • Abdel-Shafy, H.I. & Aly, R.O. (2002). Water issue in Egypt: Resources, pollution and protection endeavors. CEJOEM 8(1): 3–21.

  • Ali M.H.H., Hussian A.M., Abdel Satar, A.M., Goher, M.E., Napiórkowska-Krzebietke A. et al. (2016). The isotherm and kinetic studies of heavy metals biosorption by nonliving cells of Chlorella vulgaris. J. Elem. 21(4): 1263–1276. .

    • Crossref
    • Export Citation
  • Angelone, M. & Bini, C. (1992). Trace elements concentrations in soils and plants of Western Europe. In D.C. Adriano (Ed.), Biogeochemistry of Trace Metals (pp. 19–60). Lewis Publishers, Boca Raton, FL.

  • APHA (American Public Health Association) (1992). Standard methods of the examination of water and waste water. 17th edition (pp. 1–1015). AWWA, WPCF.

  • APHA (American Public Health Association) (2012). Standard Methods for the examination of water and wastewater. 22nd edition (pp. 1–1360). Washington, ISBN 978-087553-013-0.

  • Bahnasawy, M.H., Khidr, A.A. & Dheina, N.A. (2011). Assessment of heavy metals concentrations in water, plankton and fish of Lake Manzala, Egypt. Turk. J. Zool. 35(2): 271–280. .

    • Crossref
    • Export Citation
  • Baskaran, P.K., Venkatraman, B.R., Hema, M. & Arivoli, S. (2010). Adsorption studies of copper ion by low cost activated carbon. J. Chem. Pharm. Res. 2(5): 642–655.

  • Carlson, R.E. & Simpson, J. (1996). A Coordinator’s Guide to Volunteer Lake Monitoring Methods (pp. 1–96). North American Lake Management Society.

  • Champagne, P. (2009). Fixed-bed column study for the removal of cadmium (II) and nickel (II) ions from aqueous solutions using peat and mollusk shells. J. Hazard. Mater. 171(1–3): 872–878. .

    • Crossref
    • Export Citation
  • Chan, S.M., Wang, W. & Ni, I. (2003). The uptake of Cd, Cr, and Zn by the macroalga Enteromorpha crinita and subsequent transfer to the marine herbivorous rabbitfish, Sigunus canaliculatus. Arch. Environ. Contam. Toxicol. 44: 298–306.

    • Crossref
    • PubMed
    • Export Citation
  • Chorus, I. & Bartram, J. (1999). Toxic Cyanobacteria in water: A guide to their public health consequences, monitoring and management. WHO Publ., E & FN Spon, London and New York.

  • Deskachary, T.V. (1959). Cyanophyta. 1st edition (pp. 1–686). Indian Council of Agricultural Research, New Delhi.

  • Elmaci, A., Teksoy, A., Olcay Topaç, F., Özengin, N., Kurtoglu, S. et al. (2007). Assessment of heavy metals in Lake Uluabat, Turkey. Afr. J. Biotech. 6: 2236–2244.

    • Crossref
    • Export Citation
  • El-Shabrawy, G.M., Anufriieva, E.V., Germoush, M.O., Goher, M.E. & Shadrin, N.V. (2015). Does salinity change determine zooplankton variability in the saline Qarun Lake (Egypt)? Chin. J. Oceanol. Limn. 33(6): 1368–1377.

    • Crossref
    • Export Citation
  • Engdahl, S., Mamboya, F.A., Mtolera, M., Semesi, A.K. & Björk, M. (1998). The brown macroalgae Padina boergesenii as an indicator of heavy metal contamination in the Zanzibar Channel. Ambio 27 (8): 694–700.

  • Ettl, H., & Gärtner, J. (1988). Chlorophyta. II Tetrasporales, Chlorococcales, Gloeodendrales. In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßwasserflora von Mitteleuropa Band 10 (pp. 1–436). Gustav Fischer Verlag, Stuttgart, New. York.

  • Ferletta, M., Bråmer, P., Semesi, A.K. & Björk, M. (1996). Heavy metal contents in macroalgae in the Zanzibar channel – an initial study. In M. Björk, A.K. Semesi, M. Pedersén & B. Bergman (Eds.), Current trends in Marine Botanical Research in the East African Region (pp. 332–346). Proceedings of the Symposium on the Biology of Microalgae, Macroalgae and Seagrasses in the Western Indian Ocean. Stockholm: Sida.

  • Fu, F. & Wang, Q. (2011). Removal of heavy metal ions from wastewaters: A review. J. Environ. Manage. 92: 407–418.

    • Crossref
    • PubMed
    • Export Citation
  • Goher, M.E., Abd El-Monem, A.M., Abdel Satar, A.M., Ali, M.H.H., Hussian A.M. et al. (2016). Biosorption of some toxic metals from aqueous solution using non-living cells of Chlorella vulgaris. J. Elem. 21(3): 703–714. .

    • Crossref
    • Export Citation
  • Gustav, R (1974). Hazardous heavy metals: cadmium, mercury, lead and arsenic. WHO International Reference Centre for Waste Disposal (pp. 1–11), IRCWD News, Switzerland.

  • Guiry, M.D. & Guiry, G.M. (2017). AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org; searched on 16 November 2017.

  • Hannford, L.T. & Britton, M.E. (1952). The algae of Illinois (pp. 1–407). The Univ. of Chicago Press, Chicago, Illinois, U.S.A.

  • Huber-Pestalozzi, G. (1942). Das Phytoplankton des Süßwassers. 2. Teil, 2. Häfte. In A. Thienemann (Ed.) Die Binnengewasser. Band XVI (pp. 1–549). Schweizerbart’she Verlagsbuchhandlung, Stuttgart.

  • Hussian, A.M., Napiórkowska-Krzebietke, A., Toufeek, M.E.F., Abd El-Monem, A.M. & Morsi H.H. (2015). Phytoplankton response to changes of physicochemical variables in Lake Nasser, Egypt. J. Elem. 20(4): 855–871. .

    • Crossref
    • Export Citation
  • Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B. & Beeregowda, K.N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology 7(2): 60–72. .

    • Crossref
    • PubMed
    • Export Citation
  • Kathal, R., Malhotra, P. & Chaudhary, V. (2016). Phytoremediation of Cadmium from Polluted Soil. J. Bioremediat. Biodegrad. 7(6): 376–378. .

    • Crossref
    • Export Citation
  • Kosygin, L., Dhamendra, H. & Gyaneshwari, R. (2007). Pollution status and conservation strategies of Moirang river, Manipur with a note on its aquatic bio-resources. J. Environ. Biol. 28: 669–673.

    • PubMed
    • Export Citation
  • Krammer, K. & Lange-Bertalot, H. (1991). Bacillariophyceae 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßwasserflora von Mitteleuropa. Band 2/3 (pp. 1–576). Gustav Fischer Verlag, Stuttgart, Jena.

  • Lavoie, M., Le Faucheur, S., Fortin, C. & Campbell, P.G.C. (2009). Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aquat. Toxicol. 92: 65–75.

    • Crossref
    • PubMed
    • Export Citation
  • Machiwa, J.F. (1992). The anthropogenic pollution in the Dar es Salaam Harbour area. Tanz. Mar. Pollut. Bullet. 24: 562–567.

    • Crossref
    • Export Citation
  • Machiwa, J.F. (2000). Heavy metals and organic pollutants in sediments of Dar es Salaam Harbour prior to dredging in 1999. Tanz. J. Sci. 26: 29–46.

  • Malik, A. (2004). Metal bioremediation through growing cells. Environ. Int. 30: 261–278.

    • Crossref
    • PubMed
    • Export Citation
  • Mann, S. & Mandal, A. (2014). Removal of fluoride from drinking water using sawdust. Int. J. Eng. Res. Appl. 4(7): 116–123.

  • Mason, C.F. (2002). Biology of freshwater pollution. 4th edition (pp. 1–387). Essex Univ. England.

  • Mehta, S.K. & Gaur, J.P. (2005). Use of alga for removing heavy metal ions from wastewater: progress and prospects. Crit. Rev. Biotechnol. 25: 113–152.

    • Crossref
    • Export Citation
  • Napiórkowska-Krzebietke, A., Dunalska, J., Grochowska, J., Łopata, M. & Brzozowska, R. (2015). Intensity and thresholds of cyanobacterial blooms an approach to determine the necessity to restore urban lakes. Carpath. J. Earth Env. 10(2): 123–132.

  • Nies, D.H. (1999). Microbial heavy metal resistance. Appl. Micreobial. Biotechnol. 51: 730–750.

    • Crossref
    • Export Citation
  • Perales-Vela, H.V., Peña-Castro, J.M. & Cañizares-Villanueva, R.O. (2006). Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64: 1–10.

    • Crossref
    • PubMed
    • Export Citation
  • Perez-Rama, M., Alonso, J.A., Lopez, C.H. & Vaamonde, E.T. (2002). Cadmium removal by living cells of the marine microalga Tetraselmis suecica. Bioresour. Technol. 84: 265–270.

    • Crossref
    • PubMed
    • Export Citation
  • Phillips, D.J.H. & Rainbow, P.S. (1994). Biomonitoring of Trace Aquatic Contaminants. 2nd edition (pp. 1–371). London: Chapman and Hall.

  • Popovsky, J. & Pfiester, L.A. (1990). Dinophyceae (Dinoflagellitida). In H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer (Eds.), Süßiwasserflora von Mitteleuropa. Band 6 (pp. 1–272). Gustav Fischer Verlag, Jena, Stuttgart.

  • Prescott, A.G.W (1978). How to know the freshwater algae. The 3rd edition (pp. 1–293). WCB / McGraw, Hill.

  • Ravera, O. (2001). Monitoring of the aquatic environment by species accumulator of pollutants: a review. J. Limnol. 60: 63–78.

    • Crossref
    • Export Citation
  • Sathware, N.G., Paterl, K.G., Vyas, J.B., Patel, S., Trivedi, M.R. et al. (2007). Chromium exposure study in chemical based industry. J. Environ. Biol. 28: 405–408.

    • PubMed
    • Export Citation
  • Shadrin, N.V., El-Shabrawy, G.M., Anufriieva, E.V., Goher, M.E. & Ragab, E. (2016). Long-term changes of physicochemical parameters and benthos in Lake Qarun (Egypt): Can we make a correct forecast of ecosystem future? Knowl. Manag. Aquat. Ecosyst. 417: 18. .

    • Crossref
    • Export Citation
  • Shanab, S., Essa, A. & Shalaby, E. (2012). Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal. Behav. 7(3): 392–399. .

    • Crossref
    • PubMed
    • Export Citation
  • Soleiman, A.A., Morsy, A.M. & Kamel, G.A. (1994). Drainage water in the Nile Delta. Report 38. Drainage Research Institute Kanater, Cairo, Egypt.

  • Stahl, R., Ramadan, A.B. & Pimpl, M. (2009). Bahr El-Baqar Drain System /Egypt Environmental Studies on Water Quality. Part I: Bilbeis Drain / Bahr El-Baqar Drain. Forschungszentrum Karlsruhe in der Helmholtz-Gemeinschaft, Wissenschaftliche Berichte FZKA 7505, Germany.

  • Starmach, K. (1974). Flora Słodkowodna Polski. Tom 4. Cryptophyceae, Dinophyceae, Raphidophyceae (pp. 1–519). Kraków.

  • Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., & Sutton, D.J. (2012). Heavy Metals Toxicity and the Environment. EXS 101: 133–164. .

    • Crossref
    • PubMed
    • Export Citation
  • Tikkanen, T. (1986). Kasviplanktonopas (pp. 1–278). Helsinki. Topperwien, S., Xue, H., Behra, R. & Sigg, L. (2007). Cadmium accumulation in Scenedesmus vacuolatus under freshwater conditions. Environ. Sci. Technol. 41: 5383–5388.

  • WHO (2003a). Iron in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/8).

  • WHO (2003b). Lead in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/9).

  • WHO (2003c). Zinc in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/ WSH/03.04/17).

  • Wood, J.M. (1974). Biological cycles for toxic elements in the environment. Science 183: 1049–1052.

    • Crossref
    • PubMed
    • Export Citation
  • Zahran, M.A., El-Amier, Y.A., Elnaggar, A.A., Abd El-Azim, H. & El-Alfy, M.A. (2015). Assessment and Distribution of Heavy Metals Pollutants in Manzala Lake, Egypt. J. Geosci. Environ. Protect. 3: 107–122. .

    • Crossref
    • Export Citation
FULL ACCESS

Journal + Issues

Oceanological and Hydrobiological Studies is devoted to topics concerning the water environment, both freshwater and saltwater. The objective pursued by the Journal is to collect and publish in one medium the findings of worldwide studies on various types of water environment and climatic conditions.

Search

  • View in gallery

    Water sampling sites: 1 – El-Boom station, 2 – New Bahr El-Baqar drain in Lake Manzala in Egypt

  • View in gallery

    Chlorophyll content (mean ± SE, min.−max) in basin I (El-Boom station) and basin II (New Bahr El-Baqar drain) during the experimental period

  • View in gallery

    Phytoplankton abundance in basin I (El-Boom station) and basin II (New Bahr El-Baqar drain) during the experimental period; dotted lines indicate the abundance output levels of the experiment in each basin

  • View in gallery

    Phytoplankton structure in basin I – El-Boom station (A) and basin II – New Bahr El-Baqar drain (B) during the experimental period

  • View in gallery

    Cluster analysis based on similarity of phytoplankton taxonomic structure in basin I (A – water from El-Boom station) and basin II (B – water from New Bahr El-Baqar drain) during the 15-day experimental period; 1-15 consecutive days of the experiment

  • View in gallery

    Uptake of heavy metals: lead (a), iron (b) and zinc (c) by phytoplankton in basins I and II during the experimental period

  • View in gallery

    Uptake factor (%) used to assess the rate of heavy metal bioaccumulation by phytoplankton in basin I (A) and basin II (B)

  • View in gallery

    PCA-based relationships between phytoplankton and heavy metal bioaccumulation (A) and ordination of samples (B) during the 15-day experiment in basin I (BI) and basin II (BII)

  • View in gallery

    CCA joint plot of relationships between dominant phytoplankton species and classes and iron, zinc and lead bioaccumulation capacity on the 1st, 5th, 10th and 15th day of the experiment in basin I (BI) and basin II (BII) based on Canonical Correspondence Analysis. Kirch – Kirchneriella obesa, Nephr – Nephrocytium limneticum, Actin – Actinoptychus octonarius, Aulac – Aulacoseira granulata, Pantoc – Pantocsekiella ocellata, Chrooc – Chroococcus minor, Micr – Microcystis aeruginosa, CHL – Chlorophyceae, BAC – Bacillariophyceae, CYA – Cyanophyceae