O A

3433
Journal of Applied Sciences Research, 8(7): 3433-3447, 2012
ISSN 1819-544X
This is a refereed journal and all articles are professionally screened and reviewed
ORIGINAL ARTICLES
Regional and Seasonal Variation of Phytoplankton Assemblages and its Biochemical
Analysis in Ismailia Canal, River Nile, Egypt.
Howayda H. Abd El-Hady and Abd-Ellatif M. Hussian
Inland and Water Aquaculture Branch, National Institute of Oceanography and Fisheries (NIOF)
ABSTRACT
Phytoplankton community assemblages and its major metabolites (proteins, carbohydrates and lipids) were
evaluated through collecting seasonal samples from 16 stations along Ismailia Canal. Some physico-chemical
and biological characteristics were measured. The community composition of phytoplankton was dominated by
Bacillariophyceae, which contributed about 76.3% of total phytoplankton density and represented by 34 taxa.
Cyclotella meneghiniana, Cyclotella ocellata, Melosira granulate and Syndra ulna were abundant among the
group. Chlorophyceae with 51 taxa, dominated mainly by Actinastrum hantzchii, Pediastrum simplex,
Scenedesmus acuminatus, Scenedesmus ecornis and Staurastrum paradoxium came next, forming 16.5%, while
Cyanophyceae (25 taxa) was only constituted 6.5% of total phytoplankton crop. The biochemical contents of
phytoplankton shows a noticeable seasonal variation. The highest protein contents (11.61 g/l) was recorded in
spring, which concurrently with pronounced increase in phytoplankton crop (828 x 104 cells/l), while the highest
carbohydrates (82.5 mg/l) and lipids (12.34 mg/l) were measured in summer. Protein constitutes the major part
of the biochemical contents of the phytoplankton, while lipid constitutes the minor one. Cluster analysis
according to phytoplankton analysis revealed three main groups. The highest similarity percent of 78.3% was
recorded within group 1 (station 5 and 7). The results of Shanon diversity index indicate that, stations 11, 12, 13
and 16 sustained from incipient pollution. Thus phytoplankton could be used as biomarker of pollution in
Ismailia Canal.
Key words: Ismailia Canal, Physico-chemical variables, Phytoplankton community structure, Biochemical
compositions.
Introduction
Ismailia Canal is one of the most important water supplies and irrigation canal in Egypt. It was constructed
in 1862 in order to transfer fresh water from River Nile (north of Cairo at El-Mazalet region) to Ismailia, Port
Said and Suez governorates. It is the principle source of drinking water for a great number of the Egyptian
citizens (Geriesh et al., 2004). The canal received a lot of industrial waste water covering the industrial activities
such as petroleum, petrogas, iron and steel and detergent industries as well as water treatment plants and power
station, which caused dramatic changes in its water quality (Abdo, 1998; Geriesh et al., 2008 and Youssef et al.,
2010). Microbial contaminants, such as viruses and bacteria, and inorganic and organic contaminants were
found away to its water (Geriesh et al., 1999). Abdo et al., (2010, a) mentioned that the main pollution sources
of Ismailia Canal were due to the domestic and effluents of police camp and petroleum companies. Therefore,
the wastewater effluents should be treated before its drainage in the canal.
Microalgae are common, normal inhabitants of surface water and are beneficial to the health of a water
body, they represent primary producers of organic matter which provide food base for most marine and
freshwater food chains and play an important role in the equilibrium of aquatic ecosystem (Campanella et al.,
2000 and Field et al., 2007). Also microalgae have many uses, they can serve as water bioremediation agents
(Oswald, 1992), to feed fish and its fry in aquaculture (De Pauw and Persoone, 1992), as food for humans and
other invertebrates (Becker, 1992 and Roslin, 2003), in pigment and oil production (Johnson and An, 1991), and
in bioremoval of heavy metals (Wilde and Benemann, 1993 ). Great biochemical diversity of microalgae makes
them a valuable potential renewable source of new drugs, growth regulators and other useful chemicals (Tredici
and Materassi, 1992).
The metabolites content depends on the location and environment in which the algae are grown. The
environment includes altitude, temperature and sun exposure, which can greatly affect the lipid and pigment
content in algae (Singh et al., 2005). Algae and microalgae have been studied as a potential natural source of
different functional compounds and as a new and unlimited source of new functional food ingredients
(Meendiola et al., 2005; Herrero et al., 2006; Meizoso et al., 2008 and Plaza et al., 2008). In lsmailia Canal,
Corresponding Author: Howayda H. Abd El-Hady, Inland and Water Aquaculture Branch, National Institute of
Oceanography and Fisheries (NIOF)
E-mail: [email protected].
3434
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
very rare research studies have been conducted on the field of biochemical contents of phytoplankton. The
present work was established to evaluate temporal and spatial variability in phytoplankton community structure
besides its biochemical content in Ismailia Canal which is reliable biomarker of specific water quality problems.
This work considered as one of the first studies concerning the effect of environmental factors on the algal
biochemical compositions.
Material and Method
The study site:
Ismailia Canal is one of the largest freshwater canal branched from the Nile and has become of importance
since it provides water for irrigation; navigation; industrial and domestic purposes to areas in the eastern region
of Egypt (Ibrahim et al., 2009). It is 294.4 km long and the average of each of water depth is 2.8 m, water
velocity is 0.28 m s−1 and its discharge reached 7 × 106 m3s−1 (MWRI, 2002). Seasonal water samples were
collected from 16 stations representing the whole different microhabitats of the canal during 2011 (Fig. 1).
Fig. 1: The sampling locations of Ismailia Canal.
Physico-chemical characteristics:
Temperature, pH, transperancy, Electrical conductivity and dissolved oxygen were measured at each site.
Water temperature was measured by an ordinary thermometer, pH by Orion Research Ion Analyzer 399A pH
meter and transparency by Secchi disc. Electrical conductivity was measured using Hydro-Lab., "Multi 340 II
SET". Dissolved oxygen (DO) was determined by azide modification method as specified in APHA (1998). The
chemical parameters were analyzed by the members of the project environmental and chemical studies on
Ismalia Canal, River Nile, Egypt, 2011.
3435
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Phytoplankton sampling and composition:
One litter of water was collected from each selected stations, immediately preserved with Lugols iodine for
phytoplankton analysis. In the laboratory, the samples are transferred into a glass cylinder and left 5 days for
settling. About 90% of the supernatant siphoned off using plastic tubes covered with plankton net (5µ), and
adjusted to a fixed volume. Lugol-preserved subsamples were prepared for species identification and
enumeration using inverted microscope. Each sample was examined and counted using a Drop method
technique (APHA, 1995). The main references used in phytoplankton identification were Hannford and Britton
(1952), Deskachary (1959), Starmach (1974), Prescott (1978), Tikkanen (1986), Httl. Hand and Gartner (1988),
Popovsky and Pfiester (1990) and Krammer and long Bertalot (1991).
Biochemical analysis:
At each station water samples were collected by plastic bottles, then sieved and filtered through
zooplankton net (100 µm mesh size) to separate macrozooplankton. Then 10 ml of the filtered water was refiltered on Whatman GF/F (0.7 µm pore diameter) fiber circles and the samples were transferred to the
laboratory in ice tanks to determine the biochemical parameters of the separated phytoplankton. The total
protein contents was determined by Biuret method (David and Hazel, 1993), whereas, the total lipid content was
determined by the Sulphophosphovanillin procedure (SPV) (Chabrol and Castellano, 1961). Carbohydrate
contents were measured according to Phenol-sulphuric acid method as described by Dubois et al. (1956).
Statistical analysis:
The data recorded in this study were examined with a normalized principal component analysis (PCA)
(Chessel and Dolédec, 1992). Pearson’s correlation analysis was performed to evaluate the relationships
between physico-chemical variables, phytoplankton densities and biochemical contents, using XL stat software
version 2012. Shannon-Winner diversity, species richness, evenness and similarity index were calculated, using
Primer 5 program.
Results and Discussion
Physico-chemical characters:
The quality of drinking water has been decreased during this century due to discharge of wastewater and
pollutants into water resources (Abdo et al., 2010a). Although Ismailia Canal is a branch of River Nile, the
quality of its water is totally different (Tarek and Ali, 2007). Ismailia Canal represents the most distal
downstream of the main River Nile, so it considered as a sink for all pollutants dischargered into the Nile. In
addition, the canal is endangered from unwise, direct and indirect activities in the surrounding environments
(e.g. collapses of the canal bank due to the seepage effluent, close distribution of farmer’s houses to the canal
banks, industrial zone located directly on the canal bank).
It is well known that, the physical and chemical characteristics controlling life in aquatic habitats, which
lead to the appearance of special types of biota (Fathi and Flower, 2005). Temperature has controlling effect on
the activities and distribution of phytoplankton (Sobhy, 2006). During this study the average water temperature
was subjected to seasonal variations (16.2-18.1, 21.4-23.6, 23.7-33.1 and 25.1-28.1oC) during winter, spring,
summer and autumn, respectively. The relative increase in water temperature at summer is due to the thermal
pollution discharged to the canal from the petroleum companies located on the canal bank (Abdo et al., 2010a).
Water turbidity is caused by inorganic (sand, clay and silt) and organic matters (seston and planktons). The
clarity of a natural body of water is a major determinant of its condition and productivity (APHA, 1998). The
turbidity degree of stream water is an approximate measure of the intensity of the pollution (Siliem, 1995).
Transparency results ranged between 30-70, 25-80, 30-100 and 20-100 cm during winter, spring, summer and
autumn, respectively. The low transparency values recorded during winter, which concurrently with the
decrease in water level during drought period (Abdo, 1998). Hydrogen ion concentration (pH) is the master that
control of all aquatic chemical and biological processes, the pH of natural water affects biological and chemical
reactions, control the solubility of metal ions, and affect natural aquatic life. The desirable pH for fresh - water
aquatic life is in the range of 6.5 - 9.0 and 6.5 - 8.5 for aquatic life (Chin, 2000). Our results revealed that, the
canal water were always on the alkaline side (pH > 7). However, the seasonal variations in pH were mainly
affected by temperature, carbonate and bicarbonate system, rather than the photosynthetic activity of the
primary procedures (Ezz El-Din, 1990 and Abdo, 2005). Electrical conductivity measure of the ability of
aqueous solution to carry electric current, solutions of most inorganic compounds and more abundant ions have
higher conductivity (APHA, 1995). The highest EC value of Ismailia Canal was recorded at station 16 in winter
3436
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
(756 mS/cm), while the lowest value at station 2 in summer (327 mS/cm). Dissolved oxygen is a very important
factor to the aquatic organisms, because it affects their biological processes, respiration of animal and oxidation
of the organic matter in water and sediments. In this latter process, complex organic substances are converted to
simple dissolved inorganic salts which could be utilized by the micro - and macrophyte (Okbah and Tayel,
1999). The present study showed that, Ismailia Canal water was oxygenated during all seasons, the highest
values were recorded in both winter (9.7 mg/l) due to the decrease in water temperature, and spring (9.3 mg/l)
which corresponding to the flourishing of phytoplankton (Anon, 2007).
Phytoplankton abundance and structure:
A total of 126 species were identified during the present study (Table 1), the phytoplankton species
belonged to 7 main classes, Chlorophyceae (51 taxa), Bacillariophyceae (34 taxa), Cyanophyceae (25 taxa),
Dinophyceae (6 taxa), Cryptophyceae (5 taxa), Chrysophyceae (3 taxa) and Euglenophyceae (2 taxa). The
phytoplankton community structure was dominated by diatoms, followed by Chlorophyceae then
Cyanophyceae, constituting about 76.3, 16.5 and 6.5% of the total count, respectively. While the other classes
were appeared as a rare, forming about 0.7 % of the total count (Fig.2). Abd El-Karim (1999) and Abou ElKheir et al. (2000), indicated that, Bacillariophyceae occupied the first predominant position followed by
Chlorophyceae, Cyanophyceae, Euglenophceae and Dinophyceae, while Ibrahim (1978) investigated the effect
of some industrial pollutants on phytoplankton in different areas of River Nile and mentioned that
Bacillariophyceae were the most dominant group followed by Cyanophyceae and Chlorophyceae. Also, AbdelHamid (1991) studied phytoplankton abundance and species composition in River Nile and reported that,
phytoplankton classes were arranged as follows: Bacillariophyceae > Cyanophyceae > Chlorophyceae.
Chrysophyceae
100%
Euglenophyceae
80%
Cryptophyceae
60%
Dinophyceae
Chlorophyceae
40%
Cyanophyceae
20%
Bacillariophyceae
0%
Winter
Spring
Summer
Autumn
Fig. 2: Percentage of different phytoplankton density during the study period.
The highest population density was recorded in spring (828 x 104 cells/l), with a maximum density of 1450
x 104 cells/l at station 7 (Fig. 3), while the lowest crop was observed during autumn (506 x 104 cells/l) with a
minimum value of (110 x 104 cells/l) at station 12. This result coincides with nitrate concentration that reached
minimum in autumn (45.68 µg/l). Statistical analysis shows a positive correlation between nitrate and
phytoplankton abundance, this agrees with Nassar and Shams El-Din (2006). The phytoplankton structure
revealed a highest species number (63 spp.) at station 13, decreased to 45 spp. at station 4, and irregularly
distributed along Ismailia Canal.
Abou El- Kheir et al. (2000), clarified that, discharge of industrial effluents (especially untreated ones) have
a great effect on the diversity of the algal population along Ismailia Canal. Shehata and Bader (1985) discussed
the effect of physico- chemical parameters on phytoplankton density along the Nile at Cairo and observed that
diatoms were the most dominant group, constituting 42% - 96% of total phytoplankton community during the
investigated period.
Cluster analysis of phytoplankton count revealed three main groups. The highest similarity percent of
78.3% was recorded within group 1 (station 5 and 7), followed by group 2 (stations 8 and 10), where
represented by 75.7%. While the lowest similarity of 40.8% was recorded at station 12 and 16 (Fig. 4).
3437
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
No. of cell x 10 l
4 -1
900
800
700
600
500
400
Winter
Spring
Summer
Autumn
Fig. 3: Seasonal average of the total phytoplankton density.
Fig. 4: Cluster analysis of the studied stations according to phytoplankton data.
Diatoms, which were the predominant class during the year, flourished in winter constituting about 85.9%
and decreased to about 62.2% from the total population in spring. On contrary, Chlorophyceae ratio was
maximized in spring and minimized in winter forming about 26 and 9.5%, respectively. These results agree with
Sobhy (1999) who mentioned that diatoms contributed about 55.4% while green algae constituted 25% of the
total phytoplankton crop at River Nile.
Bacillariophyceae were represented by 34 species, dominated mainly by Cyclotella meneghiniana,
Cyclotella ocellata, Melosira granulate and Syndra ulna, which constituting 85.8% by the total density of
diatoms during the present survey. Abd El-Karim (1999) showed that, the most prevailing Bacillariophyceae
were Cyclotella meneghiniana, Cyclotella ocellata, Melosira granulate and Syndra ulna. Green algae (51 taxa)
dominated by Actinastrum hantzchii, Pediastrum simplex, Scenedesmus acuminatus, Scenedesmus ecornis,
Scenedesmus quadricuda and Staurastrum paradoxium that formed 44.4% from its density. Amin, (2007) stated
that Scenedesmus quadricuda and Actinastrum hantzchii were the most dominant species in Ismailia Lake.
While blue green algae were dominated by 5 species from the total of 25 taxa (Aphanocapsa elachista
ver.conferta, Lyngbya limnetica, Merismopedia punctata, Microcystis aeruginosa and Phormidium interruptum)
constituted about 64.8% from the total density of blue green algae and correlated with total phytoplankton by
(r=0.44).
Table 1: Phytoplankton species recorded in Ismailia Canal and its seasonal appearance during 2011.
Sampling Stations
1
2
3
4
5
6
7
8
9
List of Species
Bacillariophyceae
Achnanthes minutissima Kutz.
Amphora normani (Raben-horst).
.
.
..
.
...
..
...
Amphora ovalis Kutz.
...
.
..
..
..
..
.
..
Cocconeis placentula (Ehrenberg)
Cyclotella glomerata (Bachmann)
.
..
.
.
.
.
.
.
Cyclotella kuetzingiana Kutz.
..
...
..
..
..
..
...
.... .
Cyclotella meneghiniana Kutz.
..
Cyclotella ocellata Pant.
....
...
...
..
...
...
...
.... ...
Cyclotella operculata Pant.
....
.... .... .... .... .... .... .... ....
Cymbella cistula Grun.
...
...
...
.... ..
.... ...
..
....
10
11
12
..
..
..
.
.
.
.
..
.
....
....
..
....
....
..
...
..
.
....
....
.
13
14
15
16
.
.
.
.
.
.
..
.
..
.
.
.
.
.
.
.
..
....
....
..
...
....
..
...
....
..
...
....
3438
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Cymbella sp. Grun.
Cymbella microcephala Grun.
Diatoma hiemale (W . Smith)
Flagilaria construens var. venete (Ehr.)
Grun
Gomphonema herculeana (W . Smith)
Gyrosigma scalproides (W . Smith)
Melosira distans (Her.) Ralfs
Melosira granulata (Her.) Ralfs
Melosira italica (Her.) Ralfs
Meridion circulare (W . Smith)
Navicula creptocephala Weber
Navicula dicephala (Gregory)
Navicula pusilla Weber
Nitzschia acicularis W. Smith
Nitzschia amphibia (Kutz.)Grun.
Nitzschia fonticola (Kutz.)W. Smith
Nitzschia frustulum (Kutz.)Grun.
Nitzschia lorenziana W. Smith
Nitzschia palea (Kutz.)W. Smith
Pleurosigma deliculatum W. Smith
Syndra actinstroides Kutz.
Syndra afflinis Kutz.
Syndra ulna (Nitzsch) Her.
Syndra ulna (Nitzsch) Her.
Cyanophyceae
Aphanocapsa elachista ver.conferta
(Wittrock)
Aphanocapsa grevillei (Hansg.)
Chroococcus cohaerens (Breb.) Nag.
Chroococcus
dispersus
(Keissier)
Lemmermann
Chroococcus turgidus (Breb.) Nag.
Coelosphaerium kuetzingianum Nag.
Crucigenia quadrata(Lemmer.)
Crucigenia rectengularis (Lemmer.)
Crucigenia tetrapedia (Lemmer.)
Eucapsis minuta (F.E.Fritsch)
Gelocapsa minima (Lemmer.)
Gomphospharium kuetzingianum (Nag.)
Gomphospharium
lacustris
var.
compacta (Lemmer.)
Lyngbya contorta (Wartm.) Gom.
Lyngbya limnetica Lemmer.
Lyngbya verscolor (Wartm.) Gom.
Merismopedia alegans (Meyen)
Merismopedia punctata (Meyen)
Microcystis aeruginosa Kutz.
Microcystis flos-aquae (Wittr.) Kirchner
Myxosarcina burmensis (Geitler)
Oscillatoria tenuis (Klebahn) Geitler
Phormidium interruptum Kutz.
Phormidium laminosa (Agardh.) Gomont
Chlorophyceae
Actinastrum hantzchii (lagerheim)
Ankistrodesmus convulatus (Corda.)
Ankistrodesmus falcutus (Precott)
Ankistrodesmus fusiformis (Corda.)
Ankistrodesmus nitizschiod G.S.West
Ankistrodesmus spiralis (Corda.)
Asterococcus limneticus (G.M.Smith)
Chlorella vulgaris (Beijerinck)
Closrerium venus (Corda.)
Coelastrum microborum Naegeli
Coelastrum sphericum Naegeli
Cosmarium curtum (Naegeli) Collins
Cosmarium nitidulum (Corda)
Crucigenia quadrata Morren
Dictyosphaerium elegans (Wood)
Dictyosphaerium pulchellum (Wood)
Elkatothrix gelatinosa G. M. Smith
Golonkinia radiata (Corda)
.
.
.
.
.
.
.
.
.
..
.
.
...
...
....
....
....
....
..
.
..
..
..
.
.
...
.
.
.
...
.
.
.
..
...
.
..
..
.
..
..
....
....
.
.
..
.
....
....
....
..
.
...
.
...
...
.
..
.
....
...
..
....
.
....
....
.
....
....
.
..
....
.
...
...
.
.
....
....
...
..
...
.
..
.
.
.
.
....
.
....
..
.
.
.
.
..
.
.
.
..
..
..
..
.
..
...
.
.
..
.
...
.
.
..
...
.
..
..
..
.
.
.
..
..
..
.
.
.
.
...
.
.
...
.
..
.
.
...
.
..
.
.
..
...
.
..
..
..
..
....
.
..
..
....
.
.
..
..
.
.
..
..
....
.
.
..
..
.
....
.
...
.
..
.
.
.
....
.
..
.
.
...
..
..
..
...
..
..
.
..
..
..
..
.
.
.
.
..
.
.
.
..
.
..
..
..
..
.
....
.
..
..
.
..
.
.
.
..
..
..
..
.
...
.
.
...
.
..
..
.
..
.
...
.
.
..
..
.
..
.
..
.
..
..
.
.
...
.
..
.
.
.
.
.
.
.
..
..
..
.
.
.
..
..
.
.
.
.
..
.
.
.
.
.
..
..
.
.
.
.
.
....
.
...
.
...
.
...
..
...
..
.
....
..
.
..
..
...
.
..
.
.
.
.
..
.
..
.
.
.
.
..
.
...
...
...
.
...
..
.
.
...
.
....
.
..
..
..
..
...
..
.
.
.
.
..
...
..
.
.
.
.
..
..
..
..
.
..
.
.
..
.
...
.
..
.
...
..
.
..
...
..
.
...
..
..
...
..
.
..
..
..
.
..
...
.
...
.
..
..
.
.
..
.
.
..
..
.
..
...
..
.
.
..
.
.
.
.
...
...
.
.
..
..
.
.
.
....
..
.
..
...
...
..
.
..
.
.
.
.
..
.
.
.
.
.
.
..
...
.
.
.
..
.
..
..
..
..
.
..
.
.
..
.
.
..
.
.
.
.
..
.
.
.
.
.
..
...
.
.
..
.
.
.
..
..
.
.
...
.
.
...
..
.
.
.
..
.
..
.
.
.
..
..
.
.
.
..
.
.
..
.
..
..
.
.
..
.
.
3439
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Kirchneriella contortum Korshikov
Kirchneriella lunaris Korshikov
..
.
.
.
.
Lagerheimia citriformis (Snow) G. M.
Smith
...
.
..
Lagerheimia genevensis Chodat.
..
.
Micractium Pusillum (Fresenius)
.
Micractium quadrisetum (Fresenius)
..
.
Monoraphidium contortum (Thuret)
Komarkova-Legenerova
..
.
..
.
.
.
...
Monoraphidium tortile KomarkovaLegenerova
Nephrocytium lunatum (Snow) G. M.
Smith
.
Oocystis borgei (Wittrock)
.
Oocystis parva (Wittrock)
.
Oocystis solitaria (Wittrock)
..
.
.
.
.
.
..
Pediastrum boryanum G. M. Smith
.
Pediastrum duplex (Snow)
..
.
..
.
...
..
...
Pediastrum simplex G. M. Smith
.... .
...
...
..
...
Pediastrum simplex var.duodenarium
.
Scenedesmus abundans
(Ehrenberg)
Chodat.
Scenedesmus acuminatus (Hansgirg)
Chodat
..
...
..
..
...
..
..
Scenedesmus bicaudatus (Hansgirg)
Chodat
.
..
..
Scenedesmus bijuga (Hansgirg) Chodat
..
.
.
..
.
.
Scenedesmus dimorphus (Hansgirg)
Chodat
.
..
..
...
...
Scenedesmus ecornis
(Ehrenberg)
Chodat.
...
...
...
..
.... .... ....
Scenedesmus opoliensis (Chodat) Fott &
Komarek
Scenedesmus portuberans G.M Smith
(Chodat.)
.
..
.
.
Scenedesmus quadricuda G.M Smith
(Chodat.)
...
.
..
..
...
..
...
Selenastrum gracile Reinsch
.
..
.
.
.
Selenastrum minutum (Naegeli) Collins.
.
Staurastrum manfeldtii W. West
.
..
Staurastrum paradoxium (Ehrenberg)
...
.... ...
...
..
...
...
Staurastrum planctonicum (Ehrenberg)
..
Tetraedron constricta (Braun)
.
.
Tetraedron minimum (Braun)
..
.
.
..
.
...
Westella
botryoides
(West)
de
Wildemann
.
..
Dinophyceae
Ceratium hirundinella (O. F. Muell.)
Dujardin
.
Gymnodinum colymbeticum (Stein)
Peridinium umbonatum (Woloszynska)
.
.
Peridinium umbonatum Stein.
.
.
.
.
Peridinium umbonatum ver.goslaviense
(Wolosz.)
.
..
.
.
Peridinium umbonatum ver.umbonatum
Stein.
.
Euglenophyceae
Euglena acus (Klebs.)
Trachelomonas planctonica
.
Cryptophyceae
Creptomonas erosa (Ehrenberg)
Creptomonas obavata (Ehrenberg)
.
.
Creptomonas ovalis (Ehrenberg)
.
Creptomonas ovata (Ehrenberg)
Creptomonas rostrata (Ehrenberg)
Chrysophyceae
Mallomonas acaroides (Perty)
.
.
Mallomonas litorresa (Stokea.)
Ochromonas mutabilis (Klebs.)
.
Count spp.
62
60 57 45 60 52 61
spp. recorded in one season (.), two seasons (..), three seasons (...) and four seasons (....).
.
...
.
.
.
.
.
..
...
.
..
.
.
.
.
.
.
...
.
.
..
..
.
..
.
.
.
..
.
..
..
....
..
.
...
...
.
.
.
.
.
.
.
.
..
.
...
..
..
..
..
.
..
..
...
....
.
.
..
.
...
.
....
.
...
.
..
.
..
.
.
.
..
....
...
..
....
..
.
....
...
.
..
....
....
..
..
..
.
.
..
...
....
...
.
.
.
.
.
.
....
.
...
..
.
.
.
..
.
.
...
.
..
.
.
.
.
...
.
..
.
..
...
..
.
.
...
.
...
..
..
.
..
.
..
.
.
.
.
.
.
.
.
..
.
.
..
.
.
.
.
.
.
..
.
.
.
.
.
.
47
.
.
59
50
62
56
63
57
.
.
59
52
3440
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Table 2: Statistical analysis of phytoplankton density in different studying sites of Ismailia Canal.
Phytoplankton statistics
Stations
Total species
Total density
Species richness
4
-1
(Number of spp.)
(No.x10 unit.l )
(Margalef)
1
60
2778
7.441
2
58
2389
7.328
3
55
2881
6.779
4
44
6236
4.921
5
59
3203
7.185
6
51
10317
5.41
7
60
3578
7.21
8
45
5043
5.161
9
58
3220
7.057
10
48
3457
5.768
11
61
1841
7.981
12
55
1992
7.108
13
62
2720
7.713
14
56
2969
6.878
15
57
2301
7.234
16
50
762
7.384
Piolou,s evenness
Diversity
0.6532
0.6231
0.6193
0.4934
0.6042
0.3761
0.7014
0.5609
0.6365
0.6586
0.7661
0.8372
0.6447
0.7135
0.7358
0.8711
2.675
2.53
2.482
1.867
2.463
1.479
2.872
2.135
2.584
2.55
3.149
3.355
3.661
2.872
2.975
3.408
The statistical analysis shows that, phytoplankton richness varied from 4.921 at station 4 to 7.981 at station
11 (Table 2). The species diversity values were increased from 1.479 at station 6 to 3.661 at station 13. Species
evenness fluctuated in limited values between 0.3761 at station 6 and 0.8711 at station 16. Diversity values were
positively correlated with Margalef’s Index (r =0.79) and evenness (r =0.87). Diversity index was employed as
parameter to define the structure of the phytoplankton community in the study area. The high value of diversity
was associated with large number of taxa (57 taxa). The community was shared by several taxa (Nassar and
Shams El-Din, 2006).
Biochemical compositions of phytoplankton:
The biochemical compositions determine the nutritive quality of phytoplankton as natural food grazers such
as zooplankton and fish larvae (Bode et al., 2003; Doroudi et al., 2003; Hofmann et al., 2004 and MartinezFernández et al., 2004). The wide variation in protein content of algae indicates that these differences may be
related to the different sites of collection and the time of algal growth where the differences are in some cases
reflected to the age of the algae in different samples (Wagdy and El-Shaarawy, 1994). The highest
phytoplankton protein content was detected in spring (11.61 g/l) as illustrated in Fig. 5. This concurrently with
pronounced increase in phytoplankton crop (828 x 104 cells/l). The high percentage frequency of diatoms,
Chlorophyceae and blue-green algae (62.2, 26 and 11.1%, respectively) at this season may confirm the high
protein content of these groups. Abdo et al. (2010, b) showed that microalgae have emerged as important
sources of proteins and value added compounds with pharmaceutical and nutritional importance, they stated that
a bout 16 amino acids are produced by cayanobacterial species Anabaena sphaerica and Spirulina platensis
which have the highest concentration and numbers of amino acids in the free form. The crude protein of
Chlorella genus represent 55% to available weight (Grigorova, 2005). The glutamic amino acid is interesting for
human consumption, of which approximately 300.000 ton per annum are produced, methionine, lysine,
tryptophan, aspartic acid and phenylalanine are animal food supplements (Borowitzka, 1988). On the other
hand, the lowest protein content obtained in summer. High water temperature may be one of the main reasons.
This agrees with Oliveria et al. (1999) who mentioned that high water temperature has been related to
significant decrease in protein content. Renaud et al. (2002) added that, the tested diatoms species had
significantly lower percentage of protein when cells were cultured at highest temperature.
Stations 2, 7 and 1 in winter maintained the maximum yield of protein contents (20.37, 20.17 and 19.47 g/l,
respectively), in the same time, the maximum density of phytoplankton were noticed at station 7 (1450 x 104
cells/l). Contrarily, station 10 sustained the minimum protein content (1.0 g/l) as shown in Fig. 8, this may due
to stagnant nature of the station water. During the study, the maximum level of nitrate (120.8 µg/l) was recorded
at station 1 in spring season, this enrichment of total inorganic nitrogen caused elevation in total protein contents
at the same stations. The most credible hypothesis that reported by many authors is the elevation of protein
content with increase of nutrient especially nitrogen, Daume et al. (2003) and Sarthou et al. (2005) assumed that
protein content would be maintained in commercial farms by large scale addition of nitrogen. But, Uriarte et al.
(2006) reported that their starting hypothesis was that elevated nitrogen content in growth medium would result
in a higher protein content of benthic diatom. Several studies found that the high pollution and high
concentration of nutrients affected the standing crop of phytoplankton in Damietta Branch (Abd El-Karim,
1999), Helwan Region of River Nile (Taha et al., 2001) and in Lake Manzala (Sobhy, 2006).
3441
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Total protein contents (g/l)
14
12
10
8
6
4
2
0
Winter
Spring
Summer
Autumn
Total carbohydrate contents (mg/l)
Fig. 5: Seasonal variation in total protein contents (g/l) of phytoplankton at selected stations of Ismailia Canal.
90
80
70
60
50
40
30
20
10
0
Winter
Spring
Summer
Autumn
Fig. 6: Seasonal variation in total carbohydrate contents (mg/l) of phytoplankton at selected stations of Ismailia
Canal.
Total lipid contents ( mg/l)
14
12
10
8
6
4
2
0
Winter
Spring
Summer
Autumn
Fig. 7: Seasonal variation in total lipid contents (mg/l) of phytoplankton at selected stations of Ismailia Canal.
The maximum level of total carbohydrate concentration was found in summer, reaching 82.5 mg/l (Fig. 6),
while the minimum level detected in autumn (6.69 mg/l). Abdo et al. (2010, b) stated that cyanobacteria isolated
from River Nile contain different sugar unit of polysaccharide content which include sugars such as glucose,
galactose, mannose, fructose, xylose, glacturonic acid, sucrose and fucose, it emphasized that Spirulina platensis
have the highest total carbohydrate content. Station 1 had the highest value of carbohydrate (110 mg/l) in
summer (Fig .9), and attained moderate enrichment of total inorganic phosphorus (312 µg/l) which caused
elevation in carbohydrates, Juttner et al. (1996) pointed out that, the highest species richness and standing crop
were found at sites with intermediate levels of nutrient enrichment but the high polluted sites had much lower
abundance. Abd El-Karim and Abd El-Hady (2008) stated that carbohydrates constitute the major part of the
3442
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
biochemical contents of epiphytic microalgae in Lake Bardawil. Brouwer et al. (2003) showed that the diatoms
of Lake Manzala had the ability to produce copious amounts of extracellular polymeric substances (EPS),
mainly consist of carbohydrates. Thus responsible of the input of high-quality organic carbon into the sediment
which used as a food source for the heterotrophic consumer (Hanlon et al., 2006).
25
Total protein contents (g/l)
Winter
Spring
Summer
Autumn
20
15
10
5
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
Stations
Fig. 8: Total protein contents (g/l) of phytoplankton at different stations of Ismailia Canal.
120
Total carbohydrate contents (mg/l)
Winter
Spring
Summer
Autumn
100
80
60
40
20
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
Stations
Fig. 9: Total carbohydrate contents (mg/l) of phytoplankton at different stations of Ismailia Canal.
Total lipid content of phytoplankton reached maximum in summer (Fig. 7) with a value of 12.34 mg/l. In
addition, stations 10 and 11 were approximately equivalent to each other in their high lipid content (15.8 and 16
mg/l) in autumn season (Fig.10), while spring showed the lowest total lipid content. Abdo et al. (2010, b) stated
that cholesterol, campasterol and stigmasterol are produced by all candidate species of cyanobacteria isolated
from River Nile. While, β- sitosterol are the only unsaponifiable fatty acid produced by Spirulina platensis and
Chroococcus turgidus.
The present study shows that protein constitutes the major part of the biochemical contents of the
phytoplankton while lipid constitutes the minor one. Renaud et al. (2002) conducted that the tested microalgal
species had protein as the main chemical component (31.5-64.1% dry weight), with lower amount of lipid (8.021.7% dry weight). Moreover, Volkman and Brown (2005) made a generalized regarding the gross biochemical
composition of microalgae where the organic component is protein (30-40% of total dry weight), followed by
lipid (10-20% of total dry weight) and carbohydrates (5-15% of total dry weight).
3443
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Winter
Spring
Summer
Autumn
16
Total lipid contents (mg/l)
14
12
10
8
6
4
2
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
S tations
Fig. 10: Total lipid contents (mg/l) of phytoplankton at different stations of Ismailia Canal.
Principal component analysis (PCA):
Gabriel Biplot (axes F1 and F2)
0.6
NO2
Trans
DO
Aphanocapsa elachista
0.4
Chlorophyceae
St 2
Cyanophyceae
St 1
Lipids
St 11
St 10
0.2
St 12
ST 3
-- axis F2 -->
Scenedesmus ecornis
St 4
St 14
0
St 13
St 5
Cy clotella ocellata
Total phytoplankton
Proteins
-0.2
Bacillariophyceae
St 9
St 8
St 15
St 16
EC
St 7
NO3
-0.4
St 6
Carbohydrates
Temp
-0.6
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
-- axis F1 -->
:
Fig. 11: Principal component analysis (PCA) between environmental and biological variables in the different
stations of Ismailia Canal. (Temp) Water Temperature, (DO) Dissolved Oxygen, (NO2) Nitrite, (NO3)
Nitrate, (Trans) Transparency and (EC) Electrical Conductivity.
3444
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Component axes F1 and F2 explained 47.82% of the variance (Fig. 11) with the first explaining the bulk of
it (31.49%). Total phytoplankton directly related with Bacillariophyceae, protein and carbohydrate. Total
phytoplankton, Bacillariophyceae and Cyclotella ocellata contained high amount of protein and less amounts of
lipid and carbohydrate. On the other hand, Chlorophyceae have a high amount of lipid in compared with protein
and carbohydrate. Bacillariophyceae inversely proportion with NO2 and turbidity value and can undergo a low
amount of oxygen. Contrary, Chlorophyceae highly dependent on oxygen. Cyanophyceae were highly positively
associated with transparency and NO2 and negatively with EC, NO3 and temperature. The sample score
distribution indicated clear differences among sampling points. According to PCA analysis the studded area can
be divided in to four main groups (St.1, St. 2, St. 3 and St. 4), (St. 10, St. 11, St. 12 and St. 14), (St. 5, St. 6, St.
7, St. 8 and St. 9) and (St. 13, St. 15 and St. 16).
In conclusion, the phytoplankton structure and its biochemical composition are connected with changes in
environmental conditions.
Recommendation:
The study recommended avoiding as far as possible the discharge of different pollutants into the water of
Ismailia Canal, which is considered a main source of drinking water supply for the people of canal cities.
References
Abdel-Hamid, M.I., 1991. Phytoplankton and water quality of the River Nile in Egypt, Ph. D. Thesis, Fac. Sci.,
El-Mansoura Univ., 346.
Abd El-Karim, M.S., 1999. Phytoplankton dynamic and its productivity in Damietta Branch. M.Sc. Thesis, Fac.
Of Girls, Ain Shams University, 202pp.
Abd El-Karim, M.S. and H.H. Abd El-Hady, 2008. Abundance, structure and biochemical composition of
epiphytic microalgae of Cymodocea nodosa and Ruppia cirrhosa in hyper saline Mediterranean Lagoon,
Bardawil Lagoon, Egypt. African J. Biol. Sci., 4(1): 53-66.
Abou El-Kheir, W.S., A. El-Shimy and N. Abdel-Salam, 2000. Seasonal variations in phytoplankton structure in
some industrial polluted areas along Ismailia Canal Egypt. Al-Azhar Bull. of science proceeding of 5 Int.
Sci. Conf. 25-27, March 2000: 225-242.
Abdo, M.H., 1998. Some environmental studies on the River Nile and Ismailia Canal in front of the industrial
area of Shoubra El-Kheima. M. Sc. Thesis, Fac. of Sci., Ain Shams Univ., Cairo, Egypt.
Abdo, M.H., 2005. Physico-chemical characteristics of Abu Za’baal Ponds, Egypt. Egyptian J. of aquatic
research, 31(2): 1- 15.
Abdo, M.H., S.Z. Sabae, B.M. Haroon, B.M. Refaat and A.S. Mohammed, 2010, a. Physico-Chemical
Characteristics, Microbial Assessment And Antibiotic Susceptibility Of Pathogenic Bacteria Of Ismailia
Canal Water, River Nile, Egypt. Journal of American Science; 6(5):234-250]. (ISSN: 1545-1003).
Abdo, S.M., M.H. Hetta, R.A. Salah El Din and G.H. Ali, 2010, b. Growth Evaluation and Bioproduct
Characteristics of Certain Freshwater Algae Isolated from River Nile, Egypt. J. Appl. Sci. Res., 6(6): 642652.
Amin, A.S., 2007. Using of phytoplankton and physicochemical parameters as indicator of pollution in ElTimsah Lake, Ismailia, Egypt. N. Egypt. J. Microbiol. 17, 297-313.
Anon, 2007. Environmental studies on Lake Manzalah, final reporte on Lake Manzalah, Abdel-Satar, A. M.
(eds), freshwater and lake division - National Institute of Oceanography and Fisheries, 103 pp.
APHA (American Public Health Association), 1995. Standard methods for the examination of water and
wastewater, New York, 1193pp.
APHA (American Public Health Association), 1998. Standard methods for the examination of water and
wastewater, 19th ed. American Public Health Association, AWWA. WCPF. Washington D.C., USA,
20005.
Becker, E.W., 1992. Micro-algae for human and animal consumption, pp: 222-256. In M.A. Borowitzka and
L.J. Borowitzka (ed.), Micro-algal biotechnology. Cambridge University Press, Cambridge, United
Kingdom.
Bode, A., M.T. Alvarez-Ossorio, S. Barquero1, J. Lorenzo, A. Louro and M. Varela, 2003. Seasonal variations
in upwelling and in the grazing impact of copepods on phytoplankton off A Corun˜a (Galicia, NW Spain).
Journal of Experimental Marine Biology and Ecology, 297: 85– 105.
Borowitzka, M.A., 1988. Fats, Oils and hydrocarbons. In Borowitzka M.A, Borowitzka L.J. (eds), Micro-algal
Biotechnology. Cambridge Univ. Press, Cambridge: 257-278.
Brouwer, J.F.C., E.M.G.T. de Deckere and L.J. Stal, 2003. Distribution of extracellular carbohydrates in three
interidal mudflats in Western Europe. Estuarine, Coastal and Science, 56: 313-324.
3445
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Campanella, L., F. Cubadda, M.P. Smmartino and A. Saoncella, 2000. An algal biosensor for the monitoring of
water toxicity in estuarine environments. Water Res., 25: 69-76.
Chabrol, E. and A. Castellano, 1961. SPV method for estimation of total serum lipid. J. Lab. Clin. Med., 57:300.
Chessel, D. and S. Dolédec, 1992. ADE Software (Version 3.6). Multivariate Analyses and Graphical Display
for Environmental Data. User’s Manual.
Chin, D.A., 2000. Water-Resources Engineering. Prentice-Hall Inc. Upper Saddle River, New Jersey, pp 585 –
635.
Daume, S., B.M. Long and O. Crouch, 2003. Change in amino acid content of algal feed species (Navicula sp.)
and the effect on groth and survival of juvenile abalone (Haliotis rubra). J. App. Phyco., 15: 201-207.
David, J.H. and P. Hazel, 1993. Analytical Biochemistry. Hand Book, 18 ed. 497p.
De Pauw, N. and G. Persoone, 1992. Micro-algae for aquaculture, P. 197-221. In M.A. Borowitzka and L.J.
Borowitzka (ed.), Micro-algal biotechnology. Cambridge University press, Cambridge United Kingdom.
Desikachary, T.V., 1959. Cyanophyta. First ed. Indian Council of Agricultural Reserch. New Delhi. 686 pp.
Doroudi, M., P. Southgate and J. Lucas, 2003. Variation in clearance and ingestion rates by larvae of the blaklip pearl oyster (Pinctada margaritifera, L.) feed on various microalgae. Aqua. Nut., 9: 11-16.
Dubois, M., K.A. Gilles, J.K. Hmilton, P. A. Repers and F. Smith, 1956. Colorimetric method of sugars and
related substances. Analat. Chem., 18: 350-356.
Ezz El-Din, O., 1990. Some ecological studies on phytoplankton of Lake Bardawil, Ph. D. Thesis, Fac. of Sci.
Suez Canal Univ., Egypt.
Fathi, A.A. and R.J. Flower, 2005. Water quality and phytoplankton communities in Lake Qarun (Egypt).
Aquatic Sci., 67: 350-362.
Field, C.B., M.J. Behrenfeld, J.T. Randerson and P. Falkowski, 2007. Primary production of the biosphere:
integrating terrestrial and oceanic components. Science, 281: 237-240.
Geriesh, M.H., I.Z. El-Shamy and H. Farouk, 1999. Source of Pollution of the Sweet Suez Canal Water, Suez
Canal Province, Egypt; Proc. 4th International Conference of Geochemistry; Alexandria, Egypt. pp. 353–
368.
Geriesh, M.H., D. Stueben and Z. Berner, 2004. Deficiencies of Simple Technologies in Surface Water
Purification: A Case Study of Surface Water Treatment for Drinking Purposes atSuez City, Egypt. The 7th
International Conference of Geology of Arab World (GAW 7); Cairo, Egypt, pp. 429–437.
Geriesh, M.H., K. Balke and A. El-Bayes, 2008. Problems of drinking water treatment along Ismailia Canal
Province, Egypt. J. Zhejiang Univ. Sci. B., 9 (3): 232-242.
Grigorova, S., 2005. Dry biomass of fresh water algae of Chlorella genus in the combined forages for laying
hens. J. central European agriculture, 6(4): 625-630.
Hanlon, A.R.M., B. Belling, K. Haynes, G. Xiao, T.A. Hofmann, M.R. Gretz, A.S. Ball, A.M. Osborn and
G.J.C. Undrewood, 2006. Dynamics of extracellular polymeric substance (EPS) production and loss in an
esturine, diatoms-dominated, microalgal biofilm over a tidal emersion period. Limnology and
Oceanography, 51 (1): 79-93.
Hannford, L.T. and M.E. Britton, 1952. The algae of Illinois. The Univ. of Chicago Press, Chicago, Illinois,
U.S.A. 407 pp.
Herrero, M., L. Jaime, P.J. Martin- Alvarez, A. Cifuentes and E. Ibáñez, 2006. Optimization of the extraction of
antioxidants from Dunaliella salina microalga by pressurized liquids. Journal of agricultural & Food
Chemistry, 54: 5597-5603.
Hofmann, E.E., E.N. Powell, E.A. Bochenek and J. M. Klinch, 2004. A modeling study of the influence of
environment and food supply on survival of Crassostrea gigas larvae. J. Mar. Sci., 61: 596-616.
Httl. H. and J. Gartner, 1988. II Tetrasporales, Chlorococcales, Gloedendales. Subwasserflora Von Mitteleuropa
Herausgegeben Von. H. Ettl. J. Gerloff. H. Hevnig D. Mollenhauer. Band 10. Gustay Fischer. Verlag.
Stuttgart. New. York. 436. pp.
Ibrahim, E.A., 1978. Effect of some pollutants on some fresh water planktonic organisms. Ph. D., Bot. Dep.,
Cairo Univ., 173pp.
Ibrahim, H.S., M.A. Ibrahim and F.A. Samhan, 2009. Distribution and bacterial bioavailability of selected
metals in sediments of Ismailia Canal, Egypt. J. Hazard. Mater. 168, 1012–1016.
Johnson, E.A. and G.H. An, 1991. Astaxanthin from microbial sources. Crit. Rev. Biotechnol., 11: 297-326.
Juttner, I., R. Heike and S.J. Ormerod, 1996. Diatoms as indicators of river quality in Nepalese Middle Hills
with consideration of the effects on habitat-specific sampling. Freshwater Biology, 36:475-486.
Krammer, K. and H. Bertalot, 1991. Bacillariophyceae 3. Tell : Centrales, Fragilariaceae, Eunotiaceae
subwasserflora von. Mitteleuropa. Herausgegeben. Von. H. Ettl. J. Gerloff. H. Heynig D. Mollenhauer.
Band 2/3. Gustay Fischer Verlag. Jena, Stuttgart. 576 pp.
Martinez- Fernández, E., H. Acosta-Salmón and C. Rangel-Dávalos, 2004. Ingestion and digestion of 10 species
of microalgae by winged pearl oyster Pteria sterna (Gould) larvae. Aquacul., 230: 417-423.
3446
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Meendiola, J.A., F.R. Marin, S.F. Hernăndez, B.O. Arredondo, F.J. Señorāns, E. Ibāñez and G. Reglero, 2005.
Characterization via liquid chromatography coupled to diode array detector andtandem mass spectrometry
of supercritical fluidantioxidant extracts of Spirulina platensis microalga. J. Separa. Sci., 28: 1031-1038.
Meizoso, L., S. Jaime, A. Santoyo, G. Cifuentes, F.J. Garcia-Blairsy and J. Señorāns, 2008. Pressurized fluid
extraction of bioactive compounds from Phormidium species Agric. Food Chem., 56: 3517-3523.
Ministry of Water Resources and Irrigation (MWRI), 2002. US Agency for Interna-tional Developments,
Agricultural Policy Reform Program (APRP)-Water Policy Activity, PCE-I-00-96-00002-00, Report No.
64.
Nassar, M.Z. and N.G. Shams El-Din, 2006. Seasonal dynamics of phytoplankton community in the bitter lakes
and Temsah Lake. Egyptian journal of Aquatic Research, 32 (1): 198-219.
Okbah, M.A. and F.T.R. Tayel, 1999. Water quality in the coastal area of Alexandria. Bull. Nat. Inst. of
Oceanogr. & Fish. E.A.E., (25): 89 – 102.
Oliveira, M.A.S., M.P. Monteiro, P.G. Robbs and S.G. leite, 1999. Growth and chemical composition of
Spirulena maxima and Spirulena platensis biomass at different temperatures. Aquacul. Int., 7: 261-275.
Oswald, W.J., 1992. Micro-algae and waste-water treatment, p. 305-328. In M.A. Borowitzka and L.J.
Borowitzka (ed.), Micro-algal biotechnology. Cambridge University press, Cambridge United Kingdom.
Plaza, M., A. Cifuentes and E. Ibāñez, 2008. In the search of new functional compounds. Trends food sci.
Technol., 19: 31-39.
Popovsky, J. and L.A. Pfiester, 1990. Dinophyceae (Dinoflagellitida) subwasserflora von Mitteleuropa.
Herausgegeben von. H. Ettl J. Gerloff. H.Heynig D. Mollenhauer. Band 6 Gustav Fischer Verlag. Jena,
Stuttgart. 272 pp.
Prescott, A.G.W, 1978. How to know the fresh water algae (third edition) 293pp.
Renaud, M.S., T. Luong-Van, G. Lambrinidis and L.D. Parry, 2002. Effect of temperature on the growth,
chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures.
Aquacul., 211: 195-214.
Roslin, S.A., 2003. Seasonal variation in the protein content of marine algae in relation to environmental
parameters in Arockia puram coast. Seaweed Reseach and Utilization, 25: 77-86.
Sarthou, G., K.R. Timmermans, S. Balain and P. Tréguer, 2005. Growth physiology and fate of diatoms in the
ocean: a review. J. Sea Res., 53: 25-42.
Shehata, S.A. and S.A. Bader, 1985. Effect of Nile River water quality on algal distribution at Cairo, Egypt.
Environ. Int., 11(5): 465-474.
Siliem, T.A.E., 1995. Primary productivity of the Nile in barrage area. Menofiya J. Agric. Res. 20 (4): 16871701.
Singh, S., B.N. Kate and U.C. Banerjee, 2005. Bioactive compounds from cyanobacteria and microalgae: an
overview, Critical Reviews in Biotechnology, 25(3): 73-95.
Sobhy, E.H.M., 1999. Effects of industrial waste of Iron and Steel Factories on Nile phytoplankton communities
and productivity at Helwan. M.Sc., Fac. Sci., men. Univ., 231pp. advection.
Sobhy, E.H.M., 2006. Distribution of phytoplankton and epipelic microalgal. Communities of Lake Manzala,
Ph. D. Thesis, Dept. of Botany, Fac. Of Girls. Ain-Shams University, Egypt, 268pp.
Starmach, K., 1974. Flora Slodkowodna Polski. Tom 4. Creptophyceae Dinophyceae Raphidophyceae. Krakow
519pp.
Taha, O.E., M.A. Afifi and E.H.M. Sobhy, 2001. Physico-chemical properties and phytoplankton composition
of the River Nile at Helwan area, Egypt. J. Egypt. Acad. Soc. Environ. Develop., (D-Environmental
Studies), 2(4): 1-29.
Tarek, S.J. and O. A Ali, 2007. The effect of industrial waste of oil companies on the distribution of organic
pollution in Ismailia Canal water. Bull. National Research Center, Egypt, 32(6): 647-659.
Tikkanen, T., 1986. Kasviplanktonopas. Helsinki. 278 pp.
Tredici, M.R. and R. Materassi, 1992. From open ponds to vertical alveolar panels- the Italian experience in the
development of reactors for the mass cultivation of phototrophic microorganisms. J. appl. Phycol., 4: 221231.
Uriarte, I., R. Roberts and A. Farias, 2006. The effect of nitrate supplementation on the biochemical coposition
of benthic diatoms and the growth and survival of post-larval abalone. Aquacul, 261: 423-429.
Volkman, J.K., and M.R. Brown, 2005. Nutritional value of microalgae and applications. In: Algal Clutures,
Analogues of Blooms and Applications. Subba Rao DV (Ed). Science Publishers, Plymouth, UK, pp 407457.
Wagdy, M.E. and G. El-Shaarawy, 1994. Chemical composition of some marine algae from the Mediterranean
sea of Alexandria, Egypt. The Bulletin of the H.I.P.H. xxxiv, 3: 523-534.
Wilde, E.W. and J.R. Benemann, 1993. Biotechnology Advances. 11: 781-812.
3447
J. Appl. Sci. Res., 8(7): 3433-3447, 2012
Youssef, M., G.E. El-Taweel, M. El-Naggar, S.E. El-Hawary, M.A. El-Meleigy and S.A. Ahmed, 2010.
Hydrocarbon degrading bacteria as indicator of petroleum pollution in Ismailia Canal, Egypt. Worled
Applied Sciences. Journal, 8(10): 1226-1233.