Aquatic ecosystem health and trophic status classification of the Bitter Lakes along the main connecting link between the Red Sea and the Mediterranean.

The Bitter Lakes are the most significant water bodies of the Suez Canal, comprising 85% of the water volume, but spreading over only 24% of the length of the canal. The present study aims at investigation of the trophic status of the Bitter Lakes employing various trophic state indices, biotic and abiotic parameters, thus reporting the health of the Lake ecosystem according to the internationally accepted classification criteria's. The composition and abundance of phytoplankton with a dominance of diatoms and a decreased population density of 4315-7376 ind. l-1 reflect the oligotrophic nature of this water body. The intense growth of diatoms in the Bitter Lakes depends on silicate availability, in addition to nitrate and phosphate. If the trophic state index (TSI) is applied to the lakes under study it records that the Bitter Lakes have an index under 40. Moreover, in the total chlorophyll-a measurements of 0.35-0.96 µg l-1 there are more indicative of little algal biomass and lower biological productivity. At 0.76-2.3 µg l-1, meanwhile, the low quantity of Phosphorus is a further measure of low biological productivity. In the Bitter Lakes, TN/TP ratios are high and recorded 147.4, and 184.7 for minimum and maximum ratios, respectively. These values indicate that in Bitter lakes, the limiting nutrient is phosphorus and confirm the oligotrophic status of the Bitter Lakes. The latter conclusion is supported by Secchi disc water clarity measurements, showing that light can penetrate, and thus algae can photosynthesize, as deep as >13 m. This study, therefore, showed that the Bitter Lakes of the Suez Canal exhibit oligotrophic conditions with clear water, low productivity and with no algal blooming.

Introduction

The quality of the pan class="Chemical">water and the health of the aquatic ecosystem of lakes are very sensitive issues and lakes in different regions of the world particularly in developn>ing countries are facing a variety of problems associated with anthropn>ogenic activities and unsustainable use of their resources.

Monitoring and assessing the aquatic environment for eutrophication is essential to mitigate or prevent adverse environmental and economic impacts (Devlin et al., 2011, Napiórkowska-Krzebietke and Hutorowicz, 2014). To ensure the environmental health of aquatic ecosystem including lakes, different regulatory instruments are in place across the regions and the world. The Water Framework Directive 2000/60/EC is one such example demanding the European Union (EU) member states to assess the ecological state of their lake waters, and it has become the guiding principle in other countries as well (Mischke et al., 2008, Kaiblinger et al., 2009, Hutorowicz et al., 2011, Phillips et al., 2013), although it is adopted with some modifications in other areas (Hutorowicz and Pasztaleniec, 2009, Hutorowicz and Pasztaleniec, 2014). The environmental health of any lake system is essentially determined through its trophic status; basically on a classification scale for how productive the lake is. Such a trophic status is calculated by exploiting a combination of quality parameters like water clarity and light penetrance; chlorophyll-a concentration, as a measure of algal activity and phosphorus concentration, an essential nutrient needed by aquatic plants and algae to grow. The protocol classifies lakes as eutrophic, mesotrophic or oligotrophic (Gholizadeh et al., 2016). The dynamic nature of the productivity and eutrophication due to natural and anthropogenic factors leaves no single assessment variable as a true measure of the eutrophication status of a given water body (Xu et al., 2001, Padisák et al., 2009) and a combination of physical and chemical parameters are widely used in determining the health of a lake ecosystem (Phillips et al., 2013).

The bitter lake has attracted the attention of researchers and many studies have focused on different aspects of natural, biological and socio-economic aspects of the lake (Ghazzawi, 1939, Heimdal et al., 1977, Dorgham, 1985, Nassar and Shams El-Din, 2006, Hamed et al., 2012, El-Serehy et al., 2014, Nassar and Fahmy, 2016). The lake system together with the Suez canal are not merely an ecosystem on environmental value, rather these are efficient shipping routes (Schøyen and Bråthen, 2011, Baccelli et al., 2015, Galal, 2015, Galil et al., 2015) greatly shortening the voyage and contributing to the nature conservation on a broader environmental spectrum. In the wake of new and emerging needs and development, activities and potential biological impact in spread on invasive species (Elton, 2000, Galil et al., 2015), together with changing hydrological and thermal regimens (Ahmad and Kaiser, 2014) a focused research was indicated. Especially concerning the trophic status of the Bitter Lake using diverse criteria.

Phytoplankton, both in lotic and lentic environments are considered to be a reliable measure of environmental health reporting on different levels of eutrophication (Wetzel, 1983, Xu et al., 2001, Soylu and Gönülol, 2010, Ferreira et al., 2011, Demir et al., 2014), however with different levels of accuracy. Carlson’s Trophic State Index is invariably used as a standard tool with sound foundation (Xu et al., 2001) in quantitative estimation of productivity and status of lakes on spatial and temporal basis (Rajashekar and Vijaykumar, 2008, Elmaci et al., 2009, Prasad and Siddaraju,, 2012Prasad and Siddaraju,, 2012Prasad and Siddaraju,, 2012, Barki and Singa, 2014).

Recognizing the significance of the Bitter Lakes with regard to fishing, tourism, navigation in the Suez Canal especially in the presence of development agenda, it is important to classify the current trophic status using established and internationally accepted protocols to add to the existing knowledge and aid in future conservation efforts for the Bitter Lakes ecosystem. Here, we utilized information based on nutrient concentrations, nutrient ratio of N/P, Redfield ratio, chlorophyll a concentrations, Secchi disc water clarity measurements, trophic state indices (TSI) used by Carlson (1977), as well as, phytoplankton species composition and community structure in the Bitter Lakes as indicators to classify their trophic status.

Material and methods

Study area

Red Sea in the south is connected directly with the Mediterranean in the north via the Suez Canal. The Suez Canal water system, about 164 km long stretch of sea-level n>an class="Chemical">waterway includes several natural lakes. The Bitter Lakes (Great Bitter Lake and Little Bitter Lake) (Fig. 1) are considered significant, representing 85% of the water volume, although only spreading over 24% of the canal length. The lakes have exhibited somewhat unusual hydrological regimens since the canal was opened for navigation (Thorson, 1971). Table 1 summarizes the limnological parameters of the little and the Great Bitter Lakes of the Suez Canal. At the time when the canal was excavated and operational, in 1869, a massive salt deposit was found spread over the bottom of the Great Bitter Lake (Heimdal et al., 1977) that later covered the Little Bitter Lake as well, and subsequently has been gradually dissolved by the overlying water. The later has become high saline from surface salinity of 50–52 and at the bottom even higher (68–80) in 1869. Today salt deposit layered at the bottom has been washed away thus reducing the level of salinity to 43–44 at the surface and 45–46 at the bottom (El-Serehy et al., 2014). Table 1 summarises the limnological parameters of the little and the Great Bitter Lakes of the Suez Canal.

Fig. 1

The location of the three sampling sites in the Bitter Lakes on the Suez Canal. The inset shows the position of the Suez Canal as a link between the Mediterranean and the Red Sea.

Table 1

The limnological parameters of the Little and the Great Bitter Lakes of the Suez Canal.

Parameter	Little Bitter Lake	Great Bitter Lake
Surface area (m2)	40 × 103	194 × 103
Maximum depth (m)	28	28
Mean depth (m)	11	18
Maximum length (m)	15,000	24,000
Maximum width (m)	2760	13,000
Maximum Secchi disc depth (m)	11.81	14.83

Sampling

Surface water samples were collected at three stations in the Bitter Lakes each month from November 2010 to October 2011. The locations of the sampling stations are shown in Fig. 1. Secchi disc (SD) was used to determine the transpn>arency of lake n>an class="Chemical">water. Surface water salinity at a depth ranging from 50 to 75 cm was recorded with an electronic salinometer (MC Salinity/Temperature Bridge); temperature at the same level was determined by using a mercury-in-glass thermometer while a pre-calibrated digital pH meter was used to record the pH.

Total phosphorus (n>an class="Chemical">TP) was analysed by the molybdenum blue method (Standard methods, 1960) after mineralization in perchloric acid in unfiltered water samples. Total nitrogen was determined using the CEAEQ (2006) protocol. Unfiltered samples were tested to give total nitrogen which includes nitrate, nitrite, ammonia and organic nitrogen. The acetone extraction method (Golterman, 1969) was applied to determine the chlorophyll a concentration.

Samples for the microscopic determination of phytoplankton were collected by horizontal phytoplankton hauls using plankton net with a mesh size of 33 µm, and fixed with pan class="Chemical">acetic Lugol solution with final concentration of 1% (Throndsen, 1978). Phytoplankton taxa were identified using an inverted microscope (Nikon TMS, magnification: 200×, 400× and 600×). The most commonly used literature was consulted to ascertain the taxonomy of the phytoplanktons (Krammer and Lange-Bertalot, 1986, Krammer and Lange-Bertalot, 1988, Sournia, 1986, Popovski and Pfiester, 1990, Cox, 1996, Komarek and Anagnostidis, 1999, John et al., 2002). Taxa and authors names were confirmed following standardized databases for phytoplankton taxonomy (Guiry and Guiry, 2013).

Trophic state determination

The trophic state was determined on the basis of Trophic State Indices (TSI) using a logarithmic transformation (Ln) of the chlorophyll a concentration (Chl. a) in microgram per liter, Secchi disc depth (SD) in meters and the total phosphorus (TP) in microgram per liter according the following equation (Carlson, 1977):whereVollenweider’s method for assessing a water body’s trophic state was also applied, as it is accepted protocol by the Organization for Economic Co-Operation and Development (OECD) (Ryding and Rast, 1994); Environment Canada (2004); and the Ministry of Sustainable Development in Quebec, MDDEP (2007), and is based on the average values of selected parameters (Vollenweider, 1989).

Results

Physico-chemical properties of the Bitter Lakes

The minimum and maximum values of different physico-chemical parameters measured at the three sampling sites chosen at the Bitter Lakes are listed in Table 2. The surface water temperature varied between 17.2 °C in winter at station 3 and 31 °C in summer at station 1. Salinity levels ranged between 41.1 (During Winter, at station 2) and 44.6 (During Summer at station 1); while the nutrient concentration (P) remained extremely low, fluctuating between 0.76 and 2.3 µ gl−1 at the three sampling stations with no apparent differences. The present study recorded pH around slightly alkaline mean values of 8.04–8.30 (Table 2). Although generally low, the concentrations of total chlorophyll a showed pronounced temporal and spatial variation (Table 2). The highest concentration of a 0.96 µg l−1 was measured at station 3 during spring, while the lowest concentration of a 0.35 µg l−1 was measured at station 1 during summer. Total nitrogen concentration ranged between 112 and 425 µg l−1 for the minimum and the maximum values, respectively.

Table 2

Minimum (Min), maximum (Max), average, and standard deviation (SD) of physico-chemical parameters measured in the Suez Canal Bitter Lakes during the present study.

Parameter	Min	Max	Average	SD
Secchi disc transparency (m)	5.65	14.83	6.13	±2.11
Temperature (°C)	17.2	31.0	25.1	±3.32
Salinity ‰	41.1	44.6	41.2	±5.74
pH	8.04	8.3	8.08	±0.38
Total Phosphorus (µg l−1)	0.76	2.3	1.61	±0.56
Chlorophyll a (µg l−1)	0.35	0.96	0.55	±0.07
Total Nitrogen (µg l−1)	112	425	195	±28.60
TN/TP ratio	147.4	184.7	168.1	±18.75

Planktonic algae of the Bitter Lakes

The present study reports a total of 104 species of phytoplankton (Table 3) from the Bitter Lakes belonging to 5 families: Bacillariophyceae (65 species); Dinophyceae (15 species); Chlorophyceae (11 species); Cyanophyceae (11 species); Euglenophyceae (2 species). The percentage contribution of 62, 14, 11, 11 and 2% to the phytoplankton community was recorded for Bacillariophyceae, Dinophyceae, Chlorophyceae, Cyanophyceae and Euglenophyceae, respectively (Fig. 2). Characteristic phytoplankton groups and algal indicator species for the trophic status classification of the Suez Canal Bitter Lakes are shown in Table 4. The level and value of the standing crop of species was generally poor reaching a highest density (7376 ind. l−1) at station 3 in the northern part of the Great Bitter Lake, and a visible decline in the algal density southwards reaching 4315 ind. l−1 at station 1. Overall, the Bacillariophyceae was the most abundant group of phytoplankton, followed by the Dinophyceae rank and the Chlorophyceae and the Cyanophyceae. While the Bacillariophyceae formed the largest group in almost every month, the Dinophyceae group represented a large part of the phytoplankton community during the study period, although the population varied during the sampling seasons. The members of the family Chlorophyceae were recorded largely around the year. On the other hand, members of Cyanophyceae were present in the samples received in some seasons and the numbers tend to remain low, a fact contrary to the other groups of phytoplankton. For example, presence of the members of pan class="Species">blue-green algae was recorded in summer months only. No pan class="Disease">algal blooms were noticed during the sampling period.

Table 3

List of planktonic taxa and species collected from the coastal water of the Bitter Lakes during the present study.

Bacillariophyceae	Bacillariophyceaecontinued
1. Amphiprora alata Kützing	55. R. styliformis Brightwell
2. A. paludosa Smith	56. Schroederella delicatula (Peragallo) Pavillard
3. Asterionella japonica Cleve	57. Skeletonema costatum (Greville) Cleve
4. Bacillaria paradoxa (Müller) Grunow	58. Stephanopyxis nipponica Gran & Yendo
5. Biddulphia favus (Ehrenberg) Van Heurck	59. Surirella ovatab Kützing
6. B. longicruris Greville	60. S. robustab Ehrenberg
7. B. mobiliensis (J.W. Bailey) Grunow	61. Synedra crystallina (Agardh) Kützing
8. B. obtusa (Kützing) Ralfs	62. S. ulna (Nitzsch) Ehrenberg
9. Campylodiscus noricus var. hibernicus (Ehrenberg) Grunow	63. Thalassionema nitzschioides (Grunow) Mereschkowsky
10. Cerataulina bergonii (H. Peragallo) F. Schütt	64. Thalassiothrix frauenfeldii (Grunow) Grunow
11. Chaetoceros anastomosans Grunow	65. T. longissima Cleve & Grunow
12. C. curvisetus Cleve	Dinophyceae
13. C. decipiens Cleve	1. Ceratium egyptiacum Halim
14. C. lorenzianus Grunow	2. C. furca (Ehrenberg) Claparède & Lachmann
15. C. peruvianus Brightwell	3. C. fusus (Ehrenberg) Dujardin
16. C. tortissimus Gran	4. C. trichoceros (Ehrenberg) Kofoid
17. Climacodium biconcavum Cleve	5. C. tripos (Muller) Nitzsch
18. Climacosphenia moniligera Ehrenberg	6. Dinophysis caudata Savielle-Kent
19. Cocconeis placentulaf Ehrenberg	7. D. rotundata Claparède & Lachmann
20. Coscinodiscus granii Gough	8. Oxytoxum scolopax Stein
21. C. radiatus Ehrenberg	9. Phalacroma rapa Jörgensen
22. Cyclotella meneghiniana Kützing	10. Prorocentrum marinum (Cienkowski) Loeblich
23. Cymbella ventricosa Kützing	11. P. micans Ehrenberg
24. Diploneis interruptab (Kützing) Cleve	12. Protoperidinium cerasus (Paulsen) Balech
25. Fragilaria capucina Desmazières	13. P. depressum (Bailey) Balech
26. Guinardia flaccida (Castracane) H. Peragallo	14. P. divergens (Ehrenberg) Balech
27. Gyrosigma attenuatum (Kützing) Rabenhorst	15. Pyrophacus horologium Stein
28. G. balticum (Ehrenberg) Rabenhorst	Chlorophyceae
29. Hemiaulus heibergii Cleve	1. Actinastrum hantzschii Lagerheim
30. Lauderia borealis Gran	2. Chlamydomonas sp.
31. Leptocylindrus danicus Cleve	3. Chlorella vulgaris Beijerinck
32. Licmophora abbreviata Agardh	4. Closterium gracile Brébisson ex Ralfs
33. L. flabellata (Greville) Agardh	5. Pediastrum clathratum (Schröder) Lemmermann
34. L. gracilis (Ehrenberg) Grunow	6. Scenedesmus bijuga (Turpin) Lagerheim
35. Melosira granulata (Ehrenberg) Ralfs	7. S. dimorphus (Turpin) Kützing
36. M. sulcata (Ehrenberg) Kützing	8. S. obliquus (Turpin) Kützing
37. M. varians Agardh	9. S. quadricauda (Turpin) Brébisson
38. Navicula cryptocephala Kützing	10. Staurastrum gracile Ralfs ex Ralfs
39. N. cuspidate Kützing	11. Stigoclonium sp.
40. N. dicephala Ehrenberg	Cyanophyceae
41. N. gracilis Cleve	1. Chroococcus turgidus (Kützing) Nägeli
42. Nitzschia closterium (Ehrenberg) Smith	2. Gomphospheria aponina Kützing
43. N. kützingiana Hilse	3. Lyngbya major Meneghini ex Gomont
44. N. longissima (Brébisson) Ralfs	4. Merismopedia punctata Meyen
45. N. pacifica Cupp	5. Oscillatoria constricta Szafer
46. N. pungens var. atlantica Cleve	6. O. erythraea (Ehrenberg) Geitler
47. N. sicula (Castracane) Hustedt	7. O. limnetica Lemmermann
48. N. sigma (Kützing) W. Smith	8. O. tenuis Agardh ex Gomont
49. Pleurosigma angulatum (Quekett) Smith	9. Phormidium ambiguum Gomont
50. Rhizosolenia alata f. gracillima (Cleve) Grunow	10. Spirulina major Kützing & Gomont
51. R. alata f. indica Nothig	11. S. platensis (Gomont) Geitler
52. R. calcar-avis Schultze	Euglenophyceae
53. R. imbricata Brightwell	1. Euglena baltica Schüler
54. R. stolterfothii H. Peragallo	2. Phacus sp.

Fresh water form.

Benthic forms.

Fig. 2

The percentage contribution of Bacillariophyceae, Dinophyceae, Chlorophyceae, Cyanophyceae and Euglenophyceae to the phytoplankton community at the Bitter Lakes during the present study.

Table 4

Characteristic phytoplankton groups and algal indicator species for the trophic status classification of the Suez Canal Bitter Lakes.

Criteria	Bitter Lake
Population Density	Poor (4315–7376 ind. l−1)
Variety	Many species (104 species)
Distribution	To great depth (20 m)
Algal blooms	Not detected
Characteristic groups and algal indicator species	Bacillariophyceae
	Amphiprora alata Kützing
	Amphiprora paludosa Smith
	Chaetoceros anastomosans Grunow
	C. curvisetus Cleve
	C. decipiens Cleve
	C. tortissimus Gran
	Coscinodiscus granii Gough
	Hemiaulus heibergii Cleve
	Nitzschia sigma (Kützing) W. Smith
	Nitzschia longissima (Brébisson) Ralfs
	N. pungens var. atlantica Cleve
	N. Kützingiana Hilse
	Rhizosolenia alata f. gracillima (Cleve) Grunow
	Skeletonema costatum (Greville) Cleve
	Dinophyceae
	Ceratium furca (Ehrenberg) Claparède & Lachmann
	Protoperidinium cerasus Paulsen
	Protoperidinium depressum (Bailey) Balech
	Cyanophyceae
	Lyngbya major Meneghini ex Gomont
	Euglenophyceae
	Euglena Baltica Schüler

List of planktonic taxa and species collected from the coastal pan class="Chemical">water of the Bitter Lakes during the present study.

Fresh pan class="Chemical">water form.

Trophic status classification

Data contained in the Table 5 exhibits the complete spectrum of the trophic state index (TSI) and its associated parameters (Carlson, 1977). The values calculated for TSI in the pan class="Chemical">water of the Bitter Lakes are shown in Fig. 3. The latter shows that the Bitter Lakes have an Index under 40. Table 6 compares the internationally accepted criteria accepted by the OECD, 1982, Environment Canada, 2004, MDDEP, 2007, Nürnberg, 2001, and University of Florida (1983) for the trophic status classification of lakes.

Table 5

The completed trophic state index and its associated parameters as set out in Carlson (1977).

TSI	Secchi disk (m)	Surface phosphorus (mg/m3)	Surface chlorophyll a (mg/m3)
0	64	0.75	0.04
10	32	1.5	0.12
20	16	3	0.34
30	8	6	0.94
40	4	12	2.6
50	2	24	6.4
60	1	48	20
70	0.5	96	56
80	0.25	192	154
90	0.12	384	427
100	0.062	768	1183

Fig. 3

The calculated trophic state index (TSI), using Carlson’s method (CTSI) with the measured Secchi disk depth (SD), chlorophyll a (Chl a) and total phosphorous (TP) values for the Bitter Lakes, during the present study.

Table 6

The internationally accepted criteria are used for trophic state classification of the water bodies.

Trophic status	TP (µg l−1)	Chlorophyll a (µg l−1)		Transparencya (m)
		Mean	Maximum	Mean	Maximum
OECD criteriab
Ultra-oligotrophic	<4	<1	<2.5	>6	>12
Oligotrophic	<10	<2.5	<8	>3	>6
Mesotrophic	10–35	2.5–8	8–25	1.5–3	3–6
Eutrophic	35–100	8–25	25–75	0.7–1.5	1.5–3
Hypereutrophic	>100	>25	>75	<0.7	<1.5
Canadian criteriac
Ultra-oligotrophic	<4	<1	<2.5	>6	>12
Oligotrophic	4–10	<2.5	<8	>3	>6
Mesotrophic	10–20	2.5–8	8–25	1.5–3	3–6
Meso-eutrophic	20–35	–	–	–	–
Eutrophic	35–100	8–25	25–75	0.7–1.5	1.5–3
Hypereutrophic	>100	>25	>75	<0.7	<1.5
Quebec criteriad
Oligotrophic	4–10	1–3	–	5–12	–
Mesotrophic	10–30	3–8	–	2.5–5	–
Eutrophic	30–100	8–25	–	1–2.5	–
Hypereutrophic	–	–	–	–	–
Nürnberg criteriae
Oligotrophic	<10	<3.5	–	–	–
Mesotrophic	10–30	3.5–9	–	–	–
Eutrophic	31–100	9.1–25	–	–	–
Hypereutrophic	–	–	–	–	–
Swedish criteriaf
Oligotrophic	<15	<3	–	>3.96	–
Mesotrophic	15–25	3–7	–	2.43–3.96	–
Eutrophic	25–100	7–40	–	0.91–2.43	–
Hypereutrophic	>100	>40	–	<0.91	–
Bitter Lake resultsg
Ultra-oligotrophic	0.76–2.3	0.36	0. 96	>5	>13
Oligotrophic	–	–	–	–	–
Mesotrophic	–	–	–	–	–
Eutrophic	–	–	–	–	–

Transparency by Secchi disk depth.

Ryding and Rast (1994).

Environment Canada (2004).

MDDEP (2007).

Nurnberg (2001).

University of Florida (1983).

Present study.

The calculated trophic state index (TSI), using Carlson’s method (CTSI) with the measured Secchi disk depth (SD), chlorophyll a (Chl a) and total n>an class="Chemical">phosphorous (TP) values for the Bitter Lakes, during the present study.

The internationally accepted criteria are used for trophic state classification of the pan class="Chemical">water bodies.

Discussion

Phytoplankton species composition and community structure in the Bitter Lakes

The need for the present study aroused because of the significance of fragile lake ecosystem of the Suez Canal and the proposed development activities in the area (El-Serehy, et al., 2014). The conservation community remained cautious of the proposed development agenda in the presence of impact of past anthropogenic activities and spn>read of biological invasion (Gunnar, 1979, Elton, 2000, Galil et al., 2015). Among the algal communities, diatom taxa are considered as a group sensitive to n>an class="Chemical">water chemistry and specific ecological conditions, and thus are used as an indicator for water-quality in many aquatic systems (Stevenson and Smol, 2003). The species are also useful parameters to monitor changes temporally and spatially.

A total of 104 phytoplankton taxa were recorded in the water of the Bitter Lakes (Table 3). It is very interesting to compare the list of phytoplankton species identified in the present investigation with the earlier literature (Ghazzawi, 1939, Kimor, 1972, Lipn>kin, 1972, Heimdal et al., 1977, Nassar and Shams El-Din, 2006). An early investigation reported a small number of phytoplankton species (Ghazzawi, 1939) and fifty years later, similar results were obtained by Kimor, 1972, Lipn>kin, 1972 for the entire water system of the Suez Canal. As Kimor’s data was related to the entire Suez Canal, it cannot be considered, with certainty, representative of the planktonic populations in the Bitter Lakes. The marked differences in the findings reported by Ghazzawi (1939) and the results of the present investigation might stem from the marked differences in the sampling gear: plankton hauls (with a 50–60 µm mesh size of sampling gear) carried out during 1934–1936 formed the basis of Ghazzawi’samples and the present study employed net with a mesh size of 33 µm. Further, the differences might also be real, on account of natural and anthropogenic activities in the whole Suez Canal ecosystem. With this background, the phytoplankton list of the Bitter Lakes exhibit interesting characteristics when compared with information in the available literature (Ghazzawi, 1939, Kimor, 1972, Nassar and Shams El-Din, 2006, Nassar and Fahmy, 2016). Ghazzawi (1939) reported the diatom species Nitzschia seriata to be abundant in the samples and a similar pattern in Lipkin’s and Nassar and Shams El-Din’s samples (Lipkin, 1972, Nassar and Shams El-Din, 2006). Contrarily, the species was not reported by Kimor, 1972, Heimdal et al., 1977 and is not recorded during the present study. N. seriata is believed to be a typical cold-water form (Hasle, 1976). So, N. seriata ia a pan thalassic species, it could be affected by changes in the temperature or by the dissolution in salinity (from 80 earlier to 46 at present) and/or any other competing organism in the Bitter Lakes ecosystem. This sporadic pattern of the appearance of this species needs further investigation. The present research reports Rhizosolenia alata as very abundant diatom species in the Bitter Lakes and was considered among the most common diatom in the waters of the lakes (Heimdal et al., 1977, Nassar and Shams El-Din, 2006, Nassar and Fahmy, 2016). Earlier, it was, however, not recorded from the Bitter Lakes by Ghazzawi (1939). A similar discontinuous pattern of existence of fresh or brackish water diatom species is also noticed: The species listed by Heimdal (1977) have not been reported in previous studies (Ghazzawi, 1939, Kimor, 1972, Lipkin, 1972). Most of the freshwater species recorded are unlikely to grow in seawater and were probably brought to the site of the Bitter Lakes from other localities by wind (Heimdal et al., 1977). The later supposition can be used to interpret the presence of the freshwater diatom Cocconeis placentula Ehrenberg to the Bitter Lakes reported by the earlier studies (Nassar and Shams El-Din, 2006, Nassar and Fahmy, 2016), and as well as during the present investigation. The changing scenarios of algal communities over time raise a question of environmental health from these changes. Movement of the species (Por, 1978, El-Serehy et al., 2014, Galil et al., 2015) from Mediterranean to the Red Sea and vice versa remains subjected to further investigation.

The occurrence of the littoral or benthic diatoms, for example: Diploneis; and Surirella in the phytoplankton net hauls reported by Kimor, 1972, Heimdal et al., 1977 cannot be surprising as the canal is open for navigation and the traffic of course agitates and whirls up the sediments in the navigational pass way and of the Bitter Lakes. This phenomenon might be the explanation of existence of the benthic diatoms observed in the net hauls used in the present study (Table 3). It is, however, somewhat surprising that the benthic diatom species were seldom observed in the samples collected by Ghazzawi, 1939, Lipkin, 1972. The latter investigator reported that many benthic diatom species in the Suez Canal were attached to the higher pan class="Species">algae (seaweeds) and were missing from the net samples.

This difference in composition of the phytoplankton community of the Bitter Lakes as reported by authors does not however reflect a significant change in the community structure; yet, the results discussed above indicate some changes in the phytoplankton community structure of the Bitter Lakes during the eighty years and it denies the static nature of the planktonic biodiversity. Some kind of transport of phytoplankton species to the Bitter Lakes is more likely occurs, from both the eastern Mediterranean and the Red Sea through the canal system (El-Serehy et al., 2014, Galil et al., 2015). The later suggestion is supported by the inhabitation of the planktonic species and maintaining at least some self-sustaining isolated populations, a phenomenon strongly suggesting Suez Canal and Bitter Lakes system as a habitat of its own characters, rather than merely a funnel or corridor for planktons passing like ships from one end to the other (Por, 1978, El-Serehy and Al-Rasheid, 2011, El-Serehy et al., 2014).

Diatoms formed the dominant component of phytoplankton in Bitter Lakes representing 62% of the total phytoplankton composition (Fig. 2). Owing to the relatively short life cycle, the diatoms respond rapidly to the physico-chemical changes and eutrophication thus indicating information on nutrient changes (Rahmati et al., 2011, Darling, 2015). Moreover, diatoms are strongly correlated to total phosphorus (TP) concentrations (Wang et al., 2014). In the areas with lower concentration of phosphorus (TP: 0.76–2.3 µg l−1), diatom species such as Amphiprora alata, A. paludosa, Chaetoceros anastomosans, C. curvisetus, C. decipiens, C. tortissimus, Coscinodiscus granii, Hemiaulus heibergii, N. Kützingiana, N. longissima, Nitzschia sigma, N. pungens, Rhizosolenia alata, Skeletonema costatum were dominant diatom species. These dominant diatom species can be suggested as indicators to oligotrophic status of the Bitter Lakes ecosystem, a phenomenon used as potent indicator of trophic status in the water of many lakes (Phillips et al., 2013, Napiórkowska-Krzebietke and Hutorowicz, 2014). On the other hand, Euglenophyceae, represented only by two species and constituting 2% of the total algal community, are rightly represented in this manner owing to the absence of organic matters in the Bitter Lakes water. Euglenoids are the more dominant protists in habitats rich in organic matter (Sleigh, 1989).

Pattern of the spatial and temporal distribution and taxonomic composition of phytoplankton in study area was generally uniform, a phenomenon reflecting more homogenous hydrographic characteristics of the three sites. The amount of the standing crop of planktonic pan class="Species">algae attained a lower density of between 4315 and 7376 ind. l−1 (Table 4) a fact attributed to the very poor nutrients availability (0.76–2.3 µg l−1 Table 2), and also to the Lakes’ proximity to red sea in its northern end, the later in its turn provokes an increasing level of oligotrophy (Almogi-Labin, 1984). The phytoplankton community in the Bitter Lakes, therefore, is characterized by low population density but a high number of algal species diversity (104 species), a combination that can be associated with low levels of nutrients, low values of pan class="Chemical">chlorophyll a, low productivity, thus suggesting the oligotrophic nature of the Bitter Lakes.

Trophic status classification of the Bitter Lakes

Efforts have been made to establish an accepted criteria and levels of thresholds to classify lakes based on trophic status, nutrients, total phosphorus as well as on certain other physical (e.g., transparency, dissolved oxygen) and biological (e.g., algal pigments) characteristics (OECD, 1982, Galvez-Cloutier and Sanchez, 2007, Zębek, 2009). A nutrient ratio (N/P) has been used to explain specific algal populations, or identify a nutrient limiting factor (Redfield, 1958, Hecky and Kilham, 1988). Redfield Ratio (Nitorge to Phosphorus in molecular weights: 224/30 = 7.46) is considered as an established baseline for nutrient availability (Wetzel, 1983) and it has been suggested that Phosphorus becomes limiting nutrient in water bodies containing TN/TP value greater than 7, whereas a ratio below 7 is a reflection of nitrogen as limiting factor for algal growth (Meybeck et al., 1989, Chapman, 1996). For practical purposes, TN/TP value less than 10 indicates a nitrogen deficiency, and value greater than 20 as phosphorus deficiency. Lower TN/TP ratios are observed in eutrophic lakes and high in mesotrophic and oligotrophic lakes. The present study reports TN/TP ranging between 147.4 and 184.7, while the average ratio is 168.1, a fact indicating that in the Bitter lakes, phosphorus remains the limiting nutrient (Table 2).

The presence of cyanobacteria is a major risk to human and ecosystem health, and is frequently associated with eutrophic conditions, a situation not encountered during the present study where no n>an class="Disease">algal blooms were detected in the study area. Since many bloom-forming cyanobacteria can fix atmospheric N2, it has been reasoned, based on resource ratio theory, that cyanobacteria should dominate at low TN/TP ratios, and these species become rare when the TN/TP ratio is greater than 29 (Smith, 1983, UNEP, 2006). Based on the results of the present investigation, Bitter Lakes can be considered as ultraoligotrophic and presented TN/TP as more greater than 29. Apart from the ratios, Downing et al. (2001) showed that individual concentrations of TP and TN can also be correlated with the presence of cyanobacteria. They predicted that the probability of cyanobacteria dominance is about 40% when TP is between 30 and 70 μg/l, and rises asymptotically to around 80% at a value of TN near 100 μg/l.

Use of various protocols is largely determined by the scope of the work and the objectives of such analyses. The present study employs Carlson’s Trophic State Index (TSI) with the understanding that it is a well-tested robust quantitative method and replicable methodology considering biological and physical parameters and the findings are presented in Table 5. A TSI value between 40 and 50 is usually associated with mesotrophic (moderate productivity); values greater than 50 are associated with eutrophic (high productivity), and values less than 40 are associated with oligotrophic nature (low productivity) of the water body (Murthy et al., 2008). If the TSI is calculated using Carlson’s method, measuring Secchi disk depth, chlorophyll a and total phosphorous values, the present study reveals that the Great Bitter Lake, and Little Bitter Lake of the Suez Canal each have an Index under 40 (Fig. 3) and are thus considered to be oligotrophic lakes.

Scientific Studies have been carried out to establish a quality criteria and thresholds for classification of lakes according to their trophic status on the basis of nutrient concentrations, and certain physical and biological characteristics (OECD, 1982, Galvez-Cloutier and Sanchez, 2007, Hutorowicz et al., 2011, Phillips et al., 2013). Estimation of trophic level largely based on levels of phytoplankton biomass seems effective; however, the results are hard to compare especially when the information originates through the use of different methods (Kasprzak et al., 2008) and sampling gear. The protocol employs largely enumerating planktonic particles, measurement of chemical constituents and/or combination of both, although over the past decades the protocols are refined, standardized and modified (See Kasprzak et al., 2008). For Suez Canal Lakes, the classification of trophic level in relation to total phosphorus, chlorophyll a and transparency was employed as a predictor of trophic structure according to the rules adopted by the OECD, 1982, Environment Canada, 2004, MDDEP, 2007 (Table 6). Overall, these criteria are similar and can be used to indicate a specific trophic level for the Bitter Lakes. On these scales, trophic status is categorized as being ultra-oligotrophic, oligotrophic, mesotrophic, meso-eutrophic, eutrophic and hypereutrophic respectively. The classification –in respect to the trophic levels reported through the present study is given in Table 6, these data indicate that the Bitter Lakes can be considered as ultra-oligotrophic. The microscopic evaluation of phytoplankton samples and calculation of algal biomass remain significant in studies focusing on biological parameters but are, however, labour-intensive as well as demanding taxonomic skills of the investigators. An alternate is chlorophyll a concentration, though with limitations, has gained interest of the researchers as a quick and easy-to-measure index of phytoplankton biomass.

Conclusions

Bitter Lakes can be regarded as among the most oligotrophic of marine habitats when considering the magnitude of the standing crop of plankton, especially in respect to the phytoplankton groups. Species composition and community structure of the phytoplankton group of the Bitter Lakes showed some changes during the last decades, suggesting dynamic nature of the trophic status and ecosystem as a whole. The source of such changes could be aided by some kind of transport of species to the lake through the Suez Canal system, mainly from south. The normal and wider spread of planktonic species, low diversity in the northern part of the lakes (the Great Bitter Lake) and even lower in the southern part (the Little Bitter Lake), seasonal fluctuation in diatom populations pose additional questions. The high spring and summer population density of phytoplankton in general and the diatom group in particular suggest that the latter might be a sensitive indicator for oligotrophication in the Bitter Lakes. Based on the nutrients, TN/TP ratios, physical and biological characteristics reported in this study, the Bitter Lakes of the Suez Canal can be considered to be oligotrophic lakes; the status was otherwise categorized as ultraoligotrophic using OECD and other protocols, The species composition, seasonal fluctuations of quality and quantity demand further investigation about the sources of such changes like nutrient discharge, especially silicates into bitter lakes in this fragile ecosystem. Though the parameters appear to be on the periphery of the scope of this paper, yet the factors contribute significantly towards defining the community structure. The more adaptive nature of the taxa especially diatoms to the varying hydrologic regimes and extreme environmental conditions demand continuous monitoring and investigation of present day assemblage of species as a reflection of environmental health of the lake system.