Copepods play an important functional role in different marine ecosystems (Huys & Boxshall 1991; Schminke 2007; Anufriieva 2015; 2016). Individual species of copepods, representing various trophic levels, are often the key players that determine the structure of trophic webs and the rate of biogenic element cycling. Knowledge of the plankton copepod species structure and the patterns of its dynamics is necessary to understand the functioning of marine ecosystems and to predict their possible changes.
Coastal lakes/lagoons are an important component of the World Ocean. They cover 13% of the coastal areas around the world and significantly affect the productivity of coastal zones, the land-ocean interactions and support large human populations (Mee 1978; Pérez-Ruzafa et al. 2012). Lagoons are characterized by very high diversity, including also salinity. Most lagoons have marine or brackish salinity, only a small number of lagoons on different continents are hypersaline (salinity > 35 PSU) (Por 1972; Post et al. 1983; Orihuela et al. 1991; Lamptey & Armah 2008). The largest of them are the Sivash (The Sea of Azov, area 2560 km2), Laguna Ojo de Liebre (the Pacific coast of Baja California, 850 km2), Bardawil Lagoon (Egypt, 600 km2) and Lagoa de Araruama (the Atlantic coast of Brazil, 220 km2) (Postma 1965; Kjerfve et al. 1996; Abd Ellah & Hussein 2009; Shadrin et al. 2017).
The climatic prerequisite of lagoon salinization and hypersalinity incorporates several geophysical factors (Kjerfve et al. 1996; Shadrin 2017). Hypersalinity of lagoons is a result of arid or semi-arid climatic conditions, and a relatively small drainage basin. The evaporation in a hypersaline lagoon exceeds precipitation, the water influx (sea water and terrestrial runoff) will not compensate for the difference as usually. The energy of coastal sea/ocean waves supplies into the lagoons by filtering the seawater through the sand/gravel barrier and/or seawater flux into the channels connecting the lagoon-to-sea. An important factor for lagoons is the storm winds that sharply raise the sea level – huge waves moving through sand spits and the rising sea level substantially increase the filtration rate into a lagoon, which receives a greater seawater influx (Kjerfve et al. 1996; Shadrin & Anufriieva 2013).
Features of thermal and oxygen regimes in the hypersaline lagoon contribute to their polyextremality (Shadrin 2017). The specific heat capacity decreases as the salinity increases. This leads to faster heating and cooling of hypersaline waters with higher day and lower night temperatures compared to freshwater, brackish or marine lagoons. The range of daily temperature fluctuations in water bodies increases. Thermal conductivity also decreases with increasing salinity, and this leads to stronger spatial gradients of temperature and salinity in the water column of shallow lagoons (Shadrin 2017). Thermal stratification was observed in hypersaline lagoons with a depth below 2 m. Temperature differences in the water column with a depth of 1 m may reach 14°C. The development of floating mats of filamentous algae leads to an increase in the vertical temperature gradient. The solubility of oxygen decreases with increasing water temperature and salinity. The oxygen diffusion coefficient decreases with increasing salinity, which contributes to strong daily fluctuations of oxygen concentration and its spatial gradients in hypersaline waters. Strong fluctuations – from 200% of saturation (daytime) to zero (nighttime) were observed in the lagoons (Shadrin 2017). This contributes to the formation of near-bottom anoxic zones, which are common features of different hypersaline lagoons/coastal lakes (Shadrin & Anufriieva 2013; Shadrin et al. 2016). The coastal lagoons are continuously transformed by the variability in precipitation and temperature regimes, winds, natural and anthropogenic hydrological factors (siltation, erosion and dredging of channels) as well as other factors. Ecosystems of hypersaline lagoons generally exist in a precarious balance and demonstrate high variability, which adds to the already extreme habitable conditions.
The severity of habitat conditions and high seasonal and long-term variability of various abiotic parameters, significantly exceeding the ranges of variability in other types of marine ecosystems, make the hypersaline lagoons convenient model objects to study the role of variability of various factors in biotic composition changes. Despite the severity of their environment, hypersaline lagoons often demonstrate the highest biological productivity (Shadrin et al. 2015a). This surprising phenomenon has not yet been fully explained, but the hypothesis has been suggested that wide gradients of key abiotic factors in a microscale (e.g. Eh, pH, O2, H2S, light energy) and their short-term variability (hours) facilitate the optimal coupling between different types of metabolism, while maximizing energy and fluxes of biogenic elements in hypersaline lagoon ecosystems (Shadrin et al. 2015a). It is assumed that halotolerant and abundant copepods may contribute to high productivity in such lagoons/lakes (Mageed 2006; Lamptey & Armah 2008; Shadrin & Anufriieva 2013; Anufriieva 2015; Shadrin et al. 2017).
There are more than 100 coastal lakes/lagoons in the Mediterranean Sea, and only a few of them are hypersaline (Pérez-Ruzafa et al. 2012), including Lake Bardawil. It is located in the central part of the Mediterranean coast of Sinai, which is an arid, semi-desert area, characterized by very low precipitation, with the average annual value ranging from 80 to 90 mm, and recharged mainly by seawater intrusions (Krumgalz et al. 1980; Abd Ellah & Hussein 2009). The lake is characterized by hypersaline conditions (from 39 to 100 PSU) and has tectonic origin. The tidal effect, wind direction and speed can cause changes in the water inflow from the Mediterranean Sea, determining the variability of abiotic environmental factors and biotic composition in the lagoon. This coastal lake may serve as a good model system to assess the spatial and temporal variability of the copepod diversity and abundance, and the influence of different factors on these characteristics under hypersaline conditions. So far, several studies have been carried out on copepods in the lagoon (Kimor 1975; Por & Ben-Tuvia 1981; Fouda et al. 1985; El-Shabrawy 2006; Mageed 2006; El-Shabrawy & Gohar 2008). Based on the collected data, the authors hypothesized that: 1) long-term changes occur in the species composition of copepods and their abundance; 2) the salinity fluctuation is not the only factor responsible for these changes; 3)
The studied coastal lake is situated at 32°40′E to 33°30′E and 31°03′N to 31°14′N (Krumgalz et al. 1980; Touliabah et al. 2002; Abd Ellah & Hussein 2009) (Fig. 1). Its length from east to west is about 90 km, the average width is 10 km, and the maximum width is about 22 km at Nahal Yam or Mitizfaq. The lake surface area is more than 600 km2 when all its branches are filled with water. This area fluctuates throughout the year, while ponds and lakes are separated in summer time. The salinity varies from the lowest value of 38 PSU to the highest one – over 70 PSU. The maximum depth is 6.5 m (in the western arm), the minimum depth is 0.3 m and the average depth is 1.2 m. A sand barrier of varying width (from 300 to 2000 m) separates the lake from the Mediterranean Sea, having only one natural opening at the far eastern end. Since 1927, two artificial openings (narrow channels connecting the lagoon with the sea), Boughazes I and II, have been established to reduce the salinity through water exchange with the sea (Fig. 1). This allows the migration of commercial fish from the sea (Ben-Tuvia 1979). The regional arid climate has low precipitation restricted mostly to winter when wind-driven seawater intrusion occurs, and high evaporation during summer. There are two seasons in the region: the rainy season (November to April) and the dry season (from May to October). High air temperatures with scarce rainfall and a high rate of evaporation are observed in dry months. The rainy season is characterized by low air temperatures, strong winds and precipitation.
The precipitation fluctuates on average between 72 mm (December) and 246 mm (July). The prevailing wind direction in the area is mostly from the north but winds may come from all directions. The tidal events, wind direction and speed are among the main causes of the variability in abiotic factors and biotic composition, especially near and between three openings named Boughazes on the northern side of the lake (Touliabah et al. 2002; Mageed 2006). Lake Bardawil has high productivity; its water is often oversaturated with oxygen due to high photosynthetic activity of phytoplankton and bottom macro- and microalgae dwelling in the lake (Krumgalz et al. 1980; Touliabah et al. 2002; El-Shabrawy 2006; El-Kassas et al. 2016). Tintinnina (Ciliophora) and Foraminifera are also abundant in plankton (El-Shabrawy et al. 2018). It is the least polluted Egyptian coastal lake and an important fishing area of high economic value. A large number of migratory birds use this area, which is listed as a Ramsar site since 1988 (El-Shabrawy & Gohar 2008; El-Kassas et al. 2016).
Zooplankton and water samples were collected at 12 sites in Lake Bardawil in August and November 2009, and in February and May 2010 (Fig. 1, Table 1). Zooplankton was collected by filtration of 50 l of water through a plankton net (0.3 m diameter) with a mesh size of 55 μm. Samples were fixed with 4% buffered formalin solution in situ and analyzed using an Olympus SZ-ST stereo microscope and Olympus BX50 compound microscope. Copepod species were identified according to the literature (Lang 1948; Newell & Newell 1977; Nishida 1985; Bradford-Grieve 1994; 1999; Huys et al. 1996; Wells 2007; Prusova et al. 2011). Species names are given in accordance with the World Register of Marine Species database (
Coordinates and depth of the sampling sites in Lake Bardawil in 2009–2010
Sites
Latitude (°N); Longitude (°E)
Depth (m)
1
31°04″37″; 33°13′36″
1.40
2
31°05′58″;33°15′03″′
1.50
3
31°07′03″; 33°16′51″′
1.10
4
31°12′15″; 33°15′41″
2.00
5
31°08′35″; 33°15′40″
1.50
6
31°11′47″; 33°09′20″
1.00
7
31°11′26′ ′; 33°05′54″
1.40
8
31°03′50″; 33°00′02″
1.00
9
31°06′28″; 32°56′49″
1.60
10
31°08′01″; 32°55′47″
2.50
11
31°04′55′ ′; 32°49′17″
2.10
12
31°03′51′′; 32°46′75″
1.50
Water samples for chemical analyses were collected by a 1 l bathometer. Water turbidity was measured in situ using a black and white Secchi disk with a 0.3 m diameter, while pH and water temperature (°C) were measured by Hydrolab (Multi Set 430i WTW). Salinity (PSU) was evaluated as total dissolved solids by filtrating through a glass microfiber filter (GF/C) and a known volume of filtrate was evaporated at 180°C. Dissolved oxygen (mg l−1) was determined using a modified Winkler method.
Data were processed using standard statistical methods (Sokal & Rohlf 1995). The variability of parameters was evaluated by the coefficient of variability (CV). Parameters of regression equations and pair coefficients of correlation (R) were calculated in MS Excel. The Student’s t-test was used to evaluate the significance of differences in average values. The confidence level of correlation coefficients (p) was determined by comparison with critical values of parameters (Müller et al. 1979).
Spatial and seasonal variability of abiotic parameters in Lake Bardawil in 2009–2010 is presented in Table 2. The studied parameters fluctuated in similar ranges to those observed in other years (El-Shabrawy 2006; Mageed 2006; El-Shabrawy & Gohar 2008). A total of 10 species of copepods were recorded in zooplankton during the study period, including 5 Calanoida, 2 Cyclopoida and 3 Harpacticoida (Table 3). Only 4 species were present in all seasons, and 3 species were recorded in only one season.
Abiotic characteristics at the sampling sites (Lake Bardawil; 2009–2010). TB = transparent to the bottom; CV = the coefficient of variability
Parameter
Sites
Average
CV
1
2
3
4
5
6
7
8
9
10
11
12
Summer 2009
Temperature, °C
27.0
27.2
28.1
28.8
28.6
29.5
29.3
27.1
27.7
27.1
27.2
28.3
28.0
0.03
Salinity, PSU
57.7
51.0
57.4
46.2
53.2
48.2
48.7
54.3
44.5
39.5
53.2
67.7
51.8
0.14
Dissolved oxygen, mg l−1
8.8
8.8
9.1
9.3
8.5
8.3
9.1
7.7
8.5
8.5
7.5
8.3
8.5
0.06
pH
8.42
8.56
8.66
8.40
8.50
8.50
8.46
8.11
8.24
8.33
8.33
8.43
8.43
0.02
Transparency, m
1.25
1.25
0.70
1.50
0.60
0.60
0.60
0.70
1.20
2.00
2.00
1.00
1.17
0.46
Autumn 2009
Temperature, °C
17.3
17.5
17.2
18.5
17.6
16.7
17.0
16.4
16.7
17.6
16.4
15.9
17.1
0.04
Salinity, PSU
54.1
56.1
49.4
49.4
40.0
48.9
42.4
50.0
44.3
39.8
45.4
52.1
47.7
0.11
Dissolved oxygen, mg l−1
8.1
9.1
9.5
9.6
9.8
9.2
9.8
11.9
9.6
10.2
12.0
10.9
10.0
0.11
pH
8.33
8.37
8.50
8.31
8.35
8.20
8.28
8.11
8.19
8.30
8.18
8.22
8.28
0.01
Transparency, m
TB
TB
TB
TB
TB
TB
TB
TB
TB
TB
TB
TB
–
–
Winter 2010
Temperature, °C
20.7
20.3
20.1
19.4
20.9
18.4
20.2
22.1
21.3
19.4
21.5
21.6
20.5
0.05
Salinity, PSU
49.0
48.6
45.8
38.8
42.4
40.4
41.1
47.4
39.7
38.6
45.9
52.9
44.2
0.10
Dissolved oxygen, mg l−1
7.1
5.6
6.2
7.3
6.3
5.3
5.8
8.4
7.4
7.2
6.3
8.0
6.7
0.14
pH
7.95
8.17
8.04
8.20
8.01
8.16
8.14
8.04
8.26
8.36
8.06
8.19
8.13
0.01
Transparency, m
0.5
TB
TB
TB
TB
TB
0.4
TB
TB
TB
TB
TB
–
–
Spring 2010
Temperature, °C
23.6
23.7
23.8
24.3
26.2
25.6
25.4
25.3
25.4
25.0
24.9
24.3
24.8
0.03
Salinity, PSU
56.2
52.8
46.4
40.5
49.9
48.2
46.9
51.8
42.6
39.9
49.5
59.1
48.7
0.12
Dissolved oxygen, mg l−1
5.8
8.4
8.6
7.0
6.8
8.8
6.4
6.8
6.6
8.4
5.9
6.4
7.2
0.15
pH
8.07
8.08
8.07
8.20
8.20
8.40
8.31
8.01
8.19
8.15
8.17
8.20
8.17
0.01
Transparency, m
TB
TB
TB
TB
TB
TB
0.6
TB
TB
TB
TB
TB
–
–
Copepoda species in plankton of Lake Bardawil in 2009–2010. A = frequency of occurrence (%); B = average abundance (ind. m−3)/the coefficient of variability; C = relative abundance (%)
Species
2009
2010
Annual average/CV
August
November
February
May
Calanoida
A
B
A
B
A
B
A
B
B
36
364/1.39
0
0
0
0
0
0
91/2.00
0
0
42
767/1.67
25
267/1.95
50
1545/1.09
679/1.05
0
0
0
0
0
0
17
182/2.14
46/2.00
0
0
0
0
0
0
25
364/1.79
91/2.00
9
182/3.32
67
433/1.08
25
200/1.81
50
727/1.07
255/0.66
Cyclopoida
100
4455/0.87
100
3833/0.62
75
867/0.73
100
4273/0.64
1680/0.39
0
0
9
67/3.46
9
67/3.46
0
0
34/1.16
Harpacticoida
33
364/1.85
92
3233/1.11
50
1533/1.38
83
3273/0.98
1414/0.67
55
727/1.39
25
133/1.95
33
267/1.48
50
727/1.33
309/0.67
9
91/3.32
0
0
17
133/2.34
0
0
67/1.20
Nauplius
100
39 455/0.36
100
51 500/0.05
100
18 733/0.63
100
45 364/0.79
14 230/0.37
Cyclopoid copepodids
100
13 000/0.49
100
7567/0.36
100
2067/0.65
100
10 917/0.64
8388/0.57
Calanoid copepodids
45
1000/2.10
83
2267/1.30
25
667/2.45
75
2636/1.09
956/0.58
Total copepodids
100
14 000/0.45
100
9833/0.38
100
2733/0.77
100
13 333/0.66
9975/0.52
Total adults
100
7182/0.79
100
8467/0.70
92
3333/1.00
100
10 417/0.50
7350/0.41
Total of all stages
100
59 636/0.34
100
69 800/0.41
100
24 800/0.54
100
69 833/0.60
56 017/0.38
Total metazoan zooplankton
100
69 727/0.33
100
78 200/0.42
100
35 133/0.41
100
23 2917/0.64
10 3994/0.85
C
C
C
C
C
Percentage of all copepod stages in total metazoan zooplankton abundance, %
85
90
68
35
70
Percentage of
62
45
26
41
44
Percentage of
5
38
46
31
30
Percentage of
0
9
8
15
8
The maximum total abundance of copepods was recorded in autumn and spring (Table 3), when copepods accounted for 68 to 90% of the total abundance of metazoan zooplankton in three seasons, and only 35% in spring. In addition to Copepoda, Rotifera, Pterapoda, Appendicularia, Chetognata, and larvae of benthic fauna were present in the metazoan plankton, which will be analyzed in another work prepared by the authors. The average annual contribution of
The distribution of the total abundance of copepods was close to random in the coastal lake, while the spatial distribution of adults and copepodid stages of individual species varied from random to aggregated. The distribution of the total abundance of nauplii in particular seasons varied from close to homogeneous (autumn) to random (spring). Abiotic factors did not significantly affect the distribution of the total abundance of copepods, nauplii and copepodids, or the abundance of individual species. The salinity significantly influenced the abundance of nauplii only in autumn (R = 0.615,
Salinity and temperature limits for copepod species occurrence in Lake Bardawil (2009–2010)
Species name
Temperature, °C
Salinity, PSU
min.
max
min.
max
27.1
28.6
39.5
54.3
16.4
25.6
38.8
52.1
25.0
25.3
39.9
51.8
15.9
29.3
38.6
59.1
17.3
29.5
39.7
57.4
23.8
25.4
39.9
46.4
18.4
27.7
38.6
44.5
15.9
29.5
38.6
59.1
19.4
19.4
38.6
38.6
15.9
27.7
38.6
52.1
To date, 30 copepod species have been found in the lake (Table 5). A total of 561 species of planktic copepods were recorded in the Mediterranean Sea (Razouls et al. 2005–17; Zakaria et al. 2016), of which no more than 2% were able to adapt to the habitat conditions of a shallow hypersaline coastal lake.
Copepoda species found in Lake Bardawil in 1967–2010 authors’ data
Species
1967
1981
1985
2002–2003
2005
2006
2009–2010
Calanoida
–
+
+
+
+
+
–
–
–
–
–
–
+
+
–
–
–
–
–
–
+
–
–
+
–
–
–
–
–
–
+
–
–
–
–
–
–
–
–
–
+
–
+
–
–
–
–
–
–
–
–
–
+
+
–
–
–
–
+
+
+
+
+
–
–
+
+
+
–
–
–
–
+
–
–
–
–
–
–
+
–
–
+
+
–
–
+
–
–
–
–
–
–
+
+
+
+
+
–
+
+
+
+
–
–
–
–
+
–
–
–
–
–
–
–
–
–
+
–
–
–
+
–
–
–
–
Cyclopoida
–
–
+
–
–
–
–
–
–
–
+
+
+
+
–
–
–
+
+
–
+
Harpacticoida
–
–
+
–
–
–
–
–
–
–
+
+
+
–
–
+
+
+
+
+
+
–
–
–
+
+
+
+
–
–
–
+
+
–
–
–
–
+
+
+
+
+
Poecilostomatoida
–
–
+
–
–
–
–
–
–
+
–
–
–
–
–
–
+
–
–
–
–
–
–
–
–
–
+
-
All copepods found in the lake can be divided into three groups: 1) plankton species that form stable populations, 2) species of Mediterranean plankton incidentally entering the lake from the adjacent sea area, 3) benthic Cyclopoida –
The total copepod abundance in the lagoon was significantly higher (90 times on average) compared to that observed in 2008–2009 in the waters of the Mediterranean Sea off the coast of Egypt (Zakaria et al. 2016). The greatest differences were observed in spring, when the number of copepods in the lake was on average 93 times higher than in the sea.
The smallest differences were recorded in winter – the average abundance in the lake was only 58 times higher. In general, the nature of seasonal changes in the abundance of copepods in the sea and the lake was the same. However, the amplitude of seasonal changes in the average total abundance of copepods was significantly higher in the lake, and it was 2.8 times higher in spring than in winter, while in the sea this ratio was 1.2. The age structure of copepod taxocenes in the sea also differed from that in the lake. The contribution of nauplii and copepodid stages to the total number of copepods in the lake varied from 65 to 76% and from 8 to 22%, respectively. In the sea, these values varied from 25 to 39% and from 36 to 40%, respectively. Such high proportion of nauplii in the total number of copepods in the lake (from 53 to 79%) was also observed in 2002–2005 (El-Shabrawy 2006; Mageed 2006; El-Shabrawy & Gohar 2008). Probably these differences can be explained by the shorter lifespan of adult stages in the lake, higher fertility and/or higher mortality of copepodids and adults.
Such high abundance and a large proportion of nauplii indicate a high productive potential of the copepod taxocene in the lake. This contributes to the intensification of nutrient cycling and supports high primary productivity in the lake. An increase in zooplankton grazing on phytoplankton usually causes a greater nutrient input, which is important for the productivity of oligotrophic lakes/lagoons. There is a nutrient limitation of primary production in Lake Bardawil – N-limitation in spring and summer and P-limitation in summer and autumn (Touliabah et al. 2002). To discuss this issue in greater depth, we need information on trophology and ecophysiology of copepods in the lake.
In spring,
Since 1967, the complex of common and dominant copepod species in the lake has changed significantly (Table 5). Only the harpacticoid
The total average annual copepod abundance fluctuated (El-Shabrawy 2006; Mageed 2006; El-Shabrawy & Gohar 2008; present study): in 2002 – about 4000 ind. m−3, in 2004 – more than 152 000 ind. m−3, in 2005 – 25 300 ind. m−3, and in 2009–2010 – 56 000 ind. m−3. We do not have enough data to look for regularities of the long-term variability in copepod abundance. It can be considered that salinity in coastal lakes/lagoons is one of the most important factors affecting organisms (Reid & Wood 1976). The new data together with the previously published works (Jorcin 1999; Shadrin & Anufriieva 2013; El-Shabrawy et al. 2015; Shadrin et al. 2017) have led us to an assumption that changes in salinity are not the main cause of the spatial and temporal variability in the abundance of copepods in the lake in 2002–2010. Fluctuations in the water and species exchange between the lake and the sea are likely to contribute more to the variability in plankton composition and abundance. In general, it is very difficult to relate the total marine zooplankton changes in some areas to changes in one or two environmental parameters. As an example, a plankton time series (1988–2007) has been conducted at the monitoring station in the Western Channel off Plymouth (UK), and the analysis of these data demonstrated that long-term changes in the overall mesozooplankton community structure and abundance over a period of 20 years cannot be strongly linked to environmental descriptors (Eloire et al. 2010). Taking into account all available information, we may assume that different irregularities and the chance are among the main drivers of the spatial, seasonal and long-term variability of the copepod taxocene in the studied coastal lake. We cannot understand the dynamics of plankton without accounting for the above drivers or benthos-plankton interactions. Lack of knowledge about the above as well as some other neglected factors and associations limit our understanding of the lake ecosystem as a whole. For this reason, we do not attempt to explain spatial and temporal variability and patterns in this work, as significantly more information is needed to do this.