Summer Variability of the Zooplankton Community along the El Bibane Lagoon (Tunisia, Eastern Mediterranean)

Abstract

Studying zooplankton variability in coastal lagoons is crucial for environmental monitoring and preserving marine biodiversity. These organisms are highly valued as bio-indicators and helpful in identifying environmental phenomena such as eutrophication and assessing water quality. We studied the distribution of zooplankton in relation to environmental factors, phytoplankton, and ciliates in the coastal waters of the El Bibane lagoon during the summer of 2009 and 2010. Zooplankton assemblages were dominated by copepods, which represented 73–89% and 95–98% of total zooplankton abundance in summer 2009 and summer 2010, respectively. A total of 11 (summer 2009) and 21 (summer 2010) copepod species were identified in all stations, with an overwhelming abundance of Oithona nana in the summer of 2009 and Oithona similis in the summer of 2010. The prevalence of the two Oithona species is attributed to their adaptive strategies, which enables them to withstand environmental disturbances. Other zooplankton developed in association with an important proliferation of Cladoceran and Fish larvae, contributing 51% and 37% of total other zooplankton abundances in summer 2009 and summer 2010, respectively. The abundance of copepods or other zooplankton showed no significant correlation with phytoplankton and ciliates for both periods, suggesting an omnivorous/detritivorous diet hypothesis in El Bibane lagoon.

1. Introduction

Plankton communities are viewed as being structured by a combination of factors such as climate change, abiotic properties, biotic factors [1], and regional effects (pollution) [2]. Zooplankton is a critical trophic link between phytoplankton, commercial fish stocks, and sea birds [3], and small zooplankton is an essential link between classical and microbial trophic levels [4]. The zooplankton species may respond differently to food concentration and environmental parameter variations [3]. In this context, it is important to understand the fluctuations in zooplankton abundance and their associations with physicochemical changes in the marine environment. These factors affect zooplankton at different scales [5], both directly [6] and indirectly, by shaping the abundance and repartition of their predators and prey [7], which will define populations’ growth [8] and mortality rates [9]. Planktonic copepods are the major members of zooplankton in marine pelagic ecosystems [10]. They graze on nano-micro-phytoplankton and microzooplankton [11], and at the same time, they are preyed on by higher trophic levels, such as fishes. Planktonic ciliates play an important role in transferring the production of pico and nanoplankton to meso- and macroplankton [12]. Variations in the repartition of ciliates may significantly affect other components of the marine food web and thus may influence the community structure and species composition of lower and higher organisms [13]. This study deals with the El Bibane lagoon (Gulf of Gabès, Tunisia), a symbolic Mediterranean ecosystem classified as Ramsar Wetland since 2007. This shallow lagoon is under eutrophication stress. The Gulf of Gabès, situated in southern Tunisia, is a unique and ecologically significant area in the Mediterranean Sea. Unfortunately, this dynamic marine ecosystem is undergoing cultural eutrophication, characterized by nutrient enrichment from phosphorus and nitrogen salts [14]. Major contributors to nutrient pollution in the Gulf of Gabès include industrial discharges, urbanization, and agricultural activities [15]. A preceding study concerns the micro-phytoplankton communities [16]. Here, we focus on zooplankton, a crucial biological indicator of water quality and trophic status in lagoons, as they rapidly respond to environmental changes. With the objectives to (i) determine whether physicochemical properties such as water temperature, salinity, pH, and nutrient concentrations significantly impact the occurrence of the different zooplankton species; and (ii) analyze the dynamic and diversity of the zooplankton community in relation to phytoplankton and ciliates.

2. Materials and methods

2.1 Study site

The El Bibane lagoon, also known as Bhiret el Bibane, is a large lagoon of around 33 km in length by 10 km in width next to the Libyan limit. It is 10 km North of Ben Gardane city and 20 km West of Zarzis city. It is linked to the sea by a series of small channels, the largest of which is 800 m wide. This lagoon is the second largest in Tunisia after the Boughrara lagoon (Figure 1).

Figure 1.

Location of sampling stations along the El Bibane lagoon.

2.2 Field sampling

Samples for nutrients, phytoplankton, zooplankton, and ciliates were collected during one-day campaigns performed in summer (July 2009 and July 2010) at four stations (Figure 1). Seawater samples for nutrients, phytoplankton, and ciliates were collected with a Van Dorn-type closing bottle deployed horizontally. Zooplankton samples were collected using a cylinder-conical net (30 cm aperture, 100 cm high, and 100 μm mesh size). The volume of water filtered was about 1 m³. Back in the laboratory, samples for nutrient analyses (120 mL) were immediately filtered under a low vacuum (<50 mm Hg) through pre-combusted (500°C, 4 h) GF/F (~0.7 mm) glass fiber filters (25 or 47 mm diameter, Whatman) using glassware filtration systems. Nutriment samples (120 mL) were kept immediately upon collection at −20°C in the dark. Samples for phytoplankton were preserved with acid Lugol solution (at 3%; [17]), and alkaline Lugol solution was used for fixation of ciliates samples (at 5%; [18]). Zooplankton samples were preserved in a 2% buffered formaldehyde solution and were stained with rose Bengal to facilitate dissection. Samples for plankton were placed at 4°C in the dark for enumeration.

2.3 Physicochemical variables

Physicochemical parameters (temperature, salinity, and pH) were measured using a multi-parameter kit (Multi 340 i/SET) immediately after sampling. Water for nutrient (nitrite, nitrate, ammonium, orthophosphate, silicate, total nitrogen, and total phosphate) analyses was collected in plastic containers of 4.5 mL previously washed with distilled water. Samples were analyzed with a Bran and Luebbe type 3 autoanalyzer, and concentrations were determined colorimetrically using a UV-visible (6400/6405) spectrophotometer [19]. Analyses are independent. The automatic analysis system provides a fast and accurate analysis of these nutrients. Although each nutrient is determined differently, the method remains similar. It used colorimetry to determine the dosage of each nutrient.

2.4 Plankton enumeration

Sub-samples (50 mL) for phytoplankton and ciliates counting were analyzed under an inverted microscope using the Utermöhl method [20] after 24 h settling. Phytoplankton and ciliates species counts were carried out on the entire sedimentation chamber with 40X magnification. Phytoplankton and ciliates were identified using morphological criteria. Phytoplankton species were identified according to various keys [21, 22]. Ciliates were identified at the genus or species level after the works [23, 24, 25]. Zooplankton enumeration was performed under a vertically mounted deep focus dissecting microscope (Olympus TL 2) after being colored with Bengalrose to identify internal tissues of the different zooplankton species and also to facilitate copepod dissection such as various appendixes and leg 5 of the different species. Zooplankton species identification was identified using various keys [26, 27, 28]. Their relative frequency determined the importance value for the different species.

2.5 Statistical analyses

The environmental parameters assessed at four stations and two periods were submitted to a normalized principal component analysis (PCA) [29]. Physical-chemical variables, such as temperature, salinity, pH, nutrient concentrations, and biological parameters, were assessed by examining the projection of the plots of the extracted factors on a factorial plan consisting of the statistically significant axis of the PCA. A simple log (x + 1) transformation was applied to the data in order to stabilize variance correctly [30]. The spatiotemporal patterns of zooplankton taxonomic groups were assessed with a non-metric multidimensional scaling (NMDS) after square-root transformation of data using PRIMER v7 software. Means and standard deviations (SD) were reported when appropriate. The spatial variability of biological communities and their relationships with environmental factors were assessed using Spearman rank correlation.

3. Results

3.1 Physical, chemical, and trophic parameters

The mean and range values of the four studied stations for physical and chemical variables recorded in July 2009 and July 2010 are given in Table 1. Surface water temperature was slightly warmer in summer 2010 (28.68 ± 0.54°C) than in summer 2009 (28.20 ± 0.39°C) (Table 1). The highest temperature (29.15°C) was recorded in the summer of 2010 and the lowest one (27.74°C) in the summer of 2009 at station 3. The average salinity was 45.46 ± 0.77 psu in the summer of 2010, and 45.77 ± 0.96 psu in the summer of 2009 (Table 1). pH was higher in the summer of 2009 (8.35 ± 0.19) than in the summer of 2010 (8.29 ± 0.16) (Table 1).

Variables	Summer 2009			Summer 2010
	Minimum	Maximum	Mean ± SD	Minimum	Maximum	Mean ± SD
Physical variables
Temperature (°C)	27.74	28.56	28.20 ± 0.39	27.90	29.15	28.68 ± 0.54
Salinity (psu)	44.50	46.83	45.77 ± 0.96	44.70	46.30	45.46 ± 0.77
pH	8.21	8.61	8.35 ± 0.19	8.13	8.51	8.29 ± 0.16
Chemical variables
NO2^− (μM)	0.16	0.31	0.24 ± 0.07	0.11	0.39	0.22 ± 0.13
NO3^− (μM)	0.99	1.28	1.11 ± 0.12	0.89	2.06	1.45 ± 0.58
NH4^+ (μM)	1.09	1.46	1.23 ± 0.17	1.00	1.65	1.41 ± 0.31
T-N (μM)	4.85v	6.42	5.67 ± 0.81	6.12	7.17	6.51 ± 0.46
PO4^3− (μM)	1.94	5.65	3.25 ± 1.67	2.03	3.05	2.52 ± 0.42
T-P (μM)	10.29	15.97	12.65 ± 2.76	11.82	12.54	12.22 ± 0.32
N/P ratio	0.50	1.23	0.92 ± 0.35	0.87	1.83	1.25 ± 0.42
Si(OH)4 (μM)	2.09	4.25	3.51 ± 0.96	3.39	5.82	4.63 ± 1.09
Biological variables
Chlorophyll-a (mg l^−1)	0.83	1.15	1.00 ± 0.16	0.70	1.88	1.33 ± 0.54
T- zooplankton (ind m^−3)	12,772	26,928	18,090 ± 6520	2212	65,688	40,810 ± 27,273
Copepods (ind m^−3)	10,806	21,120	14,498 ± 4599	2170	62,470	39,076 ± 26,034
Cyclopoids (ind m^−3)	1311	16,192	7032 ± 6419	917	247	12,862 ± 9709
Calanoids (ind m^−3)	4224	8349	6392 ± 1705	501	24,704	11,893 ± 10,003
Harpacticoids (ind m^−3)	000	310	118 ± 149	210	3360	1240 ± 1477
Poecilostomatoids (ind m^−3)	000	176	119 ± 081	000	630	267 ± 263
Other zooplankton (ind m^−3)	1478	5808	3592 ± 2187	042	3218	1734 ± 1320
T- ciliates (cells l^−1)	000	700	081 ± 159	000	300	053 ± 088
T- phytoplankton (cells l^−1)	1400	18,700	8450 ± 7424	9600	22,700	16,950 ± 6077

Table 1.

Minimum (Min), maximum (Max), and mean ± SD (standard deviation) of physicochemical parameters, zooplankton, phytoplankton, and ciliates communities in summer 2009/2010 along the El Bibane lagoon.

The concentration of total nitrogen (T-N) was, on average, 5.67–6.51 μM, ranging from 4.85 (station 2, Summer 2009) to 7.17 μM (station 1, summer 2010). NO₃⁻ and NH₄⁺ concentrations were relatively high (> 1 μM), while NO₂⁻ concentration was much lower (0.22–0.24 μM) (Table 1). The concentration of total phosphorus (T-P) varied from 10.29 (station 1, summer 2009) to 15.97 μM (station 2, summer 2009). The relatively important T-P concentrations were due to the high contribution of PO₄³⁻, close to 23% of T-P, which displayed a mean concentration of 3.25 ± 1.67 μM and 2.52 ± 0.42 μM in summer 2009 and summer 2010, respectively, showed the highest value 5.65 μM in summer 2009 station 2 (Table 1). Nutrient values were indicative of a generalized eutrophication. The N/P was always lower than the Redfield ratio, suggesting potential N limitation in this area (Table 1).

3.2 Zooplankton community structure and spatial distribution

The total zooplankton abundance varied from 2212 (station 2) to 65,688 ind m⁻³ (station 3) in summer 2010. Zooplankton assemblages were dominated by copepods, representing 73–89% and 95–98% of total zooplankton abundance in summer 2009 and 2010, respectively (Figure 2). Total copepod abundance was negatively associated with salinity (r = −0.891, p > 0.05) and positively with phosphates (r = 0.923, p > 0.05). The highest copepod abundances were observed at station 3 (62,470 ind m⁻³) in July 2010. Their abundance did not exceed 21,120 ind m⁻³ in July 2009 (Table 1). Other zooplankton (Appendicularia, Bivalvia, Cirripedia nauplii, Cladoceran, Euphausiacea, Fish larvae, Gasteropoda larvae, Hydromedusae, Ostracoda, Polychaeta larvae and Zoea) presented low relative abundances at the two periods (2–26% of total zooplankton abundance) (Figure 2), with mean abundances of 1734 ± 1320 ind m⁻³ in summer 2010 and 3592 ± 2187 ind m⁻³ in summer 2009 (Table 1). Other zooplankton abundance was positively correlated with phosphates (r = 0.985, p < 0.05).

Figure 2.

Spatial variations of zooplankton groups abundance in summer 2009/2010 along the El Bibane lagoon.

Copepods composition and abundance showed four groups: Calanoids (on average 19–77% of the total copepod abundance), Cyclopoids (12–76%), Harpacticoids (0–12%) and Poecilostomatoids (0–1%) (Figure 3). A total of 23 copepod species were found at all stations (Table 2), with Oithona nana dominating the total abundance of copepods (35%) in the summer of 2009. Oithona similis abundances were also higher in the summer of 2010 (104.73 ± 7279 ind m⁻³) than in the summer of 2009 (2777 ± 497 ind m⁻³). Copepod richness was higher in the summer of 2010 (21 species) than in the summer of 2009 (11 species) (Table 2). Among other zooplankton, Cladocerans were dominant in abundance (51% of total other zooplankton) in the summer of 2009, followed by Fish larvae with 37% in the summer of 2010 (Figure 4).

Figure 3.

Spatial variations of the relative abundance of copepod groups in summer 2009/2010 along the El Bibane lagoon.

	July 2009				July 2010
	S1	S2	S3	S4	S1	S2	S3	S4
Copepoda
Nauplii	982	591	528	1240	23,730	500	11,700	15,330
Calanoida
Acartia clausi	328	—	—	—	8820	250	21,775	10,920
Acartia italica	—	—	—	—	—	—	98	—
Paracartia latisetosa	—	444	—	—	—	—	—	—
Centropages kroyeri	1474	148	352	620	—	—	231	—
Centropages typicus	4910	1035	2464	1705	315	—	325	—
Isias clavipes	—	—	—	—	210	—	325	210
Temora stylifera	—	—	—	—	210	—	—	—
Temora longicornus	164	—	—	—	—	42	—	210
Temora sp.	—	—	—	—	—	167	1950	210
Paracalanus parvus	1473	5169	1408	3875	—	42	—	1050
Megacalanus princeps	—	—	—	—	—	—	—	210
Cyclopoida
Oithona nana	1147	2365	12,848	2635	420	417	6825	1890
Oithona similis	—	2217	3168	2945	12,600	500	17,875	10,920
Oithona plumifera	164	—	176	465	—	—	—	—
Poecilostomatoida
Corycaeus clausi	—	—	—	—	—	—	—	210
Farranula rostrata	—	—	—	—	210	—	—	—
Oncaea conifera	—	148	176	155	—	—	—	420
Oncaea mediterranea	—	—	—	—	—	—	228	—
Harpacticoida
Euterpina acutifrons	164	—	—	310	210	—	325	210
Microsetella norvegica	—	—	—	—	420	—	650	—
Microsetella rosea	—	—	—	—	1890	84	—	—
Macrosetella gracilis	—	—	—	—	—	84	—	—
Tisbe battagliai	—	—	—	—	840	84	163	—
Other Crustaceans
Cladocera	328	148	4048	2790	210	—	325	—
Ostracoda	—	—	176	—	—	—	—	—
Euphausiacea	—	—	—	—	210	—	—	—
Gelatinous
Appendicularia	328	739	704	930	—	—	—	—
Hydromedusae	—	—	—	—	315	42	325	—
Meroplankton
Gasteropoda larvae	982	591	704	1085	210	—	650	210
Bivalvia	328	—	176	310	—	—	293	210
Cirripedia nauplii	—	—	—	—	—	—	—	210
Polychaeta larvae	—	—	—	—	210	—	325	—
Zoea	—	—	—	—	210	—	—	420
Fish larvae	—	—	—	—	210	—	1300	1050

Table 2.

List and abundance (in ind.m⁻³) of the zooplankton species observed in the summer 2009/2010 along the El Bibane lagoon.

Figure 4.

Average distribution of the relative abundance of other zooplankton groups in summer 2009/2010 along the El Bibane lagoon.

3.3 Relationships between zooplankton, phytoplankton, and ciliate

The spatial distribution of zooplankton abundance with the prevailing potential prey (total phytoplankton and total ciliate) is illustrated in Figure 5. The abundance of zooplankton does not show any significant correlations between the abundance of copepods or other zooplankton and phytoplankton and ciliates for both periods.

Figure 5.

Spatial variations of total zooplankton, phytoplankton, and ciliates abundance in summer 2009/2010 along the El Bibane lagoon.

3.4 Multivariate analysis

The first factorial plane (axes 1 and 2) of the PCA analysis on environmental, phytoplankton, and ciliate variables explained 86.36% of the total variance, 58.35% of it for the first component and 28.01% for the second component (Figure 6a). The first axis shows an opposition between stations 2–3 correlated to all nutrients and stations 1–4 correlated to phytoplankton, Chla pH, and ciliates. The second axis opposes the two periods for stations 2–3 associated with phosphorous nutrients in July 2009 and nitrogen nutrients and silicium in July 2010. The NMDS on zooplankton taxonomic groups clearly separates the communities of the two periods, with July 2009 associated with non-copepod crustaceans and gelatinous organisms and July 2010 associated with nauplii, Poecilostomatoide, Calanoida, and Harpacticoids.

Figure 6.

Results of (A) principal component analysis (axes I and II) performed on environmental, phytoplankton, and ciliate variables and (B) non-metric multidimensional scaling on percentage abundance of zooplankton taxonomic groups.

4. Discussion

The present study is the first to examine the spatial distribution of zooplankton communities in the coastal waters of the El Bibane lagoon in relation to nutrients, phytoplankton, and ciliates. Nutrient concentrations showed a generalized eutrophication status (Table 1). High eutrophication levels of the coastal waters of the Gulf of Gabès were confirmed [13, 14].

Copepods dominated the zooplankton community in all the stations in the El Bibane lagoon in summer. The dominance of copepods has already been reported in several studies in the Gulf of Gabès region: on western area of the Djerba coasts (54–100% of total zooplankton abundances; [16]); on the northern coast of Sfax (61–82%; [2, 31]); along the southern coast of Kerkennah Islands (98%; [32]), in Kneiss Islands (30–96%; [33]) in summer. Among copepods, Calanoids were highly dominant (19–77% of the total copepod abundance), which is very similar to what was observed by Rekik et al. [16] in the coastal area of Djerba Island (up to 79% of total copepod abundance) and Drira et al. [34] on the coast of Sfax (43% of total copepod abundance).

Although the environmental and tropic conditions did not change significantly between the summer of 2009 and the summer of 2010, the structural composition of the zooplankton community showed very distinctive traits between the two periods in the El Bibane lagoon. Cladocerans were much more abundant in 2009, and appendicularians, relatively abundant in the four stations in 2009, were absent in 2010. The copepod community was dominated by Oithona nana (35% of total copepods) in the summer of 2009 and Oithona similis (40% of total copepods) in the summer of 2010. Small planktonic copepods reached important abundance throughout the study period. Small species, particularly Oithonids, were found to mostly dominate the copepod community in both summer 2009 and summer 2010. This appears to be a common feature in coastal areas of the Gulf of Gabès [2, 35] in offshore waters of the Gulf of Gabès [36]. The prominence of small planktonic copepods in the Gulf of Gabès, such as Oithona nana and Oithona similis, in diverse marine sites of the Gulf of Gabès, was inferred owing to its adaptive strategies [37], combined with an omnivorous diet [14] and lower metabolic needs [14], allowing it to tolerate environmental perturbations and tolerance to pollution [38]. The omnivorous/detritivorous diet can be confirmed by the lack of significant correlation between copepods and phytoplankton and between copepods and ciliates for both periods.

Oithona similis is known as the most omnipresent copepod species in the world sea [38]. This small species has a clear eurythermal and euryhaline distribution [39, 40].

5. Conclusion

This study analyzes zooplankton distribution in the El Bibane lagoon, emphasizing their connections with nutrients, phytoplankton, and ciliates. It confirms a generalized eutrophication status in the Gulf of Gabès and highlights the dominance of copepods, particularly Calanoids, consistent with regional findings. Significant changes in zooplankton composition between summer 2009 and summer 2010, despite stable conditions, are noted. The prominence of small planktonic copepods like Oithona nana and Oithona similis is linked to their adaptive strategies, including an omnivorous/detritivorous diet and tolerance to environmental disturbances. This study highlights the ecological importance of zooplankton as an environmental indicator and offers valuable insights into the marine ecosystems of the Gulf of Gabès. To address eutrophication, efforts in the Gulf focus on sustainable development, stricter industrial regulations, improved agricultural practices, and enhanced wastewater management.

Acknowledgments

This study was performed in the framework of the international project Société d’étude de Réalisation d’Aménagement et d’Hydraulique (SERAH). This work was conducted in the Marine Biodiversity and Environment LR/18ES30 laboratory at the University of Sfax.