What factors drive the variations of phytoplankton, ciliate and mesozooplankton communities in the polluted southern coast of Sfax, Tunisia? Zohra Ben Salem, Zaher Drira & Habib Ayadi
Environmental Science and Pollution Research ISSN 0944-1344 Environ Sci Pollut Res DOI 10.1007/s11356-015-4416-8
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Author's personal copy Environ Sci Pollut Res DOI 10.1007/s11356-015-4416-8
RESEARCH ARTICLE
What factors drive the variations of phytoplankton, ciliate and mesozooplankton communities in the polluted southern coast of Sfax, Tunisia? Zohra Ben Salem 1 & Zaher Drira 1 & Habib Ayadi 1
Received: 5 August 2014 / Accepted: 20 March 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract We studied the spatial distribution of phytoplankton, ciliate and mesozooplankton communities coupled with environmental factors in the southern coast of Sfax (central eastern coastline of Tunisia). Phytoplankton assemblages were dominated by Dino phyceae (69.99 %) and Bacillariophyceae (15.88 %). The ciliate community consisted of Spirotrichea with a dominance of Tintinnopsis beroidea (57.69 %). The mesozooplankton community was dominated by copepods representing 66.12 % of the total zooplankton. Oithona nana showed a high frequency mainly in stations 9 and 10 with 66.86 and 64.65 %, respectively. Some toxic phytoplankton species were recorded in the present study site. For this reason, the pollution generated in this area presents a slight degradation of the water quality and can be responsible for the bloom generated by the high proliferation of these toxic microalgae. The pollution generated by Responsible editor: Philippe Garrigues Highlights There are several consequences of anthropogenic pollution in balancing the ecosystem equilibrium. The species richness indexes applied for phytoplankton, ciliates and copepods showed that the southern coast of Sfax is the subject of a slight degradation of water quality. The restoration of the southern coast of Sfax heavily contaminated with phosphogypsum waste with reference to the works carried out at the northern coast of the city and the clear improvement of the water quality remain an important necessity. Zohra Ben Salem and Zaher Drira contributed equally to this work. * Zaher Drira
[email protected] 1
Biodiversity and Aquatic Ecosystems UR/11ES72 Research Unit, Department of Life Sciences Research, Sfax Faculty of Sciences, University of Sfax, Street of Soukra Km 3.5. BP 1171, PO Box 3000, Sfax, Tunisia
industrial activities has an effect on the spatial distribution of phytoplankton, ciliate and copepod communities with a reduction of their diversity indexes. Keywords Southern coast of Sfax . Environmental impact . Phytoplankton . Ciliate . Copepods . Physicochemical parameters
Introduction The zooplankton is the optimal prey of nekton (Mazumder et al. 2006) among which copepods make a major contribution to optimal growth and survival in fish (Daan 1989; Hop et al. 1997; Tudela and Palomera 1997). Copepods are the most abundant components of coastal and oceanic zooplankton assemblages (Huggett and Richardson 2000; Peterson and Keister 2002; Albaina and Irigoien 2004; Berasategui et al. 2006; Porri et al. 2007; Duggan et al. 2008) as elsewhere in the Mediterranean Sea (Razouls and Durand 1991; Ragosta et al. 1995; Calbet et al. 2001). Indeed, the variability in their abundance in time and space is important to the dynamics of marine food webs. Ciliated protozoa are a ubiquitous component of aquatic food webs in the marine environment (Dolan et al. 1999; Petz 1999; Perez et al. 1997, 2000) and they represent a complex assemblage of interacting organisms, often including species that are sensitive, resistant or intermediate in their tolerance to pollutants. So, they play a pivotal role in mediating the transfer of organic matter to higher trophic levels in this marine coastal ecosystem (James and Hall 1995). Therefore, phytoplankton such as dinoflagellates and diatoms, with year-round presence on low concentrations on the one hand, and bloom-forming capacity on the other, suggest a differential control by nutrients/light and grazing (Al-Najjar et al. 2007). So, the investigation of the relationship between
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these different compounds of the food chain highlights the state of environmental circumstances in a studied site. Several studies were conducted in the Gulf of Gabes focusing on the spacetime changes on plankton communities such as phytoplankton (Bel Hassen et al. 2008, 2009a, b; Drira et al. 2008, 2009, 2010a), ciliate (Hannachi et al. 2008; Kchaou et al. 2009) and copepod assemblages (Drira et al. 2010a, b, 2013; Ben Ltaief et al. 2014) in offshore and inshore areas. However, data concerning the spatial and/or temporal distribution of plankton assemblages in the south coast of Sfax, which is a part of the Gulf of Gabes, were lacking or scarce. During the last few decades, the expansion of industrial and commercial activities in the coast of Sfax has become an issue of increasing environmental concern. Many works have reported its high level of atmospheric pollution (Azri et al. 2007, 2008, 2010) and aquatic pollution such as hydrocarbon (Louati et al. 2001; Zaghden et al. 2005, 2007, 2014), phosphogypsum (Tayibi et al. 2009; Rekik et al. 2012a), and heavy metal content (Mkawar et al. 2007; Gargouri et al. 2011; Ghannem et al. 2011; Serbaji et al. 2012). This anthropogenic pollution, associated with the demographic expansion and the rapid urban development, has seriously affected the biota (Hamza-Chaffai et al. 1997, 2003; Smaoui-Damak et al. 2003, 2004; Banni et al. 2005; Jebali et al. 2007; Barhoumi et al. 2009) and the spawning and refuge area for fish larvae, especially the endemic seagrass Posidonia oceanica (Hamza-Chaffai et al. 2003). The works carried out by Rekik et al. (2012b) were limited to assessing the state of ultraphytoplankton. Thus, the study of phytoplankton, ciliate and mesozooplankton communities can provide valuable information on the functioning of pelagic ecosystems. The aim of this study is to know (1) which abiotic factor mostly affects the structure, richness and composition in the distribution of phytoplankton, ciliate and zooplankton communities in the south coast of Sfax, subject to high pollution pressure; and (2) how these planktonic groups might react to the increased discharge.
Materials and methods Study site The study investigates the spatial distribution of phytoplankton, ciliate and mesozooplankton communities coupled with physicochemical factors in the southern coast of Sfax (central eastern coast of Tunisia, between 34° N and 10° E). In fact, Sfax is characterized by a dry climate (average precipitation 210 mm) and by winds, waves and currents (0.2–0.3 s−1) having a predominant north-south direction (Louati et al. 2001). It has a population of 733687 inhabitants, of which 53 % live in the urban parts of the city. The southern coast of Sfax extends along 15 km from the fish port to Gargour (zone characterized by urban and industrial activities). It has received industrial
wastewater drained from the phosphate treatment plant, Societe Industrielle d’Acide Phosphorique et d’Engrais (SIAPE), since 1952 and treated domestic wastewater drained from the wastewater treatment plant of Sfax City which has been operational since 1983 (Baati et al. 2011). Field sampling Samples for nutrients, phytoplankton, ciliates and chlorophyll-a were collected in February 2008 at 20 stations (from 0.5 to 4.2 m in depth) along the southern coast of the Sfax City (Fig. 1). The depth at 9 stations (stations 3, 5, 7, 9, 11, 13, 15, 17 and 19) varied from 0.5 to 2 m and it varied from 2 to 4.2 at 11 stations (stations 1, 2, 4, 6, 8, 10, 12, 14, 16, 18 and 20). Physicochemical analyses Temperature and pH were measured immediately in the field using a multiparameter kit (Multi 340 i/SET). Salinity was measured with a refractometer. Water transparency was measured with a Secchi disc. Samples for nutrient analyses were preserved immediately upon collection (−20 °C, in the dark). Nutrients (nitrite: NO2−, nitrate: NO3−, ammonium: NH4+, orthophosphate: PO43−, silicate: Si(OH)4), total nitrogen, and total phosphate (after transformation into NH4+ and PO43−, with nitrogen persulfate and potassium persulfate, respectively, at 120 °C) were analyzed by a Bran+Luebbe type 3 analyzer, and concentrations were determined colorimetrically according to Grasshof (1983). We also calculated the N/P:dissolved inorganic N (DIN) (DIN=NO2− +NO3− +NH4+) to dissolved inorganic P (DIP) (DIP=PO43−) ratio. The suspended matter concentrations were determined by measuring the dry weight of the residue after filtration onto Whatman GF/C membrane filters. Phytoplankton, chlorophyll-a, and ciliate collection For phytoplankton and ciliate analyses, seawater samples (1000 ml) were collected, as mentioned previously. After fixation with a Lugol (4 %) iodine solution (Bourrelly 1985), the samples were stored in the dark at low temperature until enumeration. Subsamples (50 ml) were enumerated under an inverted microscope, after settling for 24 to 48 h, using the method of Utermöhl (1958). The identification of algal taxa was made according to various keys (Tregouboff and Rose 1957; Huber-Pestalozzi 1968; Dodge 1985; Balech 1988; Tomas et al. 1996). Ciliates were counted and identified according to genus or species level with reference to the works of Alder (1999), Petz (1999), and Struder-Kypke and Montagnes (2002). Tintinnids were identified using lorica morphology and species description according to Balech (1959) and Kofoid and Campbell (1929, 1939). Cell numbers were expressed as cells per liter. Water samples (1000 ml), for chlorophyll-a analyses, were filtered by vacuum filtration onto a 0.7-mm pore size and
Author's personal copy Environ Sci Pollut Res Fig. 1 Geographical map focusing on the sampling stations in the southern coast of Sfax
Mediterranean Sea
37°
31° 8°
100 m
12°
47-mm-diameter glass fiber filter Whatman GF/F and immediately stored at −20 °C. Chlorophyll-a concentration was determined by spectrometry, after extraction of the pigments in acetone (90 %) and using the SCOR-UNESCO equations (UNESCO 1966).
i¼1
−∑ Ni
Ni N
log 2 NNi , where Ni/N is the frequency of species in the
sample and N is the total number of species in the community.
Statistical analysis Zooplankton collection Zooplankton was collected at the previously mentioned stations using a cylindroconical net (30 cm aperture, 100 cm height, 100 μm mesh size), equipped with a Hydro-Bios flowmeter. The net was towed obliquely from a depth near the bottom to the surface at each station at a mean speed of 1 m s−1 for 10 min. Zooplankton samples were rapidly preserved in 2 % buffered formaldehyde solution after collection and stored in the dark at 4 °C. For a zooplankton enumeration, subsamples were counted under a vertically mounted deepfocus dissecting microscope (Olympus TL 2) after being colored with Bengal pink, which allows to distinguish the organic matter from the inorganic matter and to facilitate the dissection of various appendices and of leg 5 of the different species. Zooplankton especially planktonic copepods were identified according to genus or species level based on the works of Rose (1933), Boltovskoy (1999), and Boxshall and Halsey (2004). The level of community structure was assessed with Shannon and Weaver’s (1949) H′ diversity index. H 0 ¼
Pearson’s rank correlation was performed using XL-Stat software to determine the correlations between the biological (phytoplankton, ciliate, and zooplankton) and the physicochemical parameters. The co-inertia analysis which is a direct extension of multiple regressions to the modeling of multivariate response matrix (Legendre and Legendre 1998) was performed to examine the correlation between an array of response variables (in this study, the sampling stations) and of independent explanatory variables (phytoplankton, ciliate, and mesozooplankton communities) conditional to a third matrix (here physicochemical parameters). Among the main axes for order and environmental variables, those that exhibit maximum covariance bring the top information to the observation description. This is the way to determine order and co-inertia axes from where observations are projected and provide evidence for similarities or differences between the different samples with respect to order or environmental variables. Computing and graphical displays were performed using R2.4 (R-Development Core Team 2006), the packages ade 41. 4.2 (Chessel et al. 2004), and vegan 1.8–3 (Oksanen et
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a
b
d
c
e
Fig. 2 Spatial variation of physical parameters: temperature (a), salinity (b), pH (c), transparency (d) and suspended matter (e) in sampled stations
al. 2011). Data matrices were explored using principal component analysis to picture the covariations between the 20 sampled stations and between phytoplankton, ciliates, mesozooplankton, and the physicochemical parameters.
Results Physicochemical parameters Water temperature ranged from 14 to 16.2 °C (mean±SD= 15.33±0.64 °C) (Fig. 2a). Temperature varied slightly among sampling sites. Salinity, which ranged from 39 to 40.1 psu (mean±SD=39.78±0.38), tended to stabilize over the spatial scale (Fig. 2b). The pH ranged from 6.79 (station 17) to 8.24 (station 10) (mean±SD=7.76±0.44) (Fig. 2c). Water transparency increased significantly from 0.8 (station 5) to 4.2 m (station 6) (mean±SD=2.4±1.25 m) (Fig. 2d). Concentrations of suspended matter varied significantly from 44 to 84 mg l−1 in station 16 and station 3, respectively (Fig. 2e). Suspended matter correlated negatively with water transparency (r= −0.353, n=20, p
