Distribution of ciliates in relation to environmental factors along the coastline of the Gulf of Gabes, Tunisia

Estuarine, Coastal and Shelf Science 83 (2009) 414–424

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Distribution of ciliates in relation to environmental factors along the coastline of the Gulf of Gabes, Tunisia Nouha Kchaou a, Jannet Elloumi a, Zaher Drira a, Asma Hamza b, Habib Ayadi a, Abderrahmen Bouain a, Lotfi Aleya c, * a

Universite´ de Sfax, Faculte´ des Sciences de Sfax, De´partement des Sciences de la Vie, Unite´ de recherche UR05ES05 Biodiversite´ et Ecosyste`me Aquatiques, Route soukra Km 3,5, BP 1171, CP 3000 Sfax, Tunisie Institut National des Sciences et Technologie de la Mer, Centre de Sfax, BP 1035, Sfax 3018, Tunisie c Universite´ de Franche-Comte´, Laboratoire de Chrono-Environnement, UMR CNRS 6249, 1, Place Leclerc, 25030 Besançon cedex, France b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 11 February 2009 Accepted 13 April 2009 Available online 22 April 2009

We studied the seasonal distribution of the ciliate community coupled with environmental factors along the coast at three stations sampled (from March 2006 to February 2007) in the Gulf of Gabes (Tunisia, Eastern Mediterranean Sea). A total of 56 species belonging to 11 orders, were identified. Harbor of Gabes station was more diversified (45 species) than both Tabia (26 species) and Karboub (31 species) stations. The ciliate assemblage was numerically dominated by Spirotrichea in Tabia (82% of the total abundance), in the Harbor of Gabes (86% of the total abundance), whereas, in Karboub, Spirotrichea represented only 40% of the total abundance. The unexpected lower quantitative importance of Spirotrichea in Karboub station was apparently the result of the high salt concentration found in water samples throughout the study, probably originating from the saline area surrounding Karboub station, known as Sabkha. The distribution of species in the nearshore of the Gulf of Gabes seemed most likely influenced by the combined effects of temperature, salinity and hydrographic conditions. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Gulf of Gabes nearshore ciliates Sabkha dynamics

1. Introduction Located in the Southern Eastern Tunisia, with an arid to semiarid climate, the Gulf of Gabes (NE Mediterranean, 33 N and 35 N) not only covers the most Tunisian prolific fish-producing area, but also shelters several stations for collecting seashells along its shores, as well as being a famous habitat for marines turtles (Baran and Kasparek, 1989; Maffucci et al., 2006). Despite its economic and wildlife conservational importance this Gulf is now strongly under stress from industrial activities, tourism and recreation (Hamza-Chaffai et al., 1997; Smaoui-Damak et al., 2003, 2006). A few studies have been conducted in the Gulf of Gabes focussing on the seasonal plankton food web structures such as the summer phytoplankton bloom (Bel Hassen et al., 2008; Drira et al., 2008) and copepod distribution (Drira et al., in press), but data on the distribution on a large scale of ciliate assemblages are lacking. In recent years, interest in the ecological role of marine planktonic ciliates has increased, and their importance in energy

* Corresponding author. E-mail address: lotfi[email protected] (L. Aleya). 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.04.019

transfer within food webs has been emphasized (Fenchel, 1988). Ciliate abundance in marine environments are under the control of zooplankton, particularly filter-feeding copepods (Lampert et al., 1986; Atkinson, 1996) as well as in the laboratory (Hartmann et al., 1993; Pe´rez et al., 1997). On the other hand, several findings have provided evidence that ciliates are important grazers on nanoplankton and bacterioplankton (Simek et al., 1997; Premke and Arndt, 2000). The study of the dynamics of ciliate species composition and standing stocks should thus provide valuable information on the functioning of aquatic ecosystems. Such studies are well documented in freshwater ecosystems (Beaver and Crisman, 1989; Aleya et al., 1992) and the western Mediterranean (Dolan and Marrase´, 1995; Pe´rez et al., 2000; Balkis, 2004) but are lacking for the northern eastern Mediterranean particularly along the nearshore of the Gulf of Gabes where more than 20 stations for collecting seashells are identified (Hamza-Chaffai et al., 1999). This area is currently undergoing extensive changes due to natural factors including sediment supply, sea-level rise and Sabkhas interference. Sabkha is an Arabic term for a coastal and inland saline mud flat built up by the deposition of silt, clay and sand in shallow, sometimes extensive, depressions (Warren, 2006). It is noteworthy that the

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

majority of studies on the ciliate community structure dealt with true plankton communities while very shallow coastal locations were poorly investigated. To our knowledge, there is no data on ciliates neither in very shallow coastal waters (<1 m depth) nor in the very shallow coastal waters that are submitted to Sabkha influence. In this context, it is important to start a survey of the protistan populations of this complex coastal region by answering to questions, such as what ciliates live here? Which types are numerically most important? Are there consistent seasonal variations? Addressing these questions may offer an opportunity to emphasize the importance of protozoa communities for the nearshore ecosystems, since their pelagic/benthic interface are likely to be complex with regenerated nutrients released from the sediment when disturbed (Verney et al., 2007). The aim of the work reported here is to explore the seasonal dynamics of ciliate assemblages and biomass and their relationships with environmental factors at three stations serving for collecting seashells along the coast of the Gulf of Gabes. These stations were likely to be significant sites because the first station is less influenced by the southern arid conditions than both the second, which is the subject of intense marine traffic inducing pollution (Drira et al., 2008) and the third station which is the saltiest as surrounded by a saline area called the Meider Sabkha. 2. Materials and methods 2.1. Study site This study was carried out in the Gulf of Gabes whose climate is dry (average precipitation: 210 mm) and sunny with strong easterly winds. The Gulf of Gabes (between 33 N and 35 N) extends from ‘‘Ras Kapoudia’’ at the 35 N parallel level to the Tunisian–Libyan border and shelters various islands (Kerkennah and Djerba) and lagoons (Bougrara and El Bibane) (Drira et al., 2008). 2.2. Sampling In this study, samples from three very shallow (<1 m) stations were taken monthly, between March 2006 and February 2007 (Fig. 1). Two replicates were taken on individual sampling dates. Given that there was almost no previous data on phytoplankton and ciliates along the nearshore of the Gulf of Gabes, sampling stations were selected with consideration of existing station locations for seashell collection, followed by field reconnaissance. We therefore selected three stations, Tabia station located at the north, the Harbor of the Gulf of Gabes in the center of the Gulf and Karboub station at the south. The third station is the saltiest as surrounded by the Meider Sabkha (Latitude 33 270 000 N, Longitude 10 450 000 E), forming a narrow belt along this station. Water samples were collected between 10 and 20 cm depth with a Van Dorm bottle. Samples for nutrient analyses were preserved immediately upon collection (20  C, in the dark), and those for ciliate enumeration (200 ml) were preserved with acid Lugol (2% final concentration) iodine solution and stored in the dark at low temperature (4  C) until analysis. 2.3. Physico-chemical variables Temperature and salinity were measured immediately after sampling using a multi-parameters kit (Multi 340 i/SET). Nutrients  þ 3 (NO 2 , NO3 , NH4 and PO4 ) and Total-nitrogen and Total-phosphate 3 (after transformation into NHþ 4 and PO4 , with nitrogen persulfate and potassium persulfate, respectively at 120  C) were analysed by with a BRAN and LUEBBE type 3 autoanalyser and concentrations

415

were determined colorimetrically using a UV-visible (6400/6405) spectrophotometer (APHA, 1992). 2.4. Phytoplankton and ciliate enumeration Phytoplankton and ciliate counts were made under an inverted microscope using the Utermo¨hl (1958) method. At least 200 ciliates were counted for each sample and were identified to genus or species level by consulting the works of Alder (1999), Petz (1999) and Stru¨der-Kypke and Montagnes (2002). Tintinnids were identified using lorica morphology and species description according to Balech, (1959) and Kofoid and Campbell (1929, 1939). The dimensions of 20–40 individual cells for each taxa were measured at 1250 magnification by image analysis. Mean biovolume of each taxon was estimated from appropriate geometric shapes. Ciliate biovolumes were estimated by geometric approximation and biomass values were calculated using the conversion factor of 0.19 pgC mm3 of biovolume (Putt and Stoecker, 1989) which corrected for shrinkage of Lugol’s iodine-fixed cells (Gifford and Caron, 2000). The phytoplankton community structure was studied by calculating the species diversity index H0 (bits cell1) (Shannon and Weaver, 1949).

H0 ¼ 

iX ¼1 ni

ni ni log2 N N

ni/N: is the frequency of species i in the sample N: number of species of the community

2.5. Statistical analyses The potential relationships between variables were tested by Pearson’s correlation coefficient. ANOVA analysis was applied to identify significant differences in physico-chemical and biological parameters between the sampled three stations. 3. Results 3.1. Physico-chemical parameters The physico-chemical parameters recorded in the three stations are summarized in Table 1. The average water temperature ranged between 13.6 and 32.3  C (Table 1). The lowest temperature (13.6  C) was recorded at Karboub station on February 2007, while the highest (32.3  C) at Tabia station on August 2006. In each station, the seasonal variation of the water temperature showed peak values (27.0–32.3  C) in July–early September and a minimum (13.6  C) in February (Fig. 1). Thermal stratification did not establish because of the shallowness of the sampled stations (<1 m). The highest water temperature was found in samples from Tabia (32.3  C), followed by Karboub (29.0  C) and Harbor of Gabes (27.0 C) (Table 1). The salinity varied from 34.5 on September, in the Harbor of Gabes to 47.4 on September, in the Karboub station and the seasonal changes of salinity were clear in stations Tabia and Karboub, following roughly those of temperature. The highest values were found in Karboub samples, most likely because this station is surrounded by a Sabkha which lead to a high significant difference between these three stations (F ¼ 117.16; df ¼ 33; p < 0.001) (Table 1). However, in the Harbor of Gabes, from March to September, the distribution of salinity did not display neither a clear pattern nor relationship with temperature, while during October to February salinity distributed similarly to temperature.

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

11 10 9 8 7 6 5 4 3 2 1 0

35

Temperature (°C)

30

20 15 10 5

Salinity

0

12 11 10 9 8 7 6 5 4 3 2 1 0

55 50 45 40 35 30 25 20 15 10 5 0 11 10 9 8 7 6 5 4 3 2 1 0

50 45 40 T-N (µmol. l-1 )

25

N-NO3-(µmol. l-1 )

P-PO43- (µmol. l - 1)

N-NH4+ (µmol .l

-1

)

416

35 30 25 20 15 10 5 0

a

3

2

Harbor of Gabes

Karboub

b

Tabia

Harbor of Gabes

Feb-07

Jan-07

Dec-06

Nov-06

Oct-06

Sep-06

Jun-06

May-06

Apr-06

Mar-06

Feb-07

Jan-07

Dec-06

Nov-06

Oct-06

Sep-06

Aug-06

0

Aug-06

1

Jul-06

N-NO2-(µmol. l -1) Tabia

Jul-06

Jun-06

May-06

Apr-06

Mar-06

T-P (µmol. l -1)

4 50 45 40 35 30 25 20 15 10 5 0

Karboub

Fig. 1. Seasonal distribution of physico-chemical parameters in the three sampled station (from above to below: Tabia, Harbor of Gabes and Karboub).

3.2. Nutritional conditions The annual means of the nutrient concentrations found in water samples of the three sampled stations are presented in Table 1. The minimum, maximum and means of nutrient concentrations of the three sampled stations are presented in Fig. 2 and Table 1. Totalnitrogen (T–N) concentrations varied between 4.9 mmol l1 on February 2007, in the Tabia station and 46.9 mmol l1 on August 2006, in the Harbor of Gabes station. On average, nitrogen consisted mainly of the dissolved organic form, with higher levels

(71  12.1%), in both the Tabia and Harbor of Gabes stations than in the Karboub station (56.8  15.3%). The dissolved inorganic form  þ (NO 2 þ NO3 þ NH4 ¼ DIN) represented (28.8  12.1%) of the Totalnitrogen, in both Tabia and Harbor of Gabes, and (43.2  15.3%) in Karboub contributing to a significant difference between these three studied areas (F ¼ 7.55; df ¼ 33; p < 0.01) (Table 1). Nitrate concentrations accounted for 49  18% of the total DIN, in Tabia followed by Karboub (38.1  16.8%) and Harbor of Gabes (36.0  22.3%). Ammonium concentrations accounted for 44  18% of the total DIN and nitrites 7  3% in all sampled stations.

Table 1 Min, max and annual mean  SD of biological and physico-chemical parameters in Tabia, Harbor of Gabes and Karboub stations. In the last column, results of one-way ANOVA analysis. F-value: between-groups mean square/ within-groups mean square. *Significant difference between sampled stations: (*p < 0.05, **p < 0.01, ***p < 0.001). Physico-chemical parameters

Tabia

Harbor of Gabes Max

16.26 36.74 0.64 0.17 0.30 2.60 4.93 0.40 2.40 2.56

32.35 39.20 4.21 0.66 3.49 6.92 30.21 1.87 20.29 8.61

Biological parameters Total ciliate abundance (cells l1) Spirotrichea abundance (cells l1) Prostomatea abundance (cells l1) Colpodea abundance (cells l1) Litostomatea abundance (cells l1) Oligohymenophorea abundance (cells l1) Heterotrichea abundance (cells l1) Karyorelectea abundance (cells l1) Other ciliate abundance (cells l1) Total ciliate biomass (mgC l1) Spirotrichea biomass (mgC l1) Prostomatea biomass (mgC l1) Colpodea biomass (mgC l1) Litostomatea biomass (mgC l1) Oligohymenophorea biomass (mgC l1) Other ciliates biomass (mgC l1) Karyorelectea (mgC l1) Heterotrichea (mgC l1)

33 0 0 0 0 0 0 0 0 0.011 0 0 0 0 0 0 0 0

5.6  103 5.6  103 3.67  102 2.33  102 50 17 0 0 33 5.62 5.47 0.11 0.15 0.02 0.04 0.05 0 0

Mean  SD

Min

Max

Mean  SD

F-values

Min

Max

23.45  5.00 37.61  0.62 2.33  1.02 0.32  0.14 2.09  0.91 4.74  1.30 18.43  6.11 0.83  0.38 6.70  5.28 6.41  2.09

14.78 34.55 0.51 0.08 0.52 1.82 11.85 0.10 2.62 0.71

27.05 37.80 8.95 1.45 9.49 14.63 46.91 10.26 39.24 1.01  102

20.87  3.90 36.77  1.00 2.65  2.62 0.57  0.46 4.05  2.50 7.28  4.03 25.52  10.74 2.25  2.73 11.50  11.27 15.80  29.45

13.60 41.65 1.83 0.15 0.55 3.14 12.58 0.26 2.25 2.91

29.05 47.40 4.01 2.22 10.04 14.08 35.71 1.08 5.21 48.61

0.98  103  1.65  103 1.08  103  1.64  103 30.58  1.05  102 19.41  67.26 6.91  16.55 1.41  4.90 0 0 4.83  11.41 1.29  1.75 1.38  1.68 0.01  0.03 0.01  0.04 0.002  0.005 0.003  0.01 0.007  0.017 0 0

1.7  102 100 0 0 0 0 0 0 0 0.38 0 0 0 0 0 0 0 0

2.1  103 2.1  103 63 2.25  102 1.25  102 50 0 0 67 9.56 8.79 0.07 0 0.03 0.30 0.14 0.13 0

9.4  102  7.42  102 8.51  102  6.95  102 7.33  18.94 23.58  64.43 22.91  48.21 8.75  15.68 0 0 13.91  25.52 1.92  3.76 1.78  2.54 0.01  0.02 0 0.002  0.01 0.05  0.11 0.02  0.04 0.02  0.04 0

25 0 0 0 0 0 0 0 0 0.01 0 0 0 0 0 0 0 0

50.35  103 2.29  104 1.36  104 50 7.5  103 8  103 6.3  103 2.25  103 75 70.4 10.7 4.03 0.03 2.66 3.22 0.53 5.8 53

Mean  SD 21.07  4.54 44.69  2.10 3.20  0.67 0.78  0.71 5.59  2.72 9.59  3.14 23.06  6.12 0.51  0.27 4.21  1.07 24.52  14.42 6.29  103  14.24  103 2.30  103  6.50  103 1.15   103  3.93  103 4.16  14.43 7.04  102  2.15  103 1.12  103  2.47  103 5.25  102  1.81  103 3.81  102  7.55  103 8.33  22.19 8.7  19.85 2.15  4.01 0.34  1.16 0.002  0.009 0.25  0.76 0.49  0.99 0.064  0.16 0.98  1.95 4.41  15.3

1.22 117.16 0.84 2.54 7.64 7.55 2.45 4.01 3.17 2,73 0.48 0.98 0.79 1.25 2.97 1 2.98 0.55 1.04 1.01 1 0.79 1.28 2.66 1.11 2.98 1 1.22

(33) (33)*** (33) (33) (33)** (33)** (33) (33)* (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33) (33)

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

Min Temperature ( C) Salinity 1 N–NO 3 (mmol l ) 1 N–NO 2 (mmol l ) 1 ) N–NHþ 4 (mmol l DIN (mmol l1) Total-N (mmol l1) 1 P–PO3 4 (mmol l ) Total-P (mmol l1) N/P ratio

Karboub

417

NO3-/NH4+

110 100 90 80 70 60 50 40 30 20 10 0 Feb-07

Jan-07

Dec-06

Nov-06

Oct-06

Sep-06

Aug-06

Jul-06

Jun-06

Apr-06

May-06

Mar-06

NO3-/NH4+ ratio

Karboub

110 100 90 80 70 60 50 40 30 20 10 0

N/P ratio

9 8 7 6 5 4 3 2 1 0

Harbor of Gabes

110 100 90 80 70 60 50 40 30 20 10 0

N/P ratio

9 8 7 6 5 4 3 2 1 0

Tabia

N/P ratio

9 8 7 6 5 4 3 2 1 0

NO3-/NH4+ ratio

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

NO3-/NH4+ ratio

418

N/P

 þ 3þ  þ Fig. 2. Seasonal distribution of N/P (NO 2 þ NO3 þ NH4 /PO4 ) and NO3 /NH4 ratios in the three sampled stations.

Orthophosphate concentrations represented 19.1  9% of the total phosphorus in the Harbor of Gabes, followed by the Tabia station (17.6  10%) and the Karboub station (12.8  6.6%). The N/P ratio (Redfield) ranged between 0.7, in the Harbor of Gabes, on January 2007 and 101.3 on October 2006, also in the Harbor of Gabes þ (Fig. 2). The NO 3 /NH4 ratio ranged between 0.05 in October 2006 of the Harbor of Gabes station and 8.64 in December 2006 at Tabia station (Fig. 2). Opposed trends in the distribution of these two þ ratios (N/P and NO 3 /NH4 ) were found in all the three sampled stations (Fig. 2). 3.3. Species composition, distribution and succession of the ciliate community in three stations 3.3.1. Species composition A summary of the ciliate taxa observed during the entire study period at the three sampling sites is given in Table 2. A total of 56 species belonging 11 orders, namely Strombidiida, Choreotrichida, Tintinnida, Euplotida, Prostomatida, Colpodida, Haptorida, Philasterida, Sessilida, Loxodida and Heterotichida were identified. A number of taxa (13 species) were identified only to generic level, but it was not possible to subscribe specific identities to three naked specimens. The Harbor of Gabes station was more diversified (45 species) than both the Tabia (26 species) and the Karboub

(31 species) stations. In general the ciliate assemblage was numerically dominated by Spirotrichea in Tabia (82% of the total abundance), in the Harbor of Gabes (86% of the total abundance), whereas in Karboub Spirotrichea represented only 40% (Fig. 3). The mean abundance and biomass values for each ciliate class recorded during the entire study period at the three sampling areas were summarized in Table 1. The most abundant Spirotrichea were tintinnids. In Tabia, tintinnida (69% of the total abundance) were numerically dominated by the genus Tintinnopsis (eight species) followed by the genus Tintinnidium (one species). In the Harbor of Gabes, we also found Tintinnopsis (nine species), but followed by the genus Codonella (four species). In the Karboub station, tintinnids were not dominant (0.7% of the total abundance) and were represented by the genera Tintinnopsis (three species), Tintinnidium (two species), Codonaria (one species), Codonella (one species), Eutintinnus (one species) and Helicostomella (one species). In the Tabia station, Spirotrichea naked ciliates (69.1% of the total abundance) were largely dominated by the species Strobilidium neptuni (64.6% of the total abundance). In the Harbor of Gabes station, they represented 50.1% of the total abundance, and were dominated also by the species S. neptuni (20.6% of the total abundance). In the Karboub station, Spirotrichea naked ciliates (35.84% of the total abundance) were largely dominated by the species Leegaardiella sol (31.4% of the total abundance) (Table 2). Other naked ciliates were frequently observed but were usually in very low numbers in the Tabia and Harbor of Gabes stations. However, in Karboub, we found substantial percentages of Prostomatea (18.3% of the total abundance), Oligohymenophorea (19.2% of the total abundance), Litostomatea (11.2% of the total abundance) and Heterotrichea (8.3% of the total abundance) with Fabrea salina being the only Heterotrichea present throughout samplings (Table 2). In this study, a few species were recognized as mixotrophic (Lohmanniella oviformis, Strombidium acutum and Strombidium conicum), or autotrophic (Mesodinium rubrum) or benthic (Urotricha sp., Euplotes sp. and Aspidisca lynceus) (Table 1). 3.3.2. Distribution and succession of ciliates 3.3.2.1. Tabia station. Ciliate abundance ranged from 33 to 5.6  103 cells l1 (mean  SD ¼ 0.98  103  1.65  103 cells l1), and the biomass varied from 0.01 to 5.6 mgC l1 (mean  SD ¼ 1.3  1.7 mgC l1). There were three peaks, in March, June and especially in August while both lowest density and biomass occurred during the wet period (October–February) (Fig. 4). The Choreotrichida, Strobilidium neptuni was responsible for the exceptional peak that occurred in August, accounting for 97.3% of the total Spirotrichea. Although, the tintinnida, Ascampbeliella obscura (loricate Spirotrichea) contributed very little to ciliate abundance in August, it was responsible for the maximum biomass (5.6 mgC l1) recorded in water samples (Fig. 5), most likely relatable to its large lorica (length: 67 mm, diameter: 50 mm). The tintinnida, Tintinnopsis cylindrica (30.1% of the total abundance) and the tintinnid Tintinnidium balechi (87.5% of the total abundance) accounted for the March and June peaks. 3.3.2.2. Harbor of Gabes station. In this station, Spirotrichea occurred on June, August, September, November and December, while the other taxonomic groups had disappeared from water samples (Fig. 3). Ciliate abundance fluctuated between 1.7  102 and 2.1  103 cells l1 (mean  SD ¼ 9.4  102  7.4  102 cells l1), and the biomass varied from 0.38 to 9.56 mgC l1 (mean  SD ¼ 1.9  3.7 mgC l1). Ciliate abundance and biomass increased gradually from March to early summer reaching a peak of 1.8  103 cells l1 and 9 mgC l1, associated with the development of the two tintinnida Tintinnopsis cylindrica and Tintinnopsis beroidea. Then, a sharp decrease of abundance and biomass occurred in July

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

419

Table 2 Species composition, mean length and biovolume of the ciliate community in the three stations (Tabia, Harbor of Gabes and Karboub). A: autotrophic ciliates, B: benthic ciliates, M: mixotrophic ciliates. Class

Subclass

Order

Species

Mean length (mm)

Biovolume (103 mm3)

Ciliates abundance (% of the total abundance) Tabia

Harbor of Gabes

Karboub

Spirotrichea Oligotrichia Strombidiida Strombidium Strombidium Strombidium Strombidium Strombidium Strombidium Strombidium

capitatum acutumM conicumM wulffi antarcticum compressum diversum

37 35 49 38 31 41 25

7.1 6.4 8.5 3.9 3.0 9.5 2.0

0.1 0.4 1.0 0.0 0.0 0.0 0.0

0.9 1.8 0.7 0.2 0.3 0.2 0.3

0.1 0.6 0.03 0.0 0.0 0.1 0.0

74 27 22 17 20

28.5 3.6 2.4 1.1 1.3

0.5 64.6 0.4 1.5 0.5

0.0 20.6 4.9 15.9 2.5

0.0 0.01 31.4 1.1 0.1

33 86 29 41 43 28 39 17 55 27 123 40 21 162 67 83 33 60 50 43 67 23 25 46 100 100 83 68

10.9 64.0 9.9 11.4 10.9 4.7 11.4 2.1 30.3 5.5 14.3 3.8 2.2 20.6 60.3 91.8 10.2 29.7 40.6 56.1 73.5 3.3 3.2 48.2 209.2 20.8 1.0 7.5

10.8 0.0 0.2 3.7 5.8 0.2 1.1 0.4 1.0 0.0 0.0 0.0 0.2 0.2 1.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

10.5 0.9 0.9 4.2 5.7 0.0 4.2 0.6 0.7 2.2 0.3 1.7 0.0 1.5 0.0 0.2 0.9 0.7 0.7 0.7 1.3 0.4 0.6 0.0 0.6 1.3 0.9 0.0

0.1 0.1 0.0 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.02 0.0 0.03 0.0 0.0 0.0 0.1

Euplotes sp.B Euplotes charon

35 60

15.1 52.7

0.1 0.0

0.0 1.8

0.1 2.3

Urotricha sp.B Balanion sp.

19 23

1.6 2.2

2.7 0.0

2.5 0.0

18.3 0.1

Colpoda sp.

27

3.3

1.7

0.0

0.1

Enchelyodon sp. Mesodinium rubrumA

59 25

3.5 1.9

0.0 0.6

0.1 0.7

0.0 11.2

Philasterine sp. Uronema marinum

48 25

12.8 2.1

0.1 0.0

1.1 1.1

0.1 19.2

238

47.2

0.0

0.2

Choreotrichia Choreotrichida Strombidinopsis acuminatum Strobilidium neptuni Leegaardiella sol Lohmanniella oviformisM Halteria sp. Tintinnida Tintinnidium balechi Tintinnidium sp. Tintinnopsis compressa Tintinnopsis nana Tintinnopsis cylindrica Tintinnopsis parva Tintinnopsis beroidea Tintinnopsis fimbriata Tintinnopsis lobiancoi Tintinnopsis parvula Tintinnopsis radix Tintinnopsis tocantinensis Tintinnopsis sp. Helicostomella subulata Ascampbeliella obscura Codonellopsis balechi Codonellopsis obesa Codonellopsis orthoceras Codonellopsis brasiliensis Codonella perforata Codonella amphorella Codonella galea Codonella cratera Codonaria sp. Favella serrata Ormosella acantharus Salpingella sp. Eutintinnus fraknoi Hypotrichia Euplodida

Prostomatea Prostomatida

Colpodea Colpodida Litostomatea Haptoria Haptorida

Oligohymenophorea Scuticociliatia Philasterida

Peritrichia Sessilida Vorticella sp.

0.0 (continued on next page)

420

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

Table 2 (continued ) Class

Subclass

Order

Species

Biovolume (103 mm3)

Mean length (mm)

Ciliates abundance (% of the total abundance) Tabia

Harbor of Gabes

Karboub

Karyorelectea Loxodida Aspidisca lynceusB

48

13.6

0.0

0.9

6.1

Fabrea salina

75

44.3

0.0

0.0

8.3

38 33 38 75 85 175 43

6.1 2.7 14.8 49.1 47.3 701.2 10.6

0.2 0.0 0.0 0.0 0.2 0.0 0.0

0.4 0.6 0.4 0.0 0.0 0.0 0.0

0.03 0.0

Heterotrichea Heterotrichida Others ciliates Monodinium sp. Tiarina fusus Urozona buetschlii Dysteria compressa sp1. sp2. sp3.

Spirotrichea

Litostomatea

Oligohymenophorea

Heterotrichea

Colpodea

Other ciliates

Prostomatea

Karyorelectea

Fig. 3. Relative contribution of ciliates groups to total ciliates abundance (a) and biomass (b) in the three sampled stations.

Jan-07

Feb-07

Dec-06

Oct-06

20

Nov-06

20

Sep-06

20

Jun-06

40

Apr-06

40

May-06

40

Mar-06

60

Jan-07

60

Feb-07

60

Dec-06

80

Oct-06

80

Nov-06

80

Sep-06

100

Aug-06

100

Jul-06

100

Jun-06

20

Apr-06

20

May-06

20

Mar-06

40

Jan-07

40

Feb-07

40

Dec-06

60

Oct-06

60

Nov-06

60

Sep-06

80

Jul-06

80

Aug-06

80

Jun-06

100

Apr-06

100

May-06

100

Jul-06

Karboub

Harbor of Gabes

Aug-06

3.3.2.3. Karboub station. Ciliate abundance varied from 25 to 50.3  103 cells l1 (mean  SD ¼ 6.29  103  14.2  103 cells l1), l1 and the biomass from 0.01 to 70.4  103 mgC

Mar-06

0.03 0.03

(mean  SD ¼ 8.7  103  19.95  103 mgC l1). There were four peaks, in June, August and especially in October and January (Fig. 4). The Oligohymenophorea Uronema marinum, was responsible for the peaks that occurred in June and October, accounting for 99.5 and 75% of the total abundance respectively, whereas the Karyorelectea Aspidisca lynceus and the Spirotrichea Euplotes charon accounted together for the relatively less important August peak. The Spirotrichea Leegaardiella sol, the Litostomatea Mesodinium rubrum, the Prostomatea Urotricha sp. and the Heterotrichea Fabrea salina were responsible for the January exceptional peak, accounting for 45.3, 15, 27.1 and 12.5% of the total abundance respectively. We should notice that F. salina was found only in Karboub station. The diversity index (H0 ) varied between the three stations (Fig. 5). The higher values are observed at the Harbor of Gabes

(Fig. 4). Soon after, the biomass decreased while the abundance increased to reach its maximum (2.1  103 cells l1), in August. The decrease in biomass was related to the decline of the Karyorelectea Aspidisca lynceus and the tintinnid genera Tintinnidium and Tintinnopsis, and the peak of abundance was associated with the growth of the Choreotrichida Strobilidium neptuni, which accounted for 62% of the total abundance in August. From October 2006 to February 2007, both abundance and biomass were low (Fig. 4). Despite the uncoupling of abundance from biomass, observed from July to September, both factors were overall significantly correlated (Pearson’s r ¼ 0.67; n ¼ 18; p < 0.05).

Tabia

0.03

4. Discussion

14 12 10 8 4 2

Abundance

Feb-07

Jan-07

Dec-06

Nov-06

Oct-06

Sep-06

Aug-06

Jul-06

Jun-06

May-06

Apr-06

Mar-06

0

Biomass

Fig. 4. Seasonal distribution of the ciliate total abundance and biomass in the three sampled stations.

4 3.5 3 2.5 2 1.5

Tabia

Harbor of Gabes

0

Harbor of Gabes

90

12

80 10 70 60

8

50 6 40 30

4

20 2 10 0

0

Karboub

90

92.5 × 103

50.4 × 103

80

12 10

70

8

60 50

6

40

4

30 20

2

10 0

0

Mar-06 Feb-07

Jan-07

Dec-06

Nov-06

Oct-06

Sep-06

Aug-06

Jun-06

May-06

Apr-06

0

Jul-06

1 0.5 Mar-06

H' (bits. cell -1)

4.5

0

Ciliates abundances (×103 cells. l-1)

station (3.8 bits cell1). However, the lowest are observed at the Karboub station (0 bits cell1). These results indicate that Harbor of Gabes is more diversified than Tabia and Karboub station (45, 26 and 31 species, respectively).

2

10

Ciliates abundances (×103 cells. l-1)

6

20

Feb-07

70.4

4

30

Jan-07

18 16

6

40

Dec-06

20

Nov-06

50.3 × 103

50

Oct-06

Karboub

12 11 10 9 8 7 6 5 4 3 2 1 0

8

60

Sep-06

0

Jul-06

2

10

70

Aug-06

4

12

80

Jun-06

6

Tabia

90

May-06

8

Apr-06

12 10

Diatoms, dinoflagellates and other phytoplankton abundances ( ×103 cells. l -1)

14

The seasonal cycle in temperature in the three sampled stations is typical for the arid to semi-arid zone of the northern hemisphere

Diatoms, dinoflagellates and other phytoplankton abundances ( ×103 cells. l -1)

16

Diatoms, dinoflagellates and other phytoplankton abundances ( ×103 cells. l -1)

20 18

The phytoplankton community of the Gabes Gulf was dominated by diatoms and dinoflagellates. Total phytoplankton abundance varied from 0.7  103 cells l1 in Tabia station during July 2006 to 92.5  103 cells l1 in Karboub station during November 2006. In Tabia and Harbor of Gabes stations, diatoms dominated the phytoplankton community, contrary to Karboub station which was dominated by dinoflagellates (Fig. 6), chiefly Karenia selliformis during Mai 2006, November 2006 and January 2007 (Fig. 6).

Ciliates abundances (×103 cells. l-1)

Ciliate abundance (×10 3 cells. l-1)

Harbor of Gabes

421

3.4. Phytoplankton composition

Ciliate biomass (µgC. l-1 )

Ciliate abundance (×10 3 cells. l-1)

20 18 16 14 12 10 8 6 4 2 0

Ciliate biomass (µgC. l-1 )

11 10 9 8 7 6 5 4 3 2 1 0

Tabia

Ciliate biomass (µgC. l-1 )

11 10 9 8 7 6 5 4 3 2 1 0

Ciliate abundance (×10 3 cells. l-1)

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

Diatoms

Dinoflagellates

Other phytoplankton

Ciliate abundance

Karboub

Fig. 5. Diversity index (H0 ) at the three stations.

Fig. 6. Seasonal distribution of the major class of phytoplankton and total ciliate abundance in the three sampled stations.

422

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

(Alaoui and Aleya, 1995; Bel Hassen et al., 2009), with a warming starting in spring and a maximum at the end of July to early August, followed by a cooling and a seasonal minimum in January. The salinity of the water increased concomitantly with the increase in temperature. The salinity in the Karboub station was similar to that encountered in the first ponds of the Sfax saltern (Abid et al., 2008; Ayadi et al., 2008) and in other salt marshes (Segal et al., 2006; Evagelopoulos et al., 2007). However, it was higher than those recorded in coastal (<50 m deep) and oceanic (>50 m deep) (37, Hannachi et al., 2009; Bel Hassen et al., 2009), in other Mediterranean coastal environments (Dolan and Marrase´, 1995; Polat, 2007) and in hypo- and mesohaline lakes (Williams, 1998). The low orthophosphate concentrations as well as their low magnitude relative to total phosphorus (Fig. 1) and the resulting high N/P ratios (>16 Redfield ratio), suggest that P availability was at times the limiting element for algal growth. On the other hand, accumulation of P may be minimal in water systems, with rapid flushing, and with sandy bottom sediments such as those found in the three sampled stations. Despite this limitation, diatoms and dinoflagellates sustained high developments similar to those obtained in the first ponds of the Sfax saltern (Abid et al., 2008; Ayadi et al., 2008) and from cultivated species acclimated over the same salinity range (Zhang et al., 2001). Our study indicates that two distinct areas should be differentiated along the cost line of the Gulf of Gabes. The Tabia and Harbor of Gabes stations, with the highest contribution of Spirotrichea to the ciliate total abundance (94.3 and 91.8% of the total abundance) and biomass (97.5 and 95.6% of the total biomass), respectively, and the Karboub station with the lowest values (36.6% of the total abundance and 98.4% of the total biomass). The prevalence in the first area of Spirotrichea was also reported from true planktonic ciliate communties in the oligotrophic Western Mediterranean (Dolan and Marrase´, 1995; Pe´rez et al., 2000; Balkis, 2004) as well as in other environments such as the Baltic Sea (Johansson et al., 2004), in an Atlantic coastal pond and in Northern Eastern Brazil (Nogueira et al., 2005). In addition, the spirotrichous species found in this survey were as large as those reported from typical oligotrophic waters (Abboud-Abi Saab, 1989; Gilron et al., 1991; Dolan, 2000). This may question the idea that spirotrichous species are indicators of oligotrophic waters (Abboud-Abi Saab, 1989; Gilron et al., 1991; Dolan, 2000; Hannachi et al., 2009), being capable of exploiting lower minimum food concentrations (Pe´rez et al., 1997; Modigh and Castaldo, 2002). Our assumption may be supported by the fact that the present study sampled shallow disturbed waters, with regenerated nutrients released from the sediment when disturbed. These very shallow environments might be truly meso-eutrophic contrasting with the oligotrophic status of this area, with pelagic chlorophyll-a concentrations averaging 69.9  220.8 ng l1 (Drira et al., 2008; Bel Hassen et al., 2009). The above observations suggest that factors other than temperature and nutrients influenced the ciliate species succession in these stations making comparisons with studies cited from elsewhere in the Mediterranean (Dolan and Marrase´, 1995; Pe´rez et al., 2000; Balkis, 2004; Hannachi et al., 2009) unjustified. These stations were frequently submitted to easterly winds and are also among the breeding sites of many Mediterranean water birds (Diawara et al., 2007). For example, it is common to see within this area the Greater Flamingo (Phoenicopterus roseus) and other waders. The presence of some non-typically planktonic ciliates (Euplotes sp., Aspidisca lynceus and Urotricha sp.) in our samples was probably due to recurrent mechanisms of resuspension, most likely induced by wind and sea bird activity (Masselink and Russell, 2006). This assumption is supported by the presence in the same samples of some typically benthic diatoms (Nitzchia sp., Gyrosigma sp.) and cysts of planktonic dinoflagellates (Protoperidinium sp., Alexandrium sp., Karenia selliformis).

The lower quantitative importance of Spirotrichea in the second area (Karboub station) was expected and was apparently the result of the high salt concentration found in water samples throughout the study, probably originating from the extended flat and very saline area surrounding the Karboub station, and known as Sabkha El Meider. Although a large set of data has been accumulated on the abundance of the different ciliate populations throughout the world ocean, their dynamics in a very shallow nearshore location close to a Sabkha remain poorly characterised. The seasonal evolution of these communities is driven by a variety of factors that act at different time and spatial scales (Barth and Boer, 2002). The high salt concentration found in water samples throughout the study is the clearest evidence of the Sabkha El Meider influence on Karboub ecosystem. Until recently, ephemeral marine and continental floodwaters covering Sabkhas are thought to be the major suppliers of ions to salts. However, new findings indicated that deeply circulating resurging continental groundwater is the major supplier of salts to the Sabkhas, and, substantial inputs of saline waters into the nearshore probably due to ground water infiltration might occur. This is at least supported by two observations. First is the average salt concentration 44.7 (range: 41.6–47.2) found in the Karboub station, which was higher than that recorded elsewhere along the coastline (<1 m depth) (average 37, Kchaou et al., unpublished), in coastal (<50 m deep) and oceanic (>50 m deep) (37, Bel Hassen et al., 2009; Hannachi et al., 2009) of the Gabes Gulf, but close to that reported in several primary ponds of the Sfax multi-pond solar saltern (Elloumi et al., 2008) located in the central part of the Gulf. Second is the presence at substantial amounts (9.2% of the ciliate total abundance), occasionally in January (over flood conditions) in Karboub samples of halotolerant Heterotichea Fabrea salina, which, for instance, were also found in abundance in the primary ponds of the Sfax saltern (Elloumi et al., 2008), but at higher salinities (range 80–200). This change in the ambient salinity resulted in smaller Fabrea in Karboub station (length ¼ 75 mm, biovolume ¼ 44.3 mm3) than in the Sfax saltern (length ¼ 111 mm, biovolume ¼ 108.1 mm3) (Elloumi et al., 2006, 2008). We make the hypothesis that the size of F. salina might have been indirectly rather than directly related to salinity. Indeed, among potentials preys of F. salina, autotrophic picoplankton (Estrada et al., 2004; Evagelopoulos et al., 2007) and especially the salt-loving Chlorophyta Dunaliella salina are the most important (Oren, 2005). The typical halophile heterotrich ciliate F. salina is large-sized (Das Sarma and Arora, 2002) and flourish beyond 150 salinity (Elloumi et al., 2009), concomitantly to its preferred prey D. salina (Williams, 1998; Estrada et al., 2004; Kipriyanova et al., 2007; Abid et al., 2008). Heterotrichous ciliates in high-salt environments are known sometimes to feed exclusively on Dunaliella (Post et al., 1983). We showed, for instance, from parallel experiments conducted in our laboratory (Guermazi et al., 2008) and in the Sfax saltern (Elloumi et al., 2006, 2008), that because of its high nutritional value, D. salina is the primary prey of F. salina (Guermazi et al., 2008). Similar observations were reported from in vitro (Pandey and Yeragi, 2004), and from field (Post et al., 1983) experiments. This may help explain the small size of Fabrea found in the Karboub Dunaliella-free station. Other potential preys might be autotrophic picoeukaryotes (Estrada et al., 2004) and pigmented nanoflagellates that seem to be common as moderate halophiles in saline waters (Evagelopoulos et al., 2007; Elloumi et al., 2009). In conclusion, we believe that starting studies of the ciliate dynamics along the coastline of the Gulf of Gabes is very challenging, and feel that we have made a bold attempt because the pelagic/benthic interface is likely to be complex as shown by the contrasting results found in this study and in reported true pelagic marine ecosystems. Nevertheless, we were able to observe a seasonal variation in the ciliate community with higher

N. Kchaou et al. / Estuarine, Coastal and Shelf Science 83 (2009) 414–424

abundance and biomass found in the samples collected during the warm season. While the tintinnid community found in many marine areas often display a broad trophic diversity (Perriss et al., 1995; Dolan, 2000), only two tintinnids (Tintinnopsis sp. and Tintinnidium sp.) were found either in the Karboub station or Sfax saltern (Elloumi et al., 2006, 2009). This result suggests that these species performed better than other tintinnids probably owing to more flexible adaptive strategies (Aleya, 1991; Reynolds, 1997). Additionally, ciliates could serve as good bioindicators in detecting the salty input coming from areas such as Sabkha or brackish springs into the coastal waters. Obviously, this approach is more resource intensive than the use of an electronic salinity meter. Ciliate species appear to be cosmopolitan in distribution with high numbers recorded in both tropical and polar environments (Perriss et al., 1995), and the main determinant of distribution (and certainly of abundance) is probably the direct effect of predation pressure and prey availability. Temperature will affect ciliates indirectly via its influence on prey growth; but even so seasonal light availability will be a more important indirect factor (Aleya, et al., 1992; Perriss and Laybourn-Parry, 1997; Sherr et al., 2003). Our findings are therefore tentative and suggest that, factors other than temperature (e.g. salinity, prey availability) were implicated in the environmental forcing of the ciliate species composition in the nearshore of typical arid to semi-arid coastal environments. The potential role of ciliates as predators of phytoplankton and bacteria but also as potential prey for filter-feeding copepods should be further addressed.

Acknowledgements This study was conducted in the framework of PhD cotutelage of Kchaou Nouha (University of Franche-Comte´, Chrono-Environnement UMR CNRS 6249, France-University of Sfax, Tunisia). We thank one anonymous reviewer for providing helpful suggestions for improvement. This work was supported by the Tunisian funded project REPHY conducted in the National Institute of Marine Sciences and Technologies (INSTM) of Sfax. The authors wish to thank M. Mahfoudhi and H. Sahraoui for technical help.

Appendix A. Supplemental material Supplementary information for this manuscript can be downloaded at doi: 10.1016/j.ecss.2009.04.019.

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