Screening for alien and harmful planktonic species in the Gulf of Gabes (Tunisia, Southeastern Mediterranean Sea)

Accepted Manuscript Screening for alien and harmful planktonic species in the Gulf of Gabes (Tunisia, Southeastern Mediterranean Sea) Amel Ben Rejeb Jenhani, Afef Fathalli, Hachem Ben Naceur, Dhekra Hayouni, Jaafer Aouani, Mohamed Salah Romdhane

PII: DOI: Article number: Reference:

S2352-4855(18)30332-3 https://doi.org/10.1016/j.rsma.2019.100526 100526 RSMA 100526

To appear in:

Regional Studies in Marine Science

Received date : 30 July 2018 Revised date : 27 January 2019 Accepted date : 6 February 2019 Please cite this article as: A.B.R. Jenhani, A. Fathalli, H.B. Naceur et al., Screening for alien and harmful planktonic species in the Gulf of Gabes (Tunisia, Southeastern Mediterranean Sea). Regional Studies in Marine Science (2019), https://doi.org/10.1016/j.rsma.2019.100526 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Screening for alien and harmful planktonic species in the Gulf of Gabes (Tunisia, Southeastern Mediterranean Sea)

Amel Ben Rejeb Jenhani1, Afef Fathalli* 1,2, Hachem Ben Naceur 1, Dhekra Hayouni 1, Jaafer Aouani 3, Mohamed Salah Romdhane 1

1

Unité de Recherche Ecosystèmes et Ressources Aquatiques, Institut National Agronomique de

Tunisie, 43, Avenue Charles-Nicolle, 1082 Tunis Mahrajène, Tunisia. Fax: 00 216 71 799 391 2

Institut National des Sciences et Technologie de la Mer, Port de pèche-2060 La Goulette, Tunis,

Tunisia 3

SERAH/ SOTINFOR, Tunis, Tunisia.

* Corresponding author, e-mail address: [email protected]

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Abstract The Gulf of Gabes, pole of shellfish production in Tunisia, is known by a great maritime traffic. The objective of the present study is to update the planktonic organisms listing and to screen alien and harmful planktonic species in the Gulf. The investigations, conducted in the four commercial ports of the Gulf of Gabes, in 2010, revealed the presence of 138 phytoplankton taxa dominated by the Dinophyceae and Bacillariophyceae and 37 Dinophyceae rest forms from which 17 were not found in their active form. Among the alien phytoplankton species in the Mediterranean, we identified 4 species in water and 6 Dinophyceae cysts taxa in sediments of the Gulf of Gabes.The four encysted forms of potentially toxic dinoflagellates, detected in this work, were wholly non-indigenous species. Eleven known harmful phytoplanktonic species, including 2 native species of Diatoms (Chaetoceros socialis and Pseudo-nitzschia sp.) and 9 Dinophyceae including the non-indigenous species Alexandrium minutum and Karenia selliformis were found during this study. The qualitative analysis of zooplankton in the gulf of Gabes showed the common presence of 21 groups which the most important is copepods. It revealed also the presence of the two Alien species Acartia (Acanthacartia) bifilosa and Paracartia (Acartia) grani.

Key words: Dinophyceae cysts, harmful species, invasive species, Plankton.

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1. Introduction Alien species, also known as exotic, introduced, invasive, non-indigenous, or non-native (Occhipinti-Ambrogi & Galil, 2004), are species that are brought to a place well-separated in time and place from its native range where they are able to reproduce and establish a population (Boudouresque and Verlaque, 2002). This may be caused directly or indirectly by human activity (Raaymakers, 2002). The non indigenous species have become a hot issue in recent decades in particular in the Mediterranean Sea. In most definitions the term “invasive aliens” is associated with adverse effects, threatening native biological diversity, the ecological stability of the invaded ecosystems, the resulting economic consequences and even human health (Katsanevakis et al., 2014). Some authors consider the spread of “invasive” species and climate change as the two major threats to biodiversity in the marine environment (Dukes, 2003). A list of the “100 Worst Invasives” in the Mediterranean has been compiled by Streftaris and Zenetos (2006). According to Zenetos (2010), the number of reported alien species in the Mediterranean reached 903 by April 2008 and 947 by October 2009 and this author suggests a rate of introduction of 1 species every 9 days in the period January 2006 to April 2008 (94 species in total) while the estimate of Galil (2009) is of 573 species, 80 species introduced in the period 2000-2007 with a rate of 10 new non-indigenous species per year in the last 20 years. The highest number of species belong to zoobenthos (473) followed by fish (125) phytobenthos (124), phytoplankton (60), zooplankton (52), foraminifera (49) and parasites (21) (Zenetos et al., 2010). For many years, fouling was the main responsible of species transports but recently attention has been devoted to organisms carried by ballast water. Up to 10 billion tonnes of ballast water and several thousand of species are transported every day. Lenz et al. (2000) has counted 50.000 zooplankton organisms and 110 million of phytoplankton per m-3 in the ballast waters. Estimates of 150 to 22 500 cysts m-3 of ballast sediment were made (Hallegraeff and Bolch, 1992). Cysts as well as 3

resting cells of diatoms can survive very harsh conditions, including anoxia, and can remain viable for 10 to 20 or more years (McQuoid et al., 2002). The introduction modes of species in the Mediterranean are more or less known and some species seem to be introduced by several vectors (Galil et al., 2014; Katsanevakis et al., 2014). In fact, the Suez Canal and navigation appear as major vectors of dispersion with 52% for the Suez Canal and 20% for navigation that allows especially the introduction of planktonic species via ballast water. In the Mediterranean, the species introduction can also be done by other ways: 11% aquaculture, 10% unknown, 6% Gibraltar, and 1% other (Streftaris et al., 2005). Galil (2008) confirmed that the majority of aliens in the eastern Mediterranean entered through the Suez Canal, whereas mariculture and shipping are powerful means of introduction in the northwestern Mediterranean. Most aliens are thermophilic species. The coastline of Tunisia spans the transition between Eastern and Western basins and therefore is a key area for understanding the progression of alien species in the Mediterranean as a whole. Thereby, monitoring programmes on spatio-temporal structures of communities particularly in the hot spot areas for aliens such as harbours and polluted waters should be undertaken. The southeast coast of Tunisia has rich aquatic resources accounting for approximately 65% of the country’s fish production (DGPA, 2005- 2009). Various pollutants from liquid and solid wastes discharged untreated from domestic and industrial activities have severely degraded this coastal ecosystem in the last decade, particularly in the Gulf of Gabes (Rekik et al., 2012) that is considered to be a nursery area for many fish species (Hattour et al., 1995) and the main pole of shellfish production in the country. This region is also known by its port infrastructure and great maritime traffic. Indeed, during 2010, 10450 vessels called at the commercial harbours in the Gulf of Gabes (OMMP, 2010).

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In this context, the present paper provides the results of a study carried out with the double objective: updating the listing of planktonic organisms and screening alien and potentially toxic species in the Gulf.

2. Materials and methods

2.1. Study area and sampling strategy The Gulf of Gabes located in the south of Tunisia in the southwestern Ionian Sea (between 35° N and 33° N) has a wide continental shelf extending from “Ras Kapoudia” to the Tunisian-Libyan border and sheltering and shelters various islands (Kerkennah and Djerba) and lagoons (Bougrara and El Bibane). It is open to the offshore area, influenced by the regional water circulation (Ben Ismail et al., 2012). The tide is semidiurnal being among the highest in the Mediterranean with a maximum range of about 2 m (Drira et al., 2008). The climate is dry (average precipitation: 210 mm/ year) and sunny with strong easterly winds. Study was conducted in the four commercial ports situated in the Gulf of Gabes: Sfax, Skhira, Gabes and Zarzis, according to three main radial from each port (northeast, east and southeast). Two sampling cruises were achieved during spring (April 2010) and summer (July 2010) seasons respectively for Sfax, Skhira ports and Gabes, Zarzis ports. In fact, these seasons are considered more conducive to the development of aquatic species diversity (Drira et al., 2008). Thus, 48 stations were sampled for water and sediment analysis (Fig. 1).

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2.2. Water sampling and plankton analysis Water samples were collected using a vertical water sampler (Rutner) of 1.7 L capacity at 1 m depth from the surface. Two threads (length: 75 cm; diameter: 25 cm) of different mesh were also used to identify phytoplankton (55μm) and zooplankton (80µm) species. Samples were preserved with 1% formaldehyde and 0.2% Lugol’s iodine solution. Phytoplankton identification and quantification were carried out throught analysing the whole sedimentation chambers using

an inverted microscope Leitz (400x magnification), by the

Uterm hl technique (Utermöhl, 1958). The zooplankton was identifed and counted under a Leica binocular microscope, in Dolffus chambers. Both for phytoplankton and zooplankton, identification was carried out using the available taxonomic descriptions (Cleve-Euler, 1951; Dussart, 1969; Huber-Pestalozzi, 1969; Amoros, 1984; Chretiennot-Dinet, 1990; Korovchinsky, 1992; Hallegraeff, 1995; Bérard-Therriault et al., 1999), when possible, at species level. The data was expressed as the number of individuals per liter (ind./L).

2.3. Sediment sampling and cysts analysis Surface sediment samples were collected in triplicate at each station using a Van Veen grab (Size: 15 x 30 cm). Once collected, samples were stored in the dark, in a plastic pouch, at 4 °C until processing. These samples were treated using the method suggested by Matsuoka and Fukuyo (2000) for dinoflagellate cyst analysis. 1 cm3 of sediment was collected using a medical syringe. The collected volume of sediment was dried at 80 ° C and weighed. For a qualitative and quantitative study, the cysts concentration was done by the method of sieving (Matsuoka and Fukuyo, 2000), based on the Utermöhl method using an inverted microscope Leitz Diavert ( 400x magnification) and a sedimentation chamber plankton. All cysts deposited at the bottom are 6

counted by scanning the total area of the chamber. Quantitative data was expressed as the number of cysts per gramme of dry weight sediment (cysts g-1 DW sediment).

3. Results 3.1. Phytoplankton assemblages A phytoplankton community list of 138 taxa was obtained, spread over 9 classes: Euglenophyceae,

Cyanobacteria,

Dictyochophyceae,

Cryptophyceae,

Chrysophyceae,

Prasinophyceae, Chlorophyceae, Dinophyceae and Bacillariophyceae. The last two groups were the most diversified with 35 and 49 species respectively (Table 1). The examination of outcomes related to radials showed that excepting for the region of Zarzis, where the Dinophyceae predominate at the radials N and NE whereas diatoms get ahead in the radial S (Fig. 2). The Gulf of Gabes was characterized by a quasi-homogeneous distribution affecting mainly these two principal classes (dinoflagellates, diatoms). However, no perceptible gradient of species diversity was detected from the port to open sea, apart from the Shkira region, that revealed a decreasing gradient of species diversity the three radial. Eleven known harmful phytoplankton species, including 2 Diatoms and 9 Dinophyceae, were found during this study (Table 1). Quantitatively, Sfax area appeared different from Skhira by much higher cell densities. In fact, among the diatoms, the highest densities were reatched by the species Skeletonema costatum (> 10 3 ind./L) and Cocconeis pediculus (> 0.5 10 3 ind./L) Among the Dinophyceae, it is mainly Gonyaulax sp., Protodinium simplex and Scrippsiella sp. which have arisen with cell densities > 0.5 103 ind./L. Cyanobacteria, mainly represented by Oscillatoria sp. were well developed in this area (> 10 7

3

ind./L). In the Shkira region, the most

dominant species were Navicula sp. and Euglena sp. whose densities exceeded 0.5 103 ind./L. Come after G. simplex and Dichtyocha fibula that reached 0.4 103 ind./L. Furthermore, it was noted that the Gabes area was characterized by much more important phytoplankton densities than the Zarzis area. Indeed, the Dichtyochophyceae represented by D. fibula and Dichtyocha sp. have characterized the region in this period. They reached 27. 103 ind./L. The highest diatoms densities were recorded by Cyclotella sp. (16.8 103 ind./L), Asterionella glacialis (4.8 103 ind./L), S. costatum (2.4 103 ind./L) and Thalassionema nitzchoides (1.28 103 ind./L). Among Dinophyceae, the two species Prorocentrum micans (2.28 103 ind./L) and Karenia selliformis (> 103 ind./L) occurred with relatively high cell densities. In the same period, the cyanobacteria were been present in all stations of Zarzis region, with highest density generated by the filamentous species Oscillatoria sp. (> 103 ind./L). Moreover, this region was characterized by the presence of species belonging to Dinophyceae such as P. micans which exceed 103 ind./l particularly in coastal station. Going to open sea, the P. micans density decreased (0.1 103 ind./L - 0.2 103 ind./L). The species Gymnodinium sp. was also presented in Zarzis area with a density less than 0.5 103 ind./L. Among the diatoms, the two harmful species, Chaetoceros socialis, that became established in the majority of stations, and Pseudo-nitzschia sp., generated densities higher than 0.5 103 ind./L (Table 1).

3.2. Zooplankton assemblages The qualitative analysis of zooplankton in the gulf of Gabes revealed the common presence of 21 groups which the most important is copepods. Twenty-five Copepods species were inventoried and spread over 4 orders: 13 Calanoida, 4 Cyclopoida, 3 Poecilostomoida and 5 Harpacticoida. Across the three radials in the four port areas, the zooplankton populations were fairly varied with dominance of copepods and larval forms among different shellfish species (Table 2; Fig 3). 8

The ciliate assemblage was composed by the species: Coxliella sp., Favella ehrenbergii, Leegardiella sol, Rhabdonella spiralis, Strombidium sp. Tintinnopsis beroidea, Tintinnopsis campanula and Tintinnopsis sp. The other groups are rather related to larval stages of the common species in the Gulf. Thus we find: Ostracoda (Cypridina mediterranea); Cladocera (Podon polyphemoides); Appendicular (Oikopleura dioica , Oikopleure albicans) ; Chaetognatha (Sagitta enflata) ; Cirripedia (Balanus amphitrite , Chtamalus sp.); Leptomedusae (Obelia sp.); foraminifera (Orbulina universa, Iridia sp.); Veliger larvae (Ruditapes decussatus, Ceritium vulgatum, Bitium reticulatum, etc.); Decapoda larvae (Palaemon elegans, Penaeus kerathurus, Sicyona carinata, Maia squinado, Carcinus sp, etc.); Annelida larvae ( Nereis sp., Lepidonotus clava, etc. ). It should be noted that the larval stages are dominated by those of crustaceans and molluscs.

3.3. Resting plankton (cysts) The search for Dinophyceae rest forms in the Gulf of Gabes resulted in the identification of 37 cysts taxa which 19 were identified to species, 16 to genus and two were assigned to different Dinophyceae orders, based on morphological characteristics such as the presence of red body in viable cysts, shape, pigmentation, wall, etc. In addition, other indeterminate forms were encountered which may correspond to other groups (other than protists Dinophyceae, cysts of ciliates, rotifers, eggs, copepods, metazoan, etc.). During this study, the surface sediments of the Sfax, Skhira, Gabes and Zarzis port areas were characterized, respectively, by the presence of 16, 18, 18 and 13 cysts taxa, belonging to the orders, Gymnodiniales, Prorocentrales, Gonyaulacales and Peridiniales. The two latters represented the most dominant groups. The four encysted forms of potentially toxic

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dinoflagellates, detected in this work, were wholly non-indigenous species (Gymnodinium catenatum, K. selliformis, Alexandrium minutum and Protoceratium reticulatum) (Table 3).

4. Discussion In the present study, 138 phytoplancton taxa were listed in the Gulf of Gabes. They are spread over 9 classes; namely Euglenophyceae, Cyanobacteria, Dictyochophyceae, Cryptophyceae, Chrysophyceae, Prasinophyceae, Chlorophyceae, Dinophyceae and Bacillariophyceae. The two latter categories were always the main dominant microalgae groups. The majority of species have previously been reported in the Mediterranean and the Tunisian coastal waters including the Bay of Tunis, the Gulf of Hammamet and the Gulf of Gabes (Hamza, 2003; Daly Yahia Kefi et al., 2005; Drira et al., 2008; Drira, 2009; Hannachi et al., 2011). Most of these species were cited in the literature as cosmopolitan. According Streftaris et al. (2005) and Gomez (2006; 2008), 40 species of phytoplankton of which 25 dinophyceae and 15 Bacillariophyceae are confirmed introduced in the Mediterranean Sea. Among these alien species we identified, in this work, 4 species in water (Table 1) and 6 in sediments of the Gulf of Gabes (Table 3). Eleven known harmful phytoplankton species, including 2 native species of Diatoms (C. socialis and Pseudonitzschia sp.) and 9 Dinophyceae including the invasive species A. minutum and K. selliformis were found during this study. A. minutum was originally described from a red tide in the Alexandria harbour. Toxins produced in high concentrations by these single-celled organisms are responsible for many global cases of paralytic shellfish poisoning (PSP) in humans. Toxins may also affect other components of the ecosystem including mammals, birds, fish and zooplankton (Van Dolah, 2000). It has a history of causing toxic blooms along the Atlantic coasts of France (Chambouvet et al., 2008), Spain (Franco et al., 1994), UK (Blanco et al., 2009) and Ireland (Touzet et al., 2008) as well as along the Mediterranean coast (Vila et al., 2005). In Tunisian 10

coast, Abdenadher et al. (2012) revealed that A. minutum, in comparison to other microalgae living under true coastal environmental conditions, in Gulf of Gabes, is significantly distinct in its behaviour and dynamic sensitivity to environmental variables providing new insights into its capabilities to take optimal advantage of niche opportunities. Since the formation of the genus Karenia in 2000, numerous new species have been described (Haywood et al., 2004). Beyond K. brevis, other taxa such as K. selliformis and K. papilionacea begin to be cited in the Mediterranean Sea. K. selliformis is the principal producer of gymnodimines (Seki et al., 1995) that demonstrate high affinity targeting of muscular and neuronal nicotinic acetylcholine receptors (Kharrat et al., 2008). Drira et al. (2008) confirmed that the toxic dinofagellate K. selliformis was distributed homogeneously in both the neritic zone and open sea. It has represented 64% of the recorded blooms in the Gulf of Gabes. This non native species has showed a specific requirement for salinity, higher than 42 g/l (Feki et al., 2013). Turki et al. (2006), Feki et al. (2008) and Geurmazi et al. (2010) noted the presence of other harmful species in the gulf of Gabes such as Osteopsis ovata, Coolia monotis and Gonyaulax polygramma. These authors suggested that the water discharges caused by anthropogenic activities, could have an impact on the phytoplankton species composition, leading to an increase in the abundance of opportunistic species which were responsible for the harmful algal blooms (Lee et al., 2005). Dammak-Zouari et al. (2006) have reported after phytoplankton quality survey of harbours surrounding the Gulf of Gabes, the presence of some toxic species presenting new records in the context of the Gulf phytoplankton flora such as A. margalefi, A. fundyense, A. insuetum, A. ostenfeldii, G. catenatum and K. papilionacea. In a general way, the increase in the phytoplankton introduction rate in the European Seas has accelerated during the last decade, reaching 31 species (Gomez, 2008) while only 8 species are

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introduced between 1981 and 2000 (Streftaris et al., 2005). Zenetos et al. (2008) report a similar number of non-indigenous phytoplankton species established in the Mediterranean. In marine areas, several planktonic species produce resting stages (cysts, spores, etc.) as part of their life cycle (Blackburn and Parker, 2005). In confined basins, usually characterised by low hydrodynamic conditions and high productivity, cysts produced in the water column sink to the sediments where they may remain for many years, constituting a reservoir of potential biodiversity (Dale, 1983; Belmonte et al., 1995). Life cycles including resting stages were previously taken as characteristic of neritic species, which underestimate the importance of the cysts production in oceanic waters (Montresor et al., 1998). The dormancy time of resting stages is very little known. However, some studies have revealed decade’s estimations both for protists (Belmonte et al., 1999) and metazoan (Marcus et al., 1994). According to Dale (1983), 10% of dinoflagellate species are capable of forming dormant cysts and have often been involved in the species invasion process, especially through ballast water (Hallegraeff, 1998; Drira, 2009). The analysis of these resting forms leads to a better consideration of rare species in the water column and to improve knowledge of planktonic biodiversity (Rubino et al., 2000). However, the correspondence in abundance between the active stages in the water column and resting stage in the sediment wasn't always validated (Rubino et al., 2009). In this study, it seems that the methodology used for sediment treatment is more favorable for dinoflagellate cyst recovery than other taxa (ciliates, rotifers, cladocerans and copepods) whose production, compared to the Dinophyceae, is lower. The use of much more important sediments quantity will increase the chances of finding the least abundant cysts (Rubino et al., 2009). Thus, the cysts inventory in sediments of the Gulf of Gabes led us to complement and enrich the taxa list established for the water column. Indeed, among the 37 inventoried cysts 17 were not found in their active form in coastal waters surveyed in this study and that can be added to the list of plankton species. Among 12

these 17 encysted forms 15 have already been listed in the Tunisian coastal waters including the Gulf of gabès (Hamza, 2003) and in the Bay of Tunis (Daly Yahia-Kéf et al., 2005). The encysted forms of Gymnodinium impudicum and Ensiculifera cf carinata were reported for the first time in this area. These non toxic species exist already in the Mediterranean at the Balearic Islands, the Sicilian-Tunisian channel and the Gulf of Lion (Gomez, 2003; Marchand et al., 2009). The five encysted forms of potentially toxic dinoflagellates, detected in this work were wholly non-indigenous species. In fact, besides the cysts of K. selliformis and A. minutum found also in vegetative form in water, the cysts of G. Catenatum, A. tamarense and P. reticulatum were detected in sediment. G. catenatum and A. tamarense are known to produces saxitoxin, the first metabolite responsible for PSP intoxication (Dale and Yentsch, 1978). G. catenatum was reported, for the first time, in 1976 in Spain after a PSP event in the Galician Rías (Estrada et al., 1984). It was probably introduced by the Galician fishing fleet, which during this period operated in Argentinan waters, where this species is common (Wyatt, 1992). The first G. catenatum records in the Mediterranean Sea appeared in the Alborán Sea transported by currents from the Atlantic Ocean according to the circulation through the Strait of Gibraltar (Bravo et al., 1990). This taxon has become an abundant and well-established species in the Alborán Sea and is associated with toxic events (Taleb et al., 2001). PSP occurrences by the toxic A. tamarense species complex were only known in Europe, North America and Japan (Hallegraeff, 1993). Their distribution, however, expanded widely from the subtropical to the subarctic of the north hemisphere and into the temperate south hemisphere (Lilly et al., 2007), and it is suggested that recent ocean climate change affects the distributions of Harmful Algal Bloom (HAB) species and their abundances (Hallegraeff, 2010). The dinoflagellate P. reticulatum is an armoured, marine, planktonic cosmopolitan globetrotter (Paza et al., 2007) known to produce Yessotoxins which are typical for this species and that was 13

assumed to have Diarrhetic Shellfish Poisoning (DSP) effects (Aune et al., 2002; Tubaro et al., 2003). Paza et al. (2007) have demonstrated that this species can either produce these Yessotoxins or another variant (homo-Yessotoxins). The highest densities cysts were mainly observed in the Zarzis port (660 cysts g-1 DW sediment). The responsible species were respectively the alien Scrippsiella acuminata and Lingulodinium polyedra. We note that the lower concentrations of cysts were recorded in the Sfax port area. It has been shown that the spatial distribution of cysts is related to sediments lithology, especially the grain size, which is responsible for existence and preservation of cysts while their abundance may be limited by surface water salinity which controls the number of planktonic Dinophyceae (Novichkova and Polyakova, 2007). The cysts concentrations in the sediments of the Gulf of Gabes (0- 660 cysts g-1 DW sediment) are very greater than those found by Ben Amor et al. (2006) in the Bay of Tunis that was caracterized by an average ranging between 3.3 and 5.1 cysts g-1 DW sediment. However, these results remain lower than those found by Giannakourou et al. (2005) in Thermaikos Gulf in Greece (446 – 5 718 cysts g-1 DW sediment) and by Novichkova and Polyakova (2007) in the White Sea (100 – 20 000 cysts g-1 DW sediment). Zmerli Triki et al. (2014) found in Bizerte Lagoon a maximum value of 1685 cyst g_1 DW sediment. Drira et al. (2008) revealed that the Dinophyceae, both motile cells and encysted forms, seems to be an important component of the phytoplankton community in the Gulf of Gabes. They occur throughout the coastal-open sea gradient. The abundance of harmful species is of great concern because their presence can lead to a significant impact on the edibility and marketability of marine foodstuffs. The dinofagellate ecology in the Gulf of Gabes is complex due to the interaction of various factors such as water movements, urban interferences and marine traffic. Treating urban and industrial wastes is the essential cornerstone for controlling aquatic

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eutrophication in the coastal waters of the Gulf. In the open sea, Modifed Atlantic Water occurrence is the main deterministic factor of dinofagellate development (Drira et al., 2008). In this work, zooplankton assemblage was dominated by copepods wich presented Twenty-five species. In the Tunis bay, located in the North Estern coast of Tunisia, copepod community was represented by 29 species (Ben Lamine et al., 2012). The copepod fauna from the Annaba region, in Algeria, consisted of 143 species (Khélifi-Touhami et al., 2007), to which Ounissi et al. (2016)

have

added ten new species for the area and two new species (Pseudiatoptomus

australiensis and Pseudiatoptomus arabicus) for the Mediterranean Sea. In Gulf of Gabes, zooplankton results revealed the presence of two Alien species (Acartia (Acanthacartia) bifilosa and Paracartia (Acartia) grani) among 39 introduced species in the Mediterranean cited in compilations of Streftaris et al. (2005) and Zenetos et al. (2008; 2010). Drira (2009) mentioned also the presence of these two species in the Gulf of Gabes. A. bifilosa is found inhabiting also a wide range of brackish-water habitats along the Atlantic and Mediterranean European shores. This species shows a great adaptability to different brackish-water environments (Uriarte et al., 1998). P. grani was reported for the first time off Western Norway and has been observed in shelf and coastal water of the Northeastern Atlantic and North Sea (Gallo, 1981). Over the last decades, it has progressively appeared in the Mediterranean Sea (Rodríguez and Vives, 1984; Belmonte and Potenza, 2001). Corriero et al. (2016) reported the occurence of this species along the Italian coast. An involuntary introduction could be the result of human activities. Bivalve transfers between the Atlantic Ocean and Mediterranean Sea could be sources of P. grani introduction. In fact, the species ecology has been closely linked with bivalve production (Audemard et al., 2004). It has been suggested to be one of the intermediate hosts of the protozoan paramyxean parasite Marteilia refringens responsible for marteiliosis, a major disease for bivalve production in Europe (Mineur et al., 2007). 15

Eight species of ciliates were identified which were quite frequent, in this study, especially in the coastal stations. No exotic species was encountered. Hannachi et al. (2009) confirmed that the total ciliates abundance, in the Gulf of Gabes, showed a gradual decrease from the coastal area to the open sea and an increase from the surface to the bottom. The same authors suggested that distribution of ciliate species in the Gulf of Gabes was most likely influenced by the combined effects of hydrographic conditions, zooplankton predation and urban interferences.

5. Conclusion This study constitutes an attempt to screen firstly the non-indigenous plankton species introduced into the Gulf of Gabes. It reveals that the proportion of introduced plankton species was hardly exceeds 3% compared to the whole Mediterranean. In fact, among the alien phytoplankton species in the Mediterranean, we identified four species in water and six in sediments of the Gulf of Gabes. Moreover, eleven known toxic phytoplankton species were also found. The Zooplankton results revealed the presence of two Alien species, only. This work attests also of the vulnerability of port areas towards the dynamic process of introductions, knowing that 97% of the species in the Mediterranean Sea are liable to settle there, given the importance of trafic intra Mediterranean.

Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Figure Caption Figure 1. Location of the study area and sampling stations 28

Figure 2. Percentage of phytoplankton groups in the Gulf of Gabes during the spring and summer cruises 2010. Figure 3. Percentage of zooplankton taxa in the Gulf of Gabes during the spring and summer cruises 2010.

Table 1: List of phytoplankton taxa inventoried in the Gulf of Gabes (Blank : absent, * : <0,1.10 3 ind. /l, ** : 0,1 - 0,5.10 3 ind /l, *** : 0,5 - 10 3 ind/l , **** : >10 3 ind/l) :

Non indigenious

:

Potentially toxic

Spring cruise

Sfax

Skhira

Summer cruise

Gabes

Zarzis

Bacillariophyceae Achnanthes sp. Bory Amphora ovalis Donkin Amphora spp. Ehrenberg Asterionella glacialis Castracane  Asterionella kariana Grunow Asterionella sp Hassall Bacteriastrum delicatulum Cleve Biddulphia rhombus (Ehrenb.) Biddulphia sp. Gray Cerataulina pelagica (Cleve) Hendey Chaetoceros borealis Osten Chaetoceros decipiens Osten Chaetoceros holsaticus Osten Chaetoceros pseudocrinitus Osten Chaetoceros simplex Ehrenberg Chaetoceros socialis Lauder Chaetoceros spp. Ehrenberg Cocconeis pediculus Ehrenb Cocconeis spp Sehmidt

**

* * * *

* **** *

* * *

*** *

* * * ** * *

* ** * *** *

29

*

* **

* *** * *

Coscinodiscus spp Ehrenberg Coscinodiscus radiatus Smith Cyclotella sp. Kützing Diatoma elongata (Lyngbye) Agardh Diatoma sp. Agardh Diploneis notabilis (Greville) Cleve Diploneis sp. Ehrenberg Fragilaria sp. Lyngbye Fragilariopsis sp. Hustedt in Schmidt Grammatophora marina (Lyngbye) Kützing Guinardia flaccida (Castracane) H.Peragallo Hemiaulus sinensis Greville, Hemiaulus sp. Greville, Leptocylindrus danicus Cleve Leptocylindrus minimus Gran. Licmophora gracilis (Ehrenberg) Grunow Licmophora paradoxa (Lyngbye) C.Agardh Melosira sp. (F.Muller) C. Agardh Navicula spp.Bory de St, Vincent Cylindrotheca closterium (Ehrenb.) Nitzschia longissima Ralfs Nitzschia spp. Hassal Plagiotropis sp. Pfitzer Pleurosigma sp. W. Smith Pseudo-nitzschia spp. Peragallo  Rhabdonema arcuatum (Lyngbye) Kützing Dactyliosolen fragilissimus Bergon Rhizosolenia setigera f.pungens ClevEuler Skeletonema costatum Cleve Stephanodiscus sp. Ehrenberg Eupyxidicula turris (Greville) Ralfs ex Pritchard Striatella sp. Agardh Striatella unipunctata Agardh Surirella sp. Turpin Toxarium undulatum Barley Tabularia tabulata (C. Agardh) Kütz Synedra spp. Smith Tabellaria fenestrata Ehrenberg Tabellaria sp. Ehrenberg Thalassionema nitzschioides Grun Thalassiothrix sp. Cleve & Grunow

*

* * *

* * *

**** * ***

** ** ** * * ** * *

* ** * * **

* ***

*

*

*

* * * * ** * * * * *

* * * ****

* ** * *

*

**

** * *** * *** *

**** * *

* * * * * * *

* *

*

**** *

Dinophyceae Akashiwo sanguinea Hirasaka Alexandrium minutum Halim   Dinophysis caudata Stein  Dinophysis sp. Stein Gonyaulax gracilis Schiller Lingulodinium polyedra Stein  Gonyaulax scrippsae Kofoid Gonyaulax spinifera Kofoid  Gonyaulax sp. Diesing Protodinium simplex (Lohmann) Gymnodinium spp. Stein Gyrodinium spirale (Bergh) Gyrodinium spp. Kofoid & Swezy Heterocapsa triquetra (Ehrenberg) Karenia selliformis Haywood  

* *

* * *

* ** * *

*

*

* *** *** *

* * ** *

*

** *

* *

*

** ** *

****

30

* * *** * *

Kryptoperidinium sp. Stein Tripos furca (Ehrenberg) Tripos fusus (Ehrenberg) Tripos lineatus (Ehrenberg) Tripos pentagonus (Gourret) Peridinium ovum Schiller Polykrikos spp. Bütschli Prorocentrum aporum (Schiller) Hasle Prorocentrum gracile (Ehrenberg) Prorocentrum lima Ehrenberg  Prorocentrum micans (Ehrenberg) Prorocentrum cordatum Schiller  Prorocentrum rotundatum Schiller Prorocentrum triestinum Schiller Prorocentrum vaginulum Schiller Protoperidinium breve Schiller Protoperidinium cerasus (Paulsen) Protoperidinium claudicans (Paulsen) Balech Protoperidinium curvipes (Ostenfe) Protoperidinium depressum (Bailey) Protoperidinium divergens (Ehrenb) Protoperidinium ovatum Schiller Peridinium quadridentatum (Jørgensen) Protoperidinium steinii (Jørgensen) Protperidinium sp. Bergh Pyrophacus steinii Schiller Scrippsiella acuminata Stein  Scrippsiella sp. Balech Cyst of dinophyceae

* *

*

* *

* * * *

*

* * ***

* *

* *

**** *

* * **

**** * * * * * * *

* **

* * * * ** *** *

* * *

* * * ** * ** **

** ** * *

* **

Dictyochophyceae

Dictyocha fibula Ehrenberg Octactis speculum Ehrenberg Dictyocha sp. Ehrenberg

*

**

*

**

**** * ***

Euglena spp. Ehrenberg Phacus longicauda Dujardin

*

**

*

*

Phacus sp. Dujardin

*

* *

** *** *

Euglenophyceae

*

Cyanobacteria

Anabaena sp. strain Chroococcus sp. Fremy Microcystis sp. Kutzing Oscillatoria sp. Ehrenberg Planktothrix sp. Gomont Spirulina sp. Turpin ex Gomont

* * * ****

* * *

*

Chlorophyceae Aureococcus sp. Hargraves & Sieburth

*

Cryptophyceae

Plagioselmis sp. Butcher

*

Chrysophyceae Chrysococcus sp. klebs

*

Prasinophyceae

Micromonas sp.Manton & Parke

*

31

Table 2: List of zooplankton taxa inventoried in the Gulf of Gabes Blank : absent

+

: present

 : Non indigenious Spring cruise Sfax Skhira

Copepoda calanoida

Acartia bifilosa Giesbrecht  Acartia clausi Giesbrecht and A. Steueri Smirnov Acartia italica Steuer Acartia latisetosa Kritchagin Acartia longiremis Lilljeborg Temora longicornis Müller O.F. Temora stylifera Dana Calanus helgolandicus Claus Centropages kroyeri Giesbrecht Centropages typicus Krøyer Eucalanus monachus Giesbrecht Paracalanus parvus Claus Paracartia grani Sars G.O. 

+ + + + + + + + + + + + +

+ + + + + + +

Summer cruise Gabes Zarzis +

+ + +

+ + + +

+ +

+ + + +

+ + +

+

Copepoda cyclopoida Oithona linearis Giesbrecht Oithona nana Giesbrecht Oithona plumifera Baird Oithona similis Claus

+ + + +

+ + +

+ + +

+ + + +

Copepoda harpacticoida Corycaeus clausi Dahl F Oncaea conifera Giesbrecht Oncaea mediterranea Claus

+

+ + +

+

+ + + + +

+ +

+ +

+ + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + + +

+

+

+ + +

Copepoda poecilostomoida Clytemnestra scutellata Dana Euterpina acutifrans Norman Microsetella norvegica Boeck Microsetella gracilis Dana Microsetella rosea Dana

+ +

+ +

Other taxa Ostracoda Tintinnids- ciliates Cladocera Appendicular Chaetognatha Pteropoda Leptomedusae Nauplii Zoe-Metazoe Postlarvae Cirripedia larvae Annelids larvae - trochophore Mollusc larvae - veliger Echinoderm larvae - Pluteus Nematoda Foraminifera Eggs

+ +

32

+ + + + + + + + + + + + + + + + +

+ + + + + + + + + + + + + + + + +

Table 3: Dinophyceae rest forms inventoried in the surface sediment of the Gulf of Gabes Blank: absent

+ : present

 : Non indigenious

 : Potentially toxic Spring cruise Sfax Skhira

Summer cruise Gabes Zarzis

Organic Peridiniales +

Ensiculifera cf carinata Matsuoka et al. 1990 Protoperidinium americanum (Gran & Braarud) Balech Protoperidinium conicoides (Paulsen) Balech Archaeperidinium minutum (Kofoid) Loeblich III Protoperidinium oblongum (Aurivillius) Parke & Dodge Protoperidinium sp. Bergh

+ + +

+ +

+

+

+

+

+

+

Calcareous Peridiniales Pyrophacus sp. Balech Scrippsiella crystallina Lewis Scrippsiella sp. Balech Scrippsiella acuminata (Stein) Balech 

+ + +

+ +

+

Gymnodiniales Gymnodinium catenatum L. W. Graham   Gymnodinium sp. Stein Akashiwo sanguinea Lebour Gymnodinium impudicum Fraga & Bravo Karenia selliformis Haywood, Steidinger & MacKenzie   Polykrikos schwartzii Bütschli Pheopolykrikos sp. Matsuoka & Fukuyo

+

+

+

+

+

+ + +

+ +

+

+

+

+

+

+

+ + +

+

Gonyaulacales Alexandrium cf affine (Inoue et Fukuyo) Balech Alexandrium minutum Halim   Alexandrium sp. Halim emend. Balech Alexandrium tamarense (Lebour) E.Balech  Gonyaulax sp. Diesing Lingulodinium polyedra Stein  Gonyaulax scrippsae Kofoid Gonyaulax spinifera Diesing  Protoceratium reticulatum Bütschli  

+ + +

+

+

+

+

+

+

+

+

+

+

+

Prorocentrales Prorocentrum sp Ehrenbergh

33

+ +