INTRODUCTION
Metazooplankton communities have a pivotal role in the functioning and evolution of marine ecosystems (Beaugrand & Ibanez, Reference Beaugrand and Ibanez2004). Copepods have colonized the pelagic realm in both inshore and open sea waters (Kiørboe, Reference Kiorboe2011). They have a key role in the marine food webs by transferring the primary production to higher trophic levels (Tiselius et al., Reference Tiselius, Saiz and Kiørboe2013). Meanwhile, the diversity and size spectrum of copepods reflect the physical and chemical properties of the water column (Richardson, Reference Richardson2008) as well as the availability of their prey, mainly phytoplankton and ciliates. Small planktonic copepods involving developmental stages (nauplii and copepodites) are important intermediaries between larger and microbial components of the marine pelagic food webs (Turner, Reference Turner2004). Their role is mainly important in oligotrophic ecosystems characterized by a relatively small size of primary producers and the dominance of microbial components (Agawin et al., Reference Agawin, Duarte and Agustí2000). Besides, heterotrophic and mixotrophic dinoflagellates are ubiquitous components of microzooplankton due to their successful feeding behaviour and their ability to overcome the lack of nutrients (Calbet, Reference Calbet2008; Jeong et al., Reference Jeong, Yoo, Kim, Seong, Kang and Kim2010). In addition to dinoflagellates, ciliates also constitute an important microzooplankton group (Hannachi et al., Reference Hannachi, Drira, Belhassen, Hamza, Ayadi and Bouain2008). They are the main components of the copepod diet in oligotrophic ecosystems (Calbet & Saiz, Reference Calbet and Saiz2005) characterized by a low autotrophic biomass produced by nano- and picoplankton which are rarely consumed by copepods (Calbet et al., Reference Calbet, Landry and Scheinberg2000). In combination with trophic conditions, the physical properties of water masses have a major influence on the abundance and spatial distribution of planktonic copepods (Beaugrand et al., Reference Beaugrand, Ibanez, Lindley and Reid2002), which are thus considered as good biological indicators for water masses exchange (Bonnet & Frid, Reference Bonnet and Frid2004).
In the Gulf of Gabes, copepods have been reported to be the main contributors to total zooplankton (Drira et al., Reference Drira, Bel Hassen, Ayadi and Aleya2014), while picoplankton and small flagellates have become the major component of the autotrophic biomass (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008). Therefore, mesozooplankton communities are affected by the prevalence of small phytoplankton fractions. They are also dependent on the water masses circulation which is strongly linked to the general circulation of the Mediterranean Sea (Hattour et al., Reference Hattour, Sammari and Ben Nassrallah2010). Previous studies have shown the presence of a salinity minima zone resulting from the propagation of the Atlantic waters off the Gulf of Gabes (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008, Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout, Messaoudi, Issaoui, Aleya and Bouaïn2009). Mediterranean and Atlantic mesozooplankton communities represent several similarities exhibiting temperate and tropical influences (Champalbert, Reference Champalbert1996). Endemic species are scarce and restricted to inshore waters (Furnestin, Reference Furnestin, van der Spoel and Pierrot-Bults1979). The influence of the Atlantic flow is important in the Alboran Sea and in the south-western basin contributing to higher biodiversity and abundance than in the Catalan Sea (Furnestin, Reference Furnestin1968). Atlantic mesozooplankton are then transferred through the Sicilo-Tunisian Strait; their abundance decreases eastward (Champalbert, Reference Champalbert1996; Nowaczyk et al., Reference Nowaczyk, Carlotti, Thibault-Botha and Pagano2011) due to the bifurcation of the Atlantic vein in this strait (Poulain & Zambianchi, Reference Poulain and Zambianchi2007).
We are aiming, through this work, to study the spatial distribution of planktonic copepods in relation to phytoplankton, microzooplankton and physical properties of the water column, to highlight the importance of small planktonic copepods and their trophic interaction with microzooplankton, mainly heterotrophic dinoflagellates and ciliates, in the oligotrophic waters of the Gulf of Gabes.
MATERIALS AND METHODS
Study site
The study was conducted in the Gulf of Gabes, in the south-east of Tunisia (Figure 1). This important marine ecosystem expands over 700 km along the Tunisian coasts from Chebba to the Tunisian–Libyan border. The immense continental shelf (250 km) and the low slopes make the main features of this region (Hattour et al., Reference Hattour, Sammari and Ben Nassrallah2010). The tide in the Gulf of Gabes is semi-diurnal. It is the highest in the Mediterranean with a maximum of 2 m resulting from resonance phenomena (Sammari et al., Reference Sammari, Koutitonsky and Moussa2006). The climate in this region is arid to semi-arid. The shallow waters run around Kerkennah, Djerba islands, and the lagoons of Boughrara and El Bibane (Hattour et al., Reference Hattour, Sammari and Ben Nassrallah2010). As the Gulf of Gabes is located between the eastern and western parts of the Mediterranean Sea, the dynamics of its water masses is strongly linked to the general circulation of the Mediterranean Sea. To the north of the Italian island Lampedusa, the current of Atlantic origin is divided into two veins: the first one goes to the south-east while the second turns southward and feeds the circulation in the Gulf of Gabes (Poulain & Zambianchi, Reference Poulain and Zambianchi2007). The flow of the Atlantic waters through the Sicilo-Tunisian Strait undergoes an obvious seasonal variability (Ben Ismail et al., Reference Ben Ismail, Sammari, Gasparini, Béranger, Brahim and Aleya2012). The intensity of this Atlantic vein is subject to fluctuations that affect the circulation of water masses along the Gulf of Gabes (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout, Messaoudi, Issaoui, Aleya and Bouaïn2009). Salinity in this region is high (37.5–39.25 psu). The existence of salinity minima in the Gulf of Gabes is attributed to the Atlantic waters (Sammari et al., Reference Sammari, Millot, Taupier-Letage, Stefani and Brahim1999).
Map of the sampled stations in the Gulf of Gabes during a summer cruise in June 2008 and the isobaths 50, 100 and 200 m.
Sampling
An oceanographic cruise was conducted during the summer, from 13 June to 16 June 2008 aboard the RV ‘Hannibal’, with 15 sampling stations in the Gulf of Gabes (Figure 1). In each station, values of temperature, salinity, dissolved oxygen and sigma-t were determined with a conductivity-temperature-depth profiler (CTD: SBE 9, Sea-bird Electronics, USA) equipped with a 12 Niskin bottle rosette sampler lowered from the surface to near the bottom. Water samples for chemical analysis, phytoplankton and ciliate examination were collected from three depths (surface, middle of the water column and near the bottom) in inshore stations less than 50 m in depth (S32, S27, S21, S26, S25, S31 and S09) and from five depths (surface, −20, −50, −75, near bottom) in offshore stations where the depth exceeded 50 m (S02, S25, S04, S07, S12, S13, S18 and S18). Samples for nutrient analyses (120 ml) were immediately preserved upon collection (−20°C, in the dark). For phytoplankton and ciliate enumeration, 1 litre was preserved in a Lugol (4%) iodine solution (Bourrelly, Reference Bourrelly1985) and stored in the dark at a low temperature (4°C) until analysis.
Chlorophyll-a samples (1000 ml) were filtered by vacuum filtration onto Whatman GF/F glass fibre filters. Filters were then immediately stored at −20°C.
Zooplankton were collected using a cylindro-conical net (30 cm aperture, 100 cm height and 100 m mesh size) equipped with a Hydro-Bios flowmeter. The net was towed obliquely from a depth near the bottom to the surface in each station at a mean speed of 1 m s−1 during 10 min. After collection, zooplankton samples were rapidly preserved in a 2% buffered formaldehyde solution. They were stained with rose Bengal to identify internal tissues of the different zooplankton species and also to facilitate the dissection of copepods.
Nutrient and chl-a analyses
The nutrients (nitrate, ammonium, orthophosphate and silicate) were analysed with a Bran and Luebbe type 3 autoanalyser.
Chlorophyll-a was analysed using the HPLC method fully described in Bel Hassen et al. (Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008).
Phytoplankton and ciliates enumeration
Sub-samples (50 ml) were counted under an inverted microscope after settling for 24–48 h. The identification of phytoplankton taxa was made according to various keys (Dodge, Reference Dodge1985; Tomas, Reference Tomas1996). Tintinnids were identified relying on the lorica morphology and species description made by Aboud-Abi Saab (Reference Abboud-Abi Saab2008). Naked ciliates were identified following the works of Alder (Reference Alder and Boltovskoy1999) and Strüder-Kypke & Montagnes (Reference Strüder-Kypke and Montagnes2002). Biovolumes were calculated from length and width measurements and converted to carbon biomass using the conversion factor for phytoplankton proposed by Menden-Deuer & Lessard (Reference Menden-Deuer and Lessard2000), with 1 μm3 = 0.216 × 10−6 μg C for all phytoplankton taxa except diatoms (1 μm3 = 0.288 × 10−6 μg C). For ciliate species, we used the conversion factor proposed by Putt & Stoecker (Reference Putt and Stoecker1989): 1 pg C = 1 μm3 × 0.19.
Zooplankton enumeration
Zooplankton samples, especially planktonic copepods, were identified according to Rose (Reference Rose1933) and Bradford-Grieve et al. (Reference Bradford-Grieve, Markhaseva, Rocha, Abiahy and Boltovsky1999) and sorted into four demographic classes (nauplii, copepodites, adult males and adult females). Miscellaneous mesozooplankton such as Doliolida, Cladocera, Appendicularia and Siphonophora, were also counted according to Tregouboff & Rose (Reference Tregouboff and Rose1957). Enumeration was performed under a vertically mounted deep-focus dissecting microscope (Olympus TL 2). The zooplankton density was expressed as: X = N/(πr 2s)/3, where N = number of individuals sampled, r = 15 cm: half of the diameter of the plankton net and s = turn numbers shown by the flowmeter. The diversity of the phytoplankton, ciliates and copepods was determined using the Shannon–Weaver index (Shannon & Weaver, Reference Shannon and Weaver1949).
Data analysis
Diagrams and contour plots were made using Ocean Data View (ODV) software, version 4.2.1, R. Schlitzer, http://odv.awi-bremerhaven.de/, 2009.
Pearson coefficients were calculated to detect significant correlations between the studied parameters. One-way analysis of variance (ANOVA) was performed to detect significant differences between inshore and offshore regions for the physico-chemical and biological parameters. Canonical correspondence analysis (CCA) was applied to different physical (temperature, salinity, water density and dissolved oxygen), chemical (nitrate, orthophosphate, ammonium and silicate) and biological parameters (Dinoflagellate biomass, diatom biomass, ciliate biomass, chl-a) in relation with the densities of the most dominant copepod species. All the analyses were performed using the X L-Stat software.
RESULTS
Physico-chemical parameters
The temperature–salinity diagram revealed the presence of different water masses (Figure 2). The deep and cool waters (>100 m depth) correspond to the Ionian Waters (IW) characterized by high salinity intruding mainly to the stations S07 and S04 in the offshore region. The intermediate depth (<100 m) and cool waters correspond to the Modified Atlantic Waters (MAW) intruding mainly to the stations S25, S04, S12, S13, S18 and S18. These waters are further recognized by their low salinity (<37.5 psu). The shallow salty and warm waters correspond to the Mixed Mediterranean Water (MMW) confined to the inshore region (<50 m depth; stations S32, S27, S21, S26, S25, S31 and S09). Nonetheless, the IW and MAW are encountered in the offshore region.
Temperature-salinity diagram showing the presence of different water masses in the Gulf of Gabes during a summer cruise in June 2008. (Ocean Data View (ODV) software, version 4.2.1, R. Schlitzer, http://odv.awi-bremerhaven.de/, 2009).
Contour plots of temperature revealed a decreasing water temperature from surface to bottom and from inshore to open sea regions (Figure 3A). Significant differences were found between the inshore and offshore regions (ANOVA, F = 32.38, P < 0.001). Inshore waters were the warmest reaching 24°C with an average of 22.06 ± 1.43°C. In the open sea region, water temperature decreased considerably with depth recording 15°C near the bottom. Therefore this quick diminution of temperature with depth led to the establishment of a thermocline (Figure 3A). The vertical distribution of salinity showed the presence of a salinity minimum (<37.5 psu) in the offshore region. The deep offshore waters were distinguished by high salinity and low temperature corresponding to the IW. Nonetheless, the inshore region of the Gulf of Gabes was characterized by salty Mediterranean waters (MMW) exceeding 38 psu (Figure 3B).
Vertical profiles of (A) temperature, (B) salinity, and (C) water density during a summer cruise in June 2008 in the Gulf of Gabes according to the coast gradient. Distance on the x-axis is scaled in kilometres from the starting point of the section: First station (10.46°E 33.91°N. The end of the section is located at the most distant station (12.91°E 35.09°N). Black dots represent sampling points.
Nutrient concentrations were low, despite higher nitrate concentration at the surface in the offshore region (with a maximum of 3.75 μm) (Figure 4A). Ammonium and orthophosphate did not exceed 1.5 and 0.1 μm respectively (Figure 4B, C). Silicate concentrations increased in the deep offshore region. They reached 6 μm near 200 m isobath (Figure 4D). Phosphorus limitation was underlined by the high N/P ratio (Figure 4E). Chlorophyll-a concentrations were very low (<0.3 μg C l−1) suggesting an oligotrophic ecosystem. A deep chl-a maximum (0.25 μg C l−1) was recorded between 80 and 120 m depth in the offshore area (Figure 4F).
Vertical profiles of (A) nitrate, (B) ammonium, (C) orthophosphate, (D) silicate, (E) N/P ratio and (F) chlorophyll-a (μg C l−1) during a summer cruise in June 2008. Details of the section are the same as in Figure 3.
Phytoplankton and ciliates
Total phytoplankton density ranged from 2.27 × 103 ± 1.45 × 103 cells l−1 in the deep offshore IW to 15.87 × 103 ± 12.34 × 103 cells l−1 in the MMW (Figure 5A, Table 1). The obvious proliferation of heterotrophic and mixotrophic dinoflagellates was the distinctive feature of this summer cruise.
Spatial distribution of (A) total phytoplankton density, (B) total phytoplankton biomass, (C) dinoflagellate biomass and (D) the heterotrophic dinoflagellate Noctiluca scintillans biomass, during a summer cruise in June 2008.
Densities and biomass of the major microplankton groups encountered in the three water masses of the Gulf of Gabes during a summer cruise in June 2008.
They contributed to 52% of total phytoplankton abundance in the MMW where the maximum of abundance was recorded (8.16 × 103 ± 7.51 × 103 cells l−1) due to the important proliferation of Protoperidinium ovatum. Dinoflagellate density was positively correlated to both temperature (r = 0.772; N = 71; P = 0.05) and salinity (r = 0.765; N = 71; P = 0.05) suggesting a good adaptation of this group to the warm and salty MMW waters in the inshore region. Diatom density showed positive correlation to both temperature (r = 0.726; N = 71; P = 0.05) and salinity (r = 0.654; N = 71; P = 0.05) in the MMW. Silicoflagellates were restricted to the MMW (Table 1). Cyanobacteria were obviously more abundant in the MMW (Table 1). Despite the low values of chl-a, total phytoplankton biomass was high especially in the MMW reaching a mean value of 8.57 × 102 ± 3.77 × 102 μg C l−1 (Table 1, Figure 5B).
Dinoflagellates were the main contributors to the total phytoplankton biomass during the whole cruise (99%). Dinoflagellate biomass was the highest in the MMW in the inshore region (Figure 5C) due to the proliferation of large taxa such as Noctiluca scintillans (400 μm), Neoceratium pentagonum (218 μm) and Protoperidinium depressum (50 μm). Noctiluca scintillans contributed to 47.23% of total dinoflagellate biomass in the MMW (Figure 5D).
Ciliate density was obviously higher in the MMW (mean ± SD = 1.56 × 103 ± 0.46 × 103 cells l−1) (Table 1). They were characterized by the prevalence of tintinnids which exceeded total naked ciliates either in abundance or in biomass. Both temperature (r = 0.701; N = 71; P = 0.05) and salinity (r = 0.642; N = 71; P = 0.05) were positively correlated to Tintinnida.
Zooplankton
The spatial distribution of the mesozooplankton communities revealed a high total mesozooplankton density in the inshore area intruded by salty and warm MMW (mean ± SD = 1033 × 103 ± 886 × 103 individuals m−3) (Figure 6A). Copepods were the most abundant mesozooplankton group; their density ranged from 50 × 103 to 1450 × 103 individuals m−3 (Figure 6B). Meanwhile, small copepods (total length 0.4–1.45 mm including all developmental stages) obviously prevailed in the MMW.
Spatial distribution of (A) total mesozooplankton, (B) total copepods, (C) small copepods and (D) large copepods in the Gulf of Gabes during a summer cruise in June 2008. Small copepods included species with total length of adult ≤1.45 mm.
The highest copepod density was recorded in the MMW (1450 × 103 individuals m−3 at S27) mainly driven by small copepods (Figure 6C). Larger copepod taxa did not exceed 76 × 103 individuals m−3 (Figure 6D). The important proliferation of Oithonidae in the inshore region led to the prevalence of small planktonic copepods accounting for 93.64% of total copepod abundance in the MMW (Table 2). Oithona similis and O. nana were the most abundant species contributing to 39.61 and 23.49% of total copepod abundance in the MMW respectively (Table 2). The prevalence of small copepods was also recorded in the MAW where they contributed up to 71.05% of total copepod abundance (Table 2). In addition to Oithonidae, this water mass was also distinguished by the proliferation of clausocalanids. In fact, O. nana, Clausocalanus furcatus and O. similis were the most dominant species in the MAW contributing to 15.49, 11.93 and 10.43% respectively in this water mass. Meanwhile, the deep offshore IW was characterized by the dominance of larger copepod fractions (total length 1.45–2.5 mm) as a result of the proliferation of Nannocalanus minor (44.05% of total copepod abundance in the IW).
Small and large copepod species classified along an increasing gradient of total body length (TL) and their relative abundance in the three major water masses of the Gulf of Gabes in June 2008 (A copepod species of Atlantic origin referring to Rose, Reference Rose1933). The highest abundances are in bold.
During this cruise, the small C. furcatus was revealed to be a permanent component of the offshore copepod communities of the Gulf of Gabes in the IW as well as in the MAW. In fact, this species contributed up to 15.08% of total copepod abundance in the IW (Table 2).
Small planktonic copepods included cyclopoids, harpacticoids, poecilostomatoids and small calanoid genera (Acartia, Metacalanus, Paracalanus, Clausocalanus and Calocalanus) (Table 2). Oithonids were numerically dominant contributing to the high cyclopoid density (Figure 7A). The latter was significantly correlated with temperature (r = 0.736, N = 71, P = 0.05) and salinity (r = 0.738, N = 71, P = 0.05). Therefore the small cyclopoids represented the best adapted group to the MMW.
The spatial distribution of the main orders making up small copepod communities in the Gulf of Gabes during a summer cruise in June 2008: (A) Cyclopoida, (B) Harpacticoida, (C) small calanoids and (D) Poecilostomatoida.
Harpacticoid density ranged from 20 × 103 to 320 × 103 individuals m−3 (Figure 7B). The abundance of harpacticoids was the result of the important proliferation of Euterpina acutifrons which was highly correlated with temperature (r = 0.695, N = 71, P = 0.05) and salinity (r = 0.742, N = 71, P = 0.05). Therefore, the occurrence of harpacticoida was mainly neritic enhanced by the warm and salty MMW (Figure 7B). Small calanoid families such as Acartiidae, Clausocalanidae and Paracalanidae contributed to the proliferation of small calanoids (Figure 7C). These small calanoids involved three Atlantic invasive species such as Calocalanus contractus, Acartia bifilosa and A. tonsa (Table 2). In contrast to other small copepods, the spatial distribution of Poecilostomatoida showed a preference to the MAW in the offshore area (Figure 7D). In fact, this order included two invasive Atlantic species, namely Corycaeus amazonicus and Pachos tuberosum (Table 2).
In addition to adults, small planktonic copepods also included copepodites and nauplii of almost all genera. Nauplii density was very low (mean ± SD = 13 × 103 ± 9.85 × 103) (Figure 8A). Meanwhile, the remaining developmental stages were characterized by the numerical dominance of copepodites (Figure 8B) (mean ± SD = 409.33 × 103 ± 407 × 103) and adults (mean ± SD = 407 × 103 ± 286 × 103) (Figure 8C).
The spatial distribution of copepod developmental stages communities in the Gulf of Gabes during a summer cruise in June 2008: (A) nauplii, (B) copepodites and (C) adult.
As opposed to the copepod density, there was an obvious increase in diversity in the offshore region (mean ± SD = 1.13 ± 0.11 bits cell−1) (Figure 9A). During our survey, rare species such as invasive Atlantic copepods were mainly encountered in the offshore region where hydrography is governed by the propagation of an Atlantic vein. The distribution of the total copepod diversity was not strongly linked to those exhibited by ciliates and phytoplankton (Figure 9B, C).
The spatial distribution of the diversity index H′ of (A) total copepods, (B) total ciliates and (C) total phytoplankton in the Gulf of Gabes during a summer cruise in June 2008.
Cladocerans, siphonophores, chaetognaths and appendicularians were also permanent components of the holoplankton in the Gulf of Gabes (Table 3). Meroplankton was made up essentially of larval stages such as bivalve larvae (Table 3).
Miscellaneous zooplankton groups and their relative abundance in the major water masses encountered in the Gulf of Gabes in June 2008.
Canonical Correspondence Analysis (CCA) showed that F1 and F2 axes explained 87.52% of the variance (Figure 10A). The small copepod species O. nana, O. similis and Euterpina acutifrons showed a close link to the temperature and salinity at the inshore stations (S26, S27) intruded by MMW. The large calanoid N. minor was more sensitive to the availability of nutrients (nitrate, silicate, ammonium) in the offshore stations (S04, S07) involving the IW. The density of the small calanoid C. furcatus and chl-a concentration were higher in the MAW. The spatial distribution of the calanoids Acartia clausi, A. longiremis, Centropages typicus and Centropages kroyeri was linked to the biomass of ciliates, diatoms and chl-a. Clausocalanus furcatus and Oithona plumifera was associated to nutrients (orthophosphate, ammonium, silicate and nitrate). Water density was the major physical parameter governing the abundance and the distribution of these two species. Canonical Correspondence Analysis applied using the sampled stations and the physical parameters showed both increasing temperature and salinity in the inshore stations S31, S32, S25, S21, S27 and S26 (Figure 10B). Therefore, these stations were likely to be intruded by the MMW.
Canonical Correspondence Analysis applied on the biomass of phytoplankton, ciliates, the abundance of copepod orders and the most dominant copepod species (A) and between stations and physical parameters (B) during a summer cruise in June 2008 in the Gulf of Gabes.
DISCUSSION
Physical and trophic context during summer stratification in the Gulf of Gabes
Our study during this summer cruise in the Gulf of Gabes showed the existence of three different water masses associated with Mediterranean (MMW and IW) and Atlantic (MAW) origins as already described in previous studies (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008; Ben Ismail et al., Reference Ben Ismail, Sammari, Gasparini, Béranger, Brahim and Aleya2012). The salinity minimum zone resulted from the propagation of Atlantic waters and was evidence of the existence of MAW in the offshore region of the Gulf of Gabes. The propagation of this Atlantic vein participated in fertilizing the offshore region with nutrients as shown by higher nitrate concentrations found at the surface in the offshore region. Conversely, the shallow inshore waters were intruded by saltier, warmer and nutrient-depleted MMW waters. Dinoflagellates and diatoms proliferated mainly in the MMW of the Gulf of Gabes characterized by higher temperature and salinity and by low and phosphorus-limited nutrients. The dominance of dinoflagellates is usually encountered during stratification in the Mediterranean Sea (Gòmez & Gorsky, Reference Gómez and Gorsky2003). In fact, they prefer a stable water column and warm temperature (Lasternas et al., Reference Lasternas, Tunin-Ley, Ibanez, Andersen, Pizay and Lemée2011). Thus, the stability of the water column during summer stratification provides the opportunity to take full advantage of these abilities. Their proliferation, despite the establishment of a thermocline limiting the replenishment of the euphotic layer with nutrients, may be linked to their motility and their ability to move and migrate vertically in the water column in search of nutrients and light (Ross & Sharples, Reference Ross and Sharples2007). Besides, they can overcome the lack of nutrients by diversifying their trophic modes (autotrophic, mixotrophic and heterotrophic) (Jeong et al., Reference Jeong, Yoo, Kim, Seong, Kang and Kim2010). Dinoflagellates are ubiquitous in marine ecosystems. They are also very abundant in the Gulf of Gabes as found by Bel Hassen et al. (Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008) who proved that the nano- and picophytoplankton were the major contributors to the autotrophic biomass in the gulf. About half of dinoflagellate species in marine plankton are deprived of chloroplasts (Sherr & Sherr, Reference Sherr and Sherr2007). Mixotrophic and heterotrophic dinoflagellates exhibit several feeding mechanisms (pallium-feeding, peduncle-feeding and direct engulfment) (Jeong et al., Reference Jeong, Yoo, Kim, Seong, Kang and Kim2010). Several Protoperidinium species are able to feed on diatoms (Sherr & Sherr Reference Sherr and Sherr2007), autotrophic dinoflagellates, eggs and early naupliar stages (Jeong et al., Reference Jeong, Yoo, Kim, Seong, Kang and Kim2010). Protoperidinium species may be in competition with mesozooplankton to feed on other dinoflagellates and diatoms. Due to the low values of chl-a and the high biomass of heterotrophic dinoflagellates and ciliates, the Gulf of Gabes had a heterotrophic microplankton standing stock feeding on a large variety of prey ranging from picoplankton to diatoms (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008).
During the study period, the ciliate biomass was very low, revealing a possible predation by copepods and even by heterotrophic dinoflagellates (Jeong et al., Reference Jeong, Yoo, Kim, Seong, Kang and Kim2010). Copepods represent an important mesozooplankton group able to complete a top-down control on ciliate populations (Zervoudaki et al., Reference Zervoudaki, Christou, Nielsen, Siokou Frangou, Assimakopoulou, Giannakourou, Maar, Pagou, Krasakopoulou, Christaki and Moraitou Apostolopoulou2007). In fact, ciliates are considered as a rich protein food source for copepods (Gifford & Dagg, Reference Gifford and Dagg1991). In the eastern Mediterranean Sea, similar results reported the strong top-down control of copepods in regulating ciliate populations (Siokou-Frangou et al., Reference Siokou-Frangou, Bianchi, Christaki, Christou, Giannakourou, Gotsis, Ignatiades, Pagou, Pitta, Psarra, Souvermezoglou, Van Wambeke and Zervakis2002). Furthermore, the subsistence of tintinnids on behalf of aloricate ciliates may be explained by their ability to escape grazing due to the presence of a protective lorica (Abboud-Abi Saab, Reference Abboud-Abi Saab2008).
Copepod communities: dominance of small copepods in the MMW in the inshore area and in the MAW in the offshore area
During this summer cruise, small copepods, particularly oithonids, were found to largely dominate copepod communities in both MMW and MAW. This appears to be a common feature in the neritic region of the Gulf of Gabes intruded by the MMW, as it was also reported in four previous cruises (July 2005, May–June 2006, September 2006 and March 2007) by Drira et al. (Reference Drira, Bel Hassen, Ayadi and Aleya2014). During these cruises, as well as what was observed during our study, oithonids recorded very high abundances with O. similis (103 to >105 ind m−3) and O. nana (104 to >105 ind m−3) being the most abundant species. The dominance of small copepods, particularly oithonids, in warm and salty coastal waters (similar to the MMW) has also been reported in the north of Tunisia (bay of Tunis; Daly Yahia et al., Reference Daly Yahia, Souissi and Daly Yahia Kefi2004) and on the Algerian coast (Hafferssas & Seridji, Reference Hafferssas and Seridji2010) as well as in other sites all over the Mediterranean: the Balearic Sea (Fernandez de Puelles et al., Reference Fernandez de Puelles, Gras and Hernandez Leon2003), the bay of Toulon (Jamet et al., Reference Jamet, Jean, Bogé, Richard and Jamet2005), the Gulf of Naples (Mazzocchi & Ribera d'Alcalà, Reference Mazzocchi and Ribera d'Alcala1995), the Adriatic Sea (Vidjak et al., Reference Vidjak, Bojanic, Kuspilic, Gladan and Ticina2007), the Aegean Sea (Zervoudaki et al., Reference Zervoudaki, Christou, Nielsen, Siokou Frangou, Assimakopoulou, Giannakourou, Maar, Pagou, Krasakopoulou, Christaki and Moraitou Apostolopoulou2007) and the Northern Levantine basin (Uysal & Shmeleva, Reference Uysal and Shmeleva2012). Most of these studies reported a very high contribution of small copepods (>80%) to the copepod community, comparable to our results (93% in the MMW).
Oithona similis has been recognized as the most ubiquitous copepod species in the world ocean (Gallienne & Robins, Reference Gallienne and Robins2001). It was reported to record very high densities in the neritic temperate seas. This may explain its prevalence in the Gulf of Gabes as a semi-arid Mediterranean site (Nakamura & Turner, Reference Nakamura and Turner1997). This small cyclopoid revealed clear eurythermal and euryhaline distribution. In fact, the abundance of O. similis was positively correlated with temperature (r = 0.712; N = 71; P = 0.05) and salinity (r = 0.712, N = 71, P = 0.05) explaining its abundance in this inshore region under the influence of salty and warm Mediterranean waters (MMW) (Bel Hassen et al., Reference Bel Hassen, Drira, Hamza, Ayadi, Akrout and Issaoui2008). In addition, this copepod is omnivorous feeding on phytoplankton, heterotrophic protists and naupliar stages of copepods, showing a preference for heterotrophic dinoflagellates and ciliates (Nakamura & Turner, Reference Nakamura and Turner1997; Turner, Reference Turner2004). Furthermore, this species revealed clear preference for motile over non-motile prey (Castellani et al., Reference Castellani, Irigoien, Mayor, Harris and Wilson2008). In fact, O. similis selects ciliates to diatoms of similar size and shape (Castellani et al., Reference Castellani, Irigoien, Mayor, Harris and Wilson2008). This goes hand in hand with our results in the Gulf of Gabes characterized by an obvious proliferation of dinoflagellates accounting for the most important part of phytoplankton biomass.
The small cyclopoid O. nana (0.48–0.8 mm) significantly contributed to total copepod abundance (23.49%) in the inshore region intruded by salty and warm MMW. It recorded high densities at the stations S32 and S27 located in the south of the Gulf of Gabes. This area is characterized by an arid climate accompanied by a higher temperature enhancing the development of this small Oithonidae (Drira et al., Reference Drira, Bel Hassen, Ayadi and Aleya2014), also shown by a positive correlation with temperature (r = 0.619, N = 71, P = 0.05). Oithona nana exhibits a certain ability to endure the environmental perturbations relying on its low respiratory rate and omnivorous diet (Gallienne & Robins, Reference Gallienne and Robins2001). Several studies proved that O. nana was able to proliferate in fluctuating ecosystems (Williams & Muxagata, Reference Williams and Muxagata2006). The monitoring of the zooplankton communities and mainly of O. nana is considered as a useful biological indicator aiming to assess the evolution of marine ecosystems (Siokou-Frangou et al., Reference Siokou-Frangou, Papathanassiou, Lepretre and Frontier1998). The semi-enclosed region of Gabes is subject to industrial discharge from cities (Gabes, Sfax), harbours and several chemical manufacturers. Transport of petrol through Skhira port may also be a source of pollution to the Gulf of Gabes as well as an uncontrolled phosphogypsum dumpsite. The link between phosphogypsum impact and the abundance of oithonids was shown in a previous study in the Gulf of Gabes (Rekik et al., Reference Rekik, Drira, Guermazi, Elloumi, Maalej, Aleya and Ayadi2012).
In the open sea region of the Gulf of Gabes, where exchange of water masses is active and under the influence of the Atlantic, oithonid density declined significantly giving place to offshore copepod species. The copepod community there was characterized by lower abundance but higher diversity. The large calanoid N. minor dominated in this offshore region. In fact, this calanoid is omnivorous, feeding on small phytoplankton and ciliates. It reveals a quick response when productivity in the water column increases by undergoing a rapid population expansion. Furthermore this copepod is able to maintain continuous reproduction, producing 2–5 generations/year (Ashjian & Wishner, Reference Ashjian and Wishner1993).
During our survey, the small calanoid C. furcatus proliferated well in the offshore region intruded by the MAW and IW. This widespread copepod species is considered as an indicator of temperate offshore waters (Fragopoulu & Lakkis, Reference Fragopoulu and Lakkis1990). It has an epipelagic distribution above the thermocline (Paffenhöfer & Mazzocchi, Reference Paffenhöfer and Mazzocchi2003). Previous studies reported high summer and autumn densities of this small calanoid regardless of the low phytoplankton biomass in the Gulf of Naples (Ribera d'Alcală et al., Reference Ribera d'alcală, Conversano, Corato, Licandro, Mangoni, Marino, Mazzocchi, Modigh, Montresor, Nardella, Saggiomo, Sarno and Zingone2004) and in the highly oligotrophic eastern Mediterranean (Siokou-Frangou et al., Reference Siokou-Frangou, Christou, Fragopoulu and Mazzocchi1997) confirming thus that this species is able to accomplish its metabolic needs even at a low autotrophic biomass. This was demonstrated by in situ feeding experiments conducted by Mazzocchi & Paffenhöfer (Reference Mazzocchi and Paffenhöfer1998). These authors confirmed that C. furcatus is the only species of the genus Clausocalanus that inhabits epipelagic waters during summer confirming a preference for the warmer waters. However other species belonging to the same genus migrate towards deep layers below the thermocline (Peralba & Mazzocchi, Reference Peralba and Mazzocchi2004). Therefore C. furcatus showed a wider tolerance to the increasing temperature during summer stratification in the Gulf of Gabes.
What are the factors leading to the success of small planktonic copepods in the Gulf of Gabes?
Despite the intensive predation by diverse meroplankton larvae or by other holoplankton such as chaetognaths, appendicularians and large copepods, small planktonic copepods succeed in recuperating from losses caused by predation. In fact, these zooplankters are able to perform a successful reproductive strategy. Cyclopoids, harpacticoids, poecilostomatoids and some small calanoids are egg-carrying, while the majority of large calanoids are free spawning (Huys & Boxshall, Reference Huys and Boxshall1991). This strategy was mainly encountered with cyclopoids in oligotrophic marine ecosystems (Satapoomin et al., Reference Satapoomin, Nielsen and Hansen2004). The advantage of the small species bearing egg sacs is to protect eggs against predators until they hatch and produce nauplii. Therefore they reduce the mortality rate by generating a higher number of juveniles (Zervoudaki et al., Reference Zervoudaki, Christou, Nielsen, Siokou Frangou, Assimakopoulou, Giannakourou, Maar, Pagou, Krasakopoulou, Christaki and Moraitou Apostolopoulou2007). In addition it was shown that egg viability of small egg-carrying copepods was roughly conserved after fish larval gut passage (Saint-Jean & Pagano, Reference Saint Jean and Pagano1995). This agrees with the advantage of egg-carrying copepods in coastal waters under strong predation pressure by fish larvae and juveniles. In the Gulf of Gabes, where fish larvae are very abundant in relation to active fishery (65% of the national fish production; Commissariat Général des Pêches, 1996), this reproductive strategy, by lowering the effects of predation by fish larvae, should favour the dominance of small egg-carrying copepods in the neritic waters.
It is evident that certain small copepods behave as predators of heterotrophic and mixotrophic protists rather than of autotrophic phytoplankton (Paffenhöffer, Reference Paffenhöfer1998; Turner, Reference Turner2000). This is the case of Acartia adults (Gifford & Dagg, Reference Gifford and Dagg1988), Oithona (Graneli & Turner, Reference Graneli and Turner2002), Paracalanus (Suzuki et al., Reference Suzuki, Nakamura and Hiromi1999) and even nauplii of Calanus spp. (Turner et al., Reference Turner, Levinsen, Nielsen and Hansen2001). The small fractions, mainly developmental stages, were revealed to feed on bacterioplankton while adult copepods are not able to consume picoplankton due to its very small size (Roff et al., Reference Roff, Turner, Webber and Hopcroft1995). They are both carnivorous and detritivorous, preying upon other mesozooplankton and organic aggregates. Poecilostomatoids such as Corycaeus species are described as predators of copepod nauplii (Landry et al., Reference Landry, Lehner Fournier and Fagerness1985). Omnivorous diet of small copepods belonging to the genera Paracalanus, Acartia, Oncaea, Corycaeus and Oithona was also deduced from the contents of their faecal pellets including diatom frustules, dinoflagellate thecae and tintinnid loricae (Turner, Reference Turner1991). Zervoudaki et al. (Reference Zervoudaki, Christou, Nielsen, Siokou Frangou, Assimakopoulou, Giannakourou, Maar, Pagou, Krasakopoulou, Christaki and Moraitou Apostolopoulou2007) highlighted the combined influence of low metabolic needs and omnivorous diet (based on phytoplankton, heterotrophic flagellates and ciliates) in sustaining the high production of small copepods in the northern Aegean Sea.
Tolerance to heavy pollution, as observed in the Gulf of Gabes, may also explain the high proliferation of oithonid species such as O. nana, as observed in the Bay of Toulon (north-west Mediterranean) by Jamet et al. (Reference Jamet, Bogé, Richard, Geneys and Jamet2001) who suggested that this species may be used as a biological indicator of such perturbed systems.
The adoption of a successful reproductive strategy combined with an omnivorous diet, lower metabolic needs and tolerance to pollution (O. nana) are certainly behind the prominence of small planktonic copepods in the oligotrophic waters of the Gulf of Gabes.
Copepods as indicators of water masses exchange
In addition to their role in the marine pelagic food web, planktonic copepods have been regarded as good indicators of water masses exchange (Hsieh et al., Reference Hsieh, Chiu and Shih2004). In fact, the strait of Gibraltar is a natural aperture that connects the Mediterranean Sea to the Atlantic Ocean. Seven invasive Atlantic copepod species (Calocalanus contractus, C. tenui, Acartia bifilosa, A. tonsa, Corycaeus amazonicus, Metacalanus inaequicornis and Pachos tuberosum) were recorded mainly in the offshore region of the Gulf of Gabes showing that hydrology and water masses exchange are certainly influenced by the Atlantic Tunisian Current.
CONCLUSION
The summer spatial distribution of zooplankton in the Gulf of Gabes revealed the prevalence of small planktonic copepods. The latter benefited from the remarkable dominance of heterotrophic microplankton, mainly dinoflagellates and tintinnids. Small oithonids such as Oithona similis and O. nana revealed very high densities in the inshore region intruded by salty and warm MMW. The MAW was also distinguished by the prevalence of small planktonic copepods such as Oithona nana and Clausocalanus furcatus. However, the large calanidae Nannocalanus minor dominated in the deep offshore region characterized by the presence of IW. The propagation of the Atlantic waters off the Gulf of Gabes was followed by the presence of invasive copepod species.
ACKNOWLEDGEMENTS
The authors are grateful to the whole crew of the RV ‘Hannibal’ for their considerable help during the oceanographic cruise. The authors are also thankful to Mr Kamel Maaloul for having proofread the article.
FINANCIAL SUPPORT
This work was supported by the Tunisian funded project POEMM: Planktonic and Oceanographic Ecosystem Monitoring and Management (LR02INSTM04), which was conducted by the National Institute of Marine Sciences and Technologies (INSTM) and the Biodiversity and Aquatic Ecosystem Research Unit of the University of Sfax. This paper is included in the PhD studies of Thouraya Ben Ltaief (University of Sfax and INSTM).
