Egg production and hatching success of Paracartia grani (Copepoda, Calanoida, Acartiidae) in two hypersaline ponds of a Tunisian Solar Saltern

Egg production and hatching success of Paracartia grani (Copepoda, Calanoida, Acartiidae) in two hypersaline ponds of a Tunisian Solar Saltern

Journal of Sea Research 134 (2018) 1–9 Contents lists available at ScienceDirect Journal of Sea Research journal homepage: www.elsevier.com/locate/s...

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Journal of Sea Research 134 (2018) 1–9

Contents lists available at ScienceDirect

Journal of Sea Research journal homepage: www.elsevier.com/locate/seares

Egg production and hatching success of Paracartia grani (Copepoda, Calanoida, Acartiidae) in two hypersaline ponds of a Tunisian Solar Saltern

T



Neila Annabi-Trabelsia, Rayda Kobbi Rebaia, Mohammad Alib, , M.N.V. Subrahmanyamb, Genuario Belmontec, Habib Ayadia a Université de Sfax, Faculté des Sciences de Sfax, Département des Sciences de la Vie. Unité de recherche UR/05ES05, Biodiversité et Ecosystème Aquatiques, Route soukra Km 3.5, B.P. 1171, CP 3000 Sfax, Tunisia b Ecosystem Based Management of Marine Resources Program, Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, P.O Box: 1638, Salmiya 22017, Kuwait c Laboratory of Zoogeography and Fauna, Department of Biological and Environmental Sciences and Technologies, University of the Salento, 73100 Lecce, Italy

A R T I C L E I N F O

A B S T R A C T

Keywords: Egg production rate Hatching success Salinity Paracartia grani Sfax Solar Saltern, Tunisia

Reproductive traits of Paracartia grani [percentage of spawning females, egg production rate (EPR), and hatching success (HS)] were investigated for the first time at high salinities (39–121 psu) to examine the impact of such a particular situation. The study was done in two hypersaline ponds [A1 (39–46 psu) and C31 (70–121 psu)] in Sfax Solar Saltern, central-eastern coast of Tunisia. These ponds also differed in terms of the composition and concentrations of nutritional parameters. The EPR differed significantly between the ponds (ANOVA, F = 29.45, p < 0.001). In pond A1, EPR varied between 12.7 ± 1.3 eggs female− 1 day− 1 (7 December 2009) and 14 ± 1 eggs female− 1 day− 1 (19 January 2010) with an average of 13.3 ± 0.44 eggs female− 1 day− 1. HS after 48 h of incubation were significantly higher than those after 24 h. The mean values of HS after 48 h were 42.72 ± 2.58% at pond A1 and 41.67 ± 3.92% at pond C31. The two peaks of HS (after 48 h) were observed at 15 °C in pond A1 (21 December 2009, 45.18% nauplii eggs− 1) and in C31 (4 January 2010, 48.78%) at the same temperature. This study confirms that a broad salinity tolerance allows P. grani to settle itself in environments, which are normally hostile to the development of other Acartiidae.

1. Introduction Spatial and temporal variability of egg production rate (EPR) is a well known phenomenon in marine calanoid copepods (Jónasdóttir et al., 2005; Belmonte and Pati, 2007; Souissi et al., 2008; AnnabiTrabelsi et al., 2012). The EPR of Calanoida represents most of the biomass production of the female (Sullivan and Kimmerer, 2013), and is an important life history trait to understand the in situ population dynamics (Carlotti et al., 2010; Thompson, 2012). In addition, EPR is a convenient indicator of the feeding environment and it potentially indicates the availability of food for higher trophic levels (Begum et al., 2012; Cruz et al., 2013; Garrido et al., 2013; Aguilera et al., 2013). Calanoida EPR and hatching success (HS) are affected by physicochemical conditions such as temperature (Holste and Peck, 2006; Cook et al., 2007; Holmborn and Gorokhova, 2008) and salinity (Holste and Peck, 2006; Peck and Holste, 2006). Among Calanoida, members of the family Acartiidae are typically found in coastal ecosystems (Mauchline, 1998) and dominate mesozooplankton communities in semi-enclosed areas such as estuaries, harbours, lagoons (Annabi-Trabelsi et al., 2012; ⁎

Boyer et al., 2012), and solar salterns (Kobbi-Rebai et al., 2013). Paracartia grani Sars G. O., 1904 was first described from western Norway (Sars, 1904) and more recently has been observed in coastal waters of the North-eastern Atlantic and North Sea (Gallo, 1981; Razouls et al., 2009). Rodríguez and Vives (1984) were the first to report P. grani in the Mediterranean, in Malaga harbour close to Gibraltar strait, probably involuntarily introduced as a by-product of human activities (Belmonte and Potenza, 2001). The spread of this species in the Mediterranean is restricted to coastal and confined waters (brackish or saline), demonstrating its adaptability to a broad range of environmental conditions (salinity, temperature, and oxygen concetnration) which may allow it to be a strong performer relative to indigenous species (Boyer, 2012; Boyer et al., 2012). Transport in the ballast water of ships and the discontinuous distribution of P. grani could be the result of the presence of resting eggs in its life cycle (Guerrero and Rodríguez, 1998; Boyer and Bonnet, 2013; Boyer et al., 2013), as usual among species of the family Acartiidae (Mauchline, 1998). Diouf and Diallo (1990) found that P. grani is adapted to a wide range of salinities (30–86 psu), this being the best factor explaining its

Corresponding author. E-mail address: [email protected] (M. Ali).

https://doi.org/10.1016/j.seares.2017.12.002 Received 21 June 2017; Received in revised form 14 December 2017; Accepted 18 December 2017 Available online 20 December 2017 1385-1101/ © 2017 Published by Elsevier B.V.

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20–70 cm), with salinity ranging from 40 to 400 psu (Ayadi et al., 2004). The seawater is therefore concentrated by evaporation until saturation, crystallization, and precipitation of NaCl which occur in the harvesting pans. Biweekly samples were collected from ponds A1 and C31, from 19 October 2009 until 26 April 2010 (Fig. 1).

occurrence in highly variable saline habitats. In the solar saltern of Sfax (central-eastern coast of Tunisia, southern Mediterranean Sea), P. grani was recorded at salinities ranging from 38 to 121 psu (Kobbi-Rebai, 2014). We examined whether the extreme salinity conditions in the Sfax Solar Saltern could influence the reproduction traits of P. grani with respect to the variability of nutritional parameters. To our knowledge, this is the first attempt to determine the reproduction features not only of P. grani but also of species of Acartiidae at high salinities.

2.2. Physicochemical and biological parameters Samples for environmental parameters were collected from 10 to 20 cm below the surface with a 5 L Van Dorn bottle in the central part of each pond. Temperature was measured using a mercury glass thermometer graduated in 0.1 °C and salinity was estimated using a refractometer (Zuzi C39545). The concentrations of suspended particulate matter were determined by measuring the dry weight of the residue after water filtration through a Whatman GF/C membrane. Water samples (200 ml), taken for phytoplankton, were fixed with acid Lugol's iodine (1% final concentration) and stored in the dark at 4 °C until they were analysed. Phytoplankton were counted under an inverted microscope (× 400) using the Uthermöhl method (Uthermöhl, 1958). Water samples (0.15 L) were filtered through Whatman GF/C glass fibre filters (nominal porosity 0.45 μm). These filters were immediately stored at − 20 °C until being extracted using acetone and read by spectrophotometer to determine Chlorophyll-a (Chl-a) concentration. The concentrations of Chl-a were then estimated using the equations reported by SCOR −UNESCO (1966). Samples of zooplankton were taken by filtering 100 L water through a 200-μm mesh net and preserved in 5% formalin solution. Because of the small size of Acartiidae, the sampling net captured only late developmental instars (mostly adults and copepodites C5). Males and females of Acartiidae were then identified according to morphological characteristics (Rose, 1933). The sex ratio of P. grani was determined by counting adult females per males. Zooplankton taxa were enumerated and counted in a Dolffus chamber under a binocular microscope.

2. Material and methods We investigated the effect of environmental parameters at different salinities on the reproductive traits of Paracartia grani Sars G. O., 1904 [percentage of spawning females, EPR, and HS after 24 and 48 h of incubation] in two ponds (A1 and C31) of the solar saltern of Sfax, from October 2009 to April 2010. The ponds A1 (39–46 psu) and C31 (70–121 psu) differed in terms of salinity range as well as in terms of the composition and concentrations of feeding conditions (Kobbi-Rebai et al., 2013). 2.1. Study site and sampling The Sfax Solar Saltern (central-eastern coast of Tunisia, located at about 34°39′ N and 10°42′ E) is an artificial system formed of consecutively connected ponds (reservoir, evaporation, concentration, and crystallization), extending over a total area of 1500 ha along the southern coast of Sfax. This ecosystem is separated from the sea by artificial seawall of red silt (Fig. 1). The ponds are shallow (depth,

2.3. EPRs and HS of Paracartia grani Females of P. grani were isolated with a pipette under light anasthesis with 10% MgCl2 solution (maximum 3 min) under a stereomicroscope. Anasthesis was applied to allow operators to isolate specimens and follows the protocols of Belmonte and Pati (2007). For EPR estimations, 30 females were placed in individual incubation wells, each with 35 ml of original seawater filtered through GF/C glass fibre filters 47 mm in diameter (nominal porosity 0.45 μm). After 24 h, the eggs were counted and collected from the bottom. The percentage of spawning females was calculated as the number of females producing eggs out of the total number of females incubated. The single-well incubation was designed to obtain individual variability of EPR's and HS’. To avoid cannibalism of mothers on their own eggs, a spawning chamber consisting of an upper and a lower level was placed inside a cylindrical “outer” housing. The well's three components were made of plexiglass. After eggs were laid, they fell through the mesh (200 μm) into the brooding chamber. The EPR was expressed as the number of eggs produced per female per day (eggs f− 1 d− 1). Eggs found in each beaker were transferred and combined in a 50-ml Petri dish filled with filtered original sea water and incubated at the spawning temperature. On 23 November 2009, P. grani in C31 pond produced a second type of eggs. These eggs were morphologically different with long spines on the chorion and were considered to be resting eggs (Guerrero and Rodríguez, 1998). Morphologically different eggs (e.g., the spiny ones) were separately considered. HS experiments were run twice with eggs incubated for 24 and 48 h, respectively. HS was determined after 48 h of incubation of only eggs with a smooth surface, by counting the number of nauplii. Fig. 1. Locations of the ponds A1 and C31 in the Sfax saltern (Tunisia).

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Fig. 2. Environmental parameters at the sampling ponds A1 and C31 every 15 days. a - salinity (psu); b - temperature (°C); c - Suspended matter (mg L− 1).

During the study period, temperature ranged from 14 °C in January 2010 to 25 °C in March 2010 in pond A1. In C31 (Fig. 2b), temperature ranged from 15 °C in January 2010 to 27 °C in March 2010. Water temperature did not differ significantly between the two ponds (Table 1). Mean values of the concentration of suspended particulate matter were 291.33 ± 91.15 mg L− 1 and 558.95 ± 155.22 mg L− 1 in A1 and C31, respectively. In A1, concentrations of suspended particulate matter varied between 140 mg L− 1 (October 2009) and 500 mg L− 1 (April 2010). In C31 concentrations of suspended particulate matter ranged from 230 mg L− 1 (October 2009) to 785 mg L− 1 (January 2010) (Fig. 2c). Significant difference in the concentrations of suspended particulate matter (ANOVA, F = 33.27, p < 0.001) was found between the two ponds (Table 1). The mean values of total phytoplankton abundance were 58.19 × 103 ± 22.25 × 103 cells L− 1 and 36.20 × 103 ± 16.07 × 103 cells L− 1 in ponds A1 and C31, respectively (Table 1). The concentration of phytoplankton differed significantly between ponds (ANOVA, F = 4.63, p < 0.05) (Table 1). Diatoms dominated the phytoplankton community in A1 and varied between 13.5 × 103 cells L− 1 and 64.2 × 103 cells L− 1, while dinoflagellates dominated in C31 and ranged between 5.5 × 103 cells L− 1 and 59.2 × 103 cells L− 1 (Fig. 3). The concentration of diatoms differed significantly between ponds (ANOVA, F = 53.17, p < 0.001). The concentration of dinoflagellates was higher in A1 than in C31 but without any significant difference (Table 1). The mean values of

2.4. Statistical analysis A principal component analysis (PCA) based on a correlation coefficient matrix among parameters at each pond was used to reveal relationships between physicochemical and biological parameters. A Pearson's correlation analysis was applied to environmental data to identify any relationships with EPR. In addition, one-way ANOVA analysis, followed by a post-hoc comparison using Tukey's test, was applied to examine the difference in physicochemical factors and biological parameters among the ponds. Statistical differences were considered to be significant if p < 0.05. All statistical analyses were performed using the statistical program XL.

3. Results 3.1. Environmental parameters Temporal variation of salinity and other physicochemical parameters (water temperature and suspended particulate matter) recorded at the sampling ponds are presented in Fig. 2. During the studied period, average salinity was 42.6 ± 1.95 psu in A1 and 92.01 ± 16.40 psu in C31 (Fig. 2a). In A1, salinity varied between 39 (January 2010) and 46 psu (April 2010), while in C31 salinity ranged between 70 (October 2009) and 121 psu (March 2010). The salinity of the two ponds differed significantly (ANOVA, F = 170.74, p < 0.001) (Table 1). 3

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Table 1 Parameters of physicochemical and biological factors and reproductive traits of Paracartia grani Sars G. O, 1904 (mean ± SD) in ponds A1 and C31. Parameters of physicochemical and biological

Ponds

F-value (df)

Factors and reproductive traits (mean ± SD)

A1

C31

Physicochemical parameters Salinity (psu) Temperature (°C) Suspended matter (× 103 mg L− 1)

42.6 ± 1.95 19.3 ± 3.26 291.33 ± 91.15

92.01 ± 16.40 20.4 ± 3.75 558.95 ± 155.22

170.74 (21)*** 0.41 (21) 33.27 (21)***

Biological parameters Total phytoplankton density (× 103 cells L− 1) Diatom (× 103 cells L− 1) Dinoflagellate(× 103 cells L− 1) Chlorophyll-a (mg− 1) Total density of P. grani (× 103 ind m− 3) Sex-ratio (F/M)

58.19 ± 22.25 35.47 ± 15.03 17.72 ± 8.58 0.049 ± 0.014 5.10 ± 3.58 2.33 ± 0.64

36.208 ± 16.07 6.67 ± 2.81 27.03 ± 15.91 0.034 ± 0.009 1.18 ± 1.19 3.68 ± 1.9

4.63 (21)* 53.17 (21)*** 3.97 (21) 5.15 (21)* 63.47 (21)*** 2.15 (21)

Reproduction traits parameters EPR (eggs female− 1 day− 1) Percentage of spawning females (%) Hatching success after 24 h (% naupli eggs− 1) Hatching success after 48 h (% naupli eggs− 1)

13.3 ± 0.44 78.05 ± 9.77 21.11 ± 1.42 4.72 ± 2.58

12.1 ± 0.56 85.08 ± 13.68 20.46 ± 2.16 41.67 ± 3.92

11.92 (21)*** 1.74 (21) 1.81 (21) 0.54 (21)

Results of one-way ANOVA analysis. F values: between groups mean square/within-groups mean square. *Significant difference between sampled ponds: (*p < 0.05, **p < 0.01, ***p < 0.001).

chlorophyll-a (Chl-a) concentration were 0.049 ± 0.014 mg L− 1 and 0.034 ± 0.009 mg L− 1 in ponds A1 and C31, respectively (Table 1). The highest values (0.068 mg L− 1) and (0.048 mg L− 1) were observed during spring (24 April 2010) in the ponds A1 and C31, respectively (Fig. 3). The Chl-a concentrations of the two ponds differed significantly (ANOVA, F = 5.15, p < 0.05) (Table 1).

3.4. Egg production rate (EPR) The EPR for P. grani differed significantly between the ponds (ANOVA, F = 29.45, p < 0.001) (Table 1). In pond A1, EPR at 24 h varied between 12.7 ± 1.3 eggs female− 1 day− 1 (7th December 2009) and 14 ± 1 eggs female− 1 day− 1 (19 January 2010) (Fig. 4a) with an average of 13.3 ± 0.44 eggs female− 1 day− 1. The highest value of EPR (14 eggs female− 1 day− 1) was observed at 17 °C and 39 psu in A1. The EPR correlated negatively with salinity (r = −0.662, p < 0.05) and temperature (r = − 0.716, p < 0.05), and positively with diatoms (r = 0.671, p < 0.05). In C31, the EPR of P. grani oscillated between 11 ± 1.33 eggs female− 1 day− 1 (19 October 2009) and 13.1 ± 1.37 eggs female− 1 day− 1 (1 February 2010) (Fig. 4b) (mean ± SD = 12.1 ± 0.56 eggs female− 1 day− 1). The EPR correlated positively with suspended particulate matter (r = 0.775, p < 0.05) with the highest value (13.1 eggs female− 1 day− 1) observed at 15 °C and 96 psu.

3.2. Paracartia grani abundance and reproductive traits The mean values of P. grani abundance at each pond were 5.10 ± 3.58 × 103 ind·m− 3 (A1) and 1.18 ± 1.19 × 103 ind·m− 3 (C31). The abundance of P. grani had a peak value of 10.25 × 103 ind·m− 3 (February 2010), and the species disappeared at the end of March 2010 in the pond A1 (Fig. 4a). In contrast, in pond C31, P. grani adults disappeared on 15 February and re-appeared at the end of March and the beginning of April (Fig. 4b) (< 2 × 103 ind·m− 3). The highest abundance was recorded on 23 November 2009 (3.6 × 103 ind·m− 3) (Fig. 4b). The abundances of Paracartia grani differed significantly between the two ponds (ANOVA, F = 63.47, p < 0.001, Table 1). In A1, the abundance of P. grani showed a negative correlation with salinity (r = − 0.627, p < 0.05) and temperature (r = − 0.628, p < 0.05). In C31 the abundance showed a negative correlation only with salinity (r = −0.775, p < 0.05). The mean value of the P. grani sex ratio (F/M) was 1.71 ± 1.2 and 2.7 ± 2.33 in A1 and C31, respectively (Table 1). The sex ratio did not differ significantly between the ponds (ANOVA, p < 0.05) and showed a negative correlation with temperature (r = − 0.663, p < 0.05).

3.5. Hatching success (HS) Hatching success (HS) after 24 h was 21.11 ± 1.42% and 20.46 ± 2.16% in A1 and C31, respectively (Fig. 6). HS did not differ significantly between the ponds (ANOVA, p < 0.05) and showed a negative correlation with diatom abundance (r = −0.530, p < 0.05) and Chl-a concentration (r = − 0.699, p < 0.05) in pond A1. HS after 48 h of incubation were significantly higher than those after 24 h because eggs layed at the end of the incubation period have had a chance to hatch. The mean values of HS after 48 h were 42.72 ± 2.58% at pond A1 and 41.67 ± 3.92% at pond C31 (Fig. 5). The two peaks of HS (after 48 h) were observed at 15 °C in pond A1 (21 December 2009, 45.18% nauplii eggs− 1) and in C31 (4 January 2010, 48.78%) at the same temperature. In A1, the axes F1 and F2 of the PCA explained 54.10% of the total variance (F1 = 31.08% of total variance; F2–23.02%) (Fig.6). The PCA identified positive relationships between total abundance of phytoplankton, Chl-a concentration, diatoms, and EPR. The PCA reveals that EPR and diatom were closely coupled (r = 0.671, p < 0.05). In contrast, EPR was negativeley correlated with salinity (r = −0.662, p < 0.05) and temperature (r = − 0.716, p < 0.05). Salinity, temperature and total abundance of P. grani load negatively on the F2 axis. In C31 (Fig. 6), the component axes F1 and F2 explained 58.93% of total variance. The first axis component F1 (37.94% of total variance)

3.3. Percentage of spawning females In A1, the percentage of spawning females varied from 60 to 100% (Fig. 4a). It showed a positive correlation with Chl-a concentration (r = 0.740, p < 0.05) and the abundance of diatoms (r = 0.5, p < 0.05). In C31, the percentage of spawning females varied from 50 to 100% (Fig. 4b) and was correlated negatively with salinity (r = −0.667, p < 0.05) and the abundance of dinoflagellates (r = −0.612, p < 0.05). The percentage of spawning females did not differ significantly between the two ponds (ANOVA, p < 0.05).

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Fig. 3. Seasonal variation in total phytoplankton abundance (× 103 cells L− 1), diatom, dinoflagellate, and Chl-a concentration (mg L− 1) at the sampling ponds A1 and C31.

with salinity between 34 and 40 psu. Data from the present study refer to a salinity range of 39–121 psu and, consequently, can be used to complete the salinity-abundance curve in hyperhaline conditions. P. grani adults were dominant during winter in A1 and disappeared completely from the water column from 15 March 2010 onwards. According to many data (e.g., Mauchline, 1998) copepods living in variable ecosystems can disappear from the water column when environmental conditions become unfavourable. In C31, P. grani adults were present from the end of March until 26 April 2010. The appearance of P. grani adults in April is probably the result of the hatching of resting eggs that were produced on 23 November 2009. Previous investigations (Guerrero and Rodríguez, 1998) demonstrated the production of resting eggs by P. grani that allow the species to survive during unfavourable conditions and provide a pool of potential recruits in favorable conditions (Boyer and Bonnet, 2013; Boyer et al., 2013) which seem to be in April in C31 when salinity showed a decline below 105 psu. In both ponds, the sex-ratio of P. grani was strongly skewed, with

selected positively abiotic variables (salinity and suspended particulate matter) and biotic variables (total phytoplankton abundance, total abundance of dinoflagellates, EPR, and abundance of P. grani). The suspended particulate matter and EPR were significantly coupled (r = 0.775, p < 0.05). The second axis component F2 (20.99% of total variance) selected negatively salinity and percentage of spawning females, both being significantly coupled (r = − 0.667, p < 0.05). 4. Discussion Calanoid copepods found in coastal confined waters are often well adapted to cope with salinity fluctuations (Marcus and Cheng-Sheng, 2005). During the present study, P. grani showed that its abundance was negatively correlated with salinity (a thalassophylic characteristic according Kobbi-Rebai et al., 2013). In fact, the abundance of P. grani was substantially lower in C31 relative to A1. In addition, at high salinities (105–121 psu), P. grani was completely absent. Boyer (2012) and Boyer et al. (2012) showed that abundance of P. grani is positively correlated 5

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Fig. 4. Spatial and temporal variation in the abundance of Paracartia grani Sars G. O., 1904 population, percentage of spawning females, and egg production rate (EPR) of P. grani in ponds A1 and C31 in the Sfax Saltern (Tunisia). Bars: standards deviation.

The EPR's of P. grani obtained from both ponds in this study are comparable with those reported by Boyer et al. (2013) (12.4 ± 6.6 eggs female− 1 day− 1), but different from values obtained by Annabi-Trabelsi et al. (2012) (2.08 ± 0.5–7.9 ± 0.6 eggs female− 1 day− 1), or by those observed by Rodríguez et al. (1995) (79 eggs female− 1 day− 1). It was also found that P. grani had a higher EPR in A1 (13.3 ± 0.44 eggs female− 1 day− 1) than in C31 (12.1 ± 0.56 eggs female− 1 day− 1). Additionally, in the present study, the peak value of EPR was recorded in winter in both ponds. Boyer et al. (2013) observed the highest values of P. grani EPR (28 eggs female− 1 day− 1) in summer. Annabi-Trabelsi et al. (2012) recorded, for the same species, a maximum EPR of about 8.8 ± 4.9 eggs female− 1 day− 1 during autumn. The present study did not report EPR values from summer, and the differences found in autumn period were probably due to environmental conditions in the various investigations in solar salterns versus lagoons. The significant difference in EPR between the two ponds A1 and C31 confirms that this parameter is impacted by different factors in each pond. The complicated spatial and temporal variations in environmental factors such as temperature, salinity, food quantity, and quality may result in a wide range of EPR from 1 eggs female− 1 day− 1 to 50 eggs female− 1 day− 1 in Acartiidae copepods (Jónasdóttir and Kiørboe, 1976; Castro-Longoria, 2003; Diekmann et al., 2012; Aguilera et al., 2013). Many authors showed that the EPR of Acartiidae depends primarily on temperature (Devreker et al., 2004, 2005; Cook et al., 2007;

adult females outnumbering males. In fact, sex ratio of adult Acartiidae skewness is primarily due to differential mortality of the sexes in the adult stage (Hirst et al., 2010). Mortality rates of adult Acartia are conditioned by male preferencial predation (Hirst et al., 2010). In our case, however, the female survival could be due to their higher resistance to high salinities than males (Kobbi-Rebai, 2014). Also, field and laboratory populations of Calanoida tend to be female-dominated (Kiørboe, 2006). In the present study, the sex ratio of P. grani showed a negative correlation with temperature in A1 confirming that temperature has an influence on the sex ratios of Calanoida (Devreker et al., 2010; Dur et al., 2012). It has been reported that phytoplankton diversity was correlated with the fecundity of Acartia spp. considering as a percentage of spawning females (Ianora et al., 1996). In this study, the percentage of spawning females did not differ significantly between the two ponds but showed different correlations. It was positively correlated with Chla concentration and diatom abundance in A1 and negatively correlated with the salinity and the dinoflagellate abundace in C31. Boyer et al. (2013), in a different salinity condition, demonstrated a negative correlation with Chl-a. Evidently, Chl-a is not directly responsible for fecundity but it is simply affected by the same external conditions. Indeed, in ponds A1 and C31, P. grani is not limited by food quantity as expressed by Chl-a concentrations, knowing that food saturated condition for Acartia is defined at 1 μg L− 1 (Uye, 1981). Furthermore, Dutz (1998) found a reduction of copepod fecundity in Acartia females exposed to dinoflagellates. 6

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Fig. 5. Spatial and temporal variations in hatching success (HS) after one day and two days in ponds A1 and C31. Grey histograms: HS at one day after spawning; Black histograms: after a 2 days.

However, many studies have indicated that several diatom species decrease the reproductive success of copepods, by directly affecting EPR (Halsband-Lenk et al., 2005; Ianora et al., 2008; Neffati et al., 2013). Indeed in C31, in the presence of low diatom and high dinoflagellate abundances, we detected a positive correlation of the P. grani EPR with Suspended Particulate Matter. Annabi-Trabelsi et al. (2012) found the highest P. grani EPR was recorded during the autumn period, which is characterized by high particulate organic carbon concentrations. This observation agrees with the fact that Acartiidae shift from a herbivorous to detritivorous behaviour with the changing season (Liu and Dagg, 2003; Broglio et al., 2004; Liu et al., 2005; Hu et al., 2012) and to feed on detritus more than on phytoplankton (Roman, 1984). Their omnivorous feeding behaviour allows them to survive and reproduce under different diets (Saiz et al., 2007), and different factors that can affect their growth in different times. In the solar saltern ponds A1 and C31, no significant correlation was found between the temperature and HS of P. grani. The same finding was reported by Boyer et al. (2013), who showed that the influence of temperature in a Mediterranean lagoon on P. grani HS was not statistically significant. In most cases, physicochemical factors controlling HS are unclear even if temperature has sometimes been considered a factor influencing the hatching of copepod eggs (Laabir et al., 1995).

Henriksen et al., 2007; Devreker et al., 2009; Min-Chul et al., 2013). The results herein showed a negative correlation of temperature on EPR of P. grani only in A1. Previously, Annabi-Trabelsi et al. (2012) reported that temperature was determinant and positively correlated with EPR for P. grani in a northern African lagoon (salinity range 34.2–44.2 psu). This contrasting results, obtained by the same authors, in the same geographical region, with the same species, in similar salinity conditions, simply demonstrates that temperature (even if significantly correlated) cannot be considered as a true and sole affecting factor. At higher salinities in C31 (70–121 psu), no correlation has been shown between temperature and EPR. In solar saltern ponds, strong values of salinity should impact significantly upon P. grani EPR more than temperature. Also in the case of Salinity, however, the two situations here studied do not allow us to consider this parameter as undoubtedly affecting the EPR. In fact, in the A1 pond EPR appears as negatively affected by salinity, but no significant correlation is derivable from data coming from the C31 pond. It seems that also Salinity, as Temperature, had no significant linear relationship with EPR and it cannot be considered as a true affecting factor. Gusmão and McKinnon (2009) reported that the EPR was also correlated with the nutritional quality of food. The positive impact of diatoms on Acartia EPR was previously observed by Hassett (2004).

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Fig. 6. Principal component analysis (PCA) (Axis I and II) made on the total abundance of Paracartia grani (T-P. grani), percentage of spawning females (% SF), eggs production rates (EPR), hatching success after 24 h (HS 24) and after 48 h (HS 48) and that of the total abundance of phytoplankton (T-Phyto), diatoms, dinoflagellates, chlorophyll-a concentration (Chla), salinity, temperature and suspended particulate matter (SM) in ponds A1 and C31.

In the present study, HS (after 24 h) of P. grani was negatively correlated with Chl-a concentration and with diatoms in A1. However, studies on other Acartiidae showed a positive relationship between the occurrence of diatoms and HS (Jónasdóttir et al., 2005; Carotenuto et al., 2006; Wichard et al., 2008). The studies of Poulet et al. (1994) and Ianora et al. (1995) suggest particularly that diatoms contain toxins or inhibitors that may suppress normal development of copepod eggs. Ianora et al. (2003) showed, in the pelagos, that diatoms often reduce fecundity, HS, or both, in copepods. On the other hand, Jónasdóttir and Kiørboe (1976) showed that HS was positively affected by diatom extracts. In the present study, negative effects were only evident at high diatom concentrations as observed in A1. In summary, the results of this study confirm that a broad salinity tolerance allows P.grani to affirm itself in environments with wide salinity variations. Consequently, salinity is an important parameter that allows defining the dimensions of the ecological niche for P.grani regarding the reproduction. The realized niche takes into account fluctuations in food resources. The copepod species in this study was known mostly from coastal areas and brackish waters (Rodríguez and Vives, 1984; Belmonte and Potenza, 2001; Annabi-Trabelsi et al., 2006; Boyer et al., 2012). Here it is reported for the first time from the extreme saline conditions of the salterns which negatively affect the existence of most coastal species. Such an adaptation to a wide salinity range is interesting and probably suggests that the species success can adapt to a wide variations in environmental conditions. The P. grani ruderality, and the presence of resting eggs, could have a high utility in production of food source for fish, since there is a high demand for calanoid nauplii in aquaculture (Marcus and Murray, 2001; Drillet et al., 2011). Furthermore, it is worth comparing the seasonal abundance, distribution, and reproduction of P. grani in both solar salterns and adjacent areas of the Mediterranean Sea throughout the year could allow a comprehensive assessment of the role of salinity and food type on its reproduction.

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