- Email: [email protected]
Phytoplankton dynamics related to water mass properties in the Gulf of Gabes: Ecological implications
Journal of Marine Systems 75 (2009) 216–226
Contents lists available at ScienceDirect
Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s
Phytoplankton dynamics related to water mass properties in the Gulf of Gabes: Ecological implications M. Bel Hassen a,⁎, Z. Drira a,b, A. Hamza a, H. Ayadi b, F. Akrout a, S. Messaoudi a, H. Issaoui c, Lotfi Aleya d, Abderrahmen Bouaïn b a b c d
Institut National des Sciences et Technologies de la Mer, 28 rue 2 mars 1934 2025 Salammbô. Tunisia Université de Sfax Route soukra Km 4 BP 1171 CP 3000 Sfax, Tunisia Centre de Biotechnologies de Sfax, B.P "K". 3038 Sfax, Tunisia Université de Franche-comté, Laboratoire de Chrono-Environnement, UMR CNRS 6249 1, Place Leclerc, F-25030 Besançon cedex, France
a r t i c l e
i n f o
Article history: Received 25 December 2007 Received in revised form 1 September 2008 Accepted 25 September 2008 Available online 10 October 2008 Keywords: Phytoplankton Photosynthetic pigments Atlantic Water Mediterranean Water Gulf of Gabes
a b s t r a c t The spatial distribution of chlorophylls and carotenoids was recorded throughout the Gulf of Gabes (South Ionian Sea) in March 2007, and was related to patterns of the physical structure and the nutrient concentrations. Two distinct water masses were identified based on the temperature and salinity (T–S) analysis: a cool and less salty Modified Atlantic Water (MAW) and a saltier Mediterranean Mixed Water (MMW). There was no significant difference in the mean nitrogen and phosphate concentrations between MMW and MAW, although the silica values were significantly higher in MAW. The Integrated chlorophyll a mean value was about 4 mg m− 2, with a maximum of 13 mg m− 2 at MAW stations. Higher Chlorophyll a records in typical MAW stations were mainly due to chlorophytes, which contributed up to 58% of the pigments concentrations in the MAW and about 46% in the MMW. The contribution of chlorophytes to total Chlorophyll a was found to be relatively stable throughout the water column. The contribution of diatoms, which were twofold higher in the MMW than in the MAW, did not exceed 17% of chlorophyll a and was mainly due to subsurface maxima. The chlorophytes, pelagophytes, prymnesiophytes and cryptophytes all together accounted for more than 77% of total chlorophyll a in the MAW and about 67% in the MMW. There were statistically significant differences between MMW and MAW in the pigment contribution of cyanobacteria and pelagophytes. These two taxa accounted for 13% and 24% of chlorophyll a respectively in the MAW and MMW indicating that these differences concerned phytoplankton classes at relatively low contributions to total chlorophyll a. © 2008 Published by Elsevier B.V.
1. Introduction The Gulf of Gabes, situated in the south Ionian Sea, occupies a wide continental shelf area. The existence of salinity minima in the region is attributed to the Modified Atlantic Water (MAW) was firstly described by Brandhost (1977). Using climatological datasets and high-resolution numerical simulations, Béranger et al. (2004) gave further support to these observations. These authors pointed out a ⁎ Corresponding author. Tel.: +216 71 730 420; fax: +216 71 732 622. E-mail address: [email protected] (M. Bel Hassen). 0924-7963/$ – see front matter © 2008 Published by Elsevier B.V. doi:10.1016/j.jmarsys.2008.09.004
seasonal variability along the Tunisian coast, describing that the Atlantic water was generally stronger during the winter and flowed in the upper 100 m, while they revealed a weakening of the advection during the summer. Similar observations were reported by Poulain and Zambianchi (2007) using Lagrangian drifters data. They particularly showed that, during winter, the MAW strongly flowed along the Tunisian coast through the shallow Gulf of Gabes. The physical forcing resulting from the MAW advection could confront distinct water masses and generate potential mixing of water from coastal and/or open-ocean origin. This water mixing may have an impact on the phytoplankton
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
populations, which experience large variations in their abundance, composition and size structure due to the dynamic nature of their environment (Pelegrí et al., 2005). Interactions between the physical processes and the biological features have been investigated in frontal regions showing that the physical forcing affects the abundance and composition of phytoplankton directly (Estrada et al., 1999; Gomez et al., 2000). Estrada et al. (1999) found high Chlorophyll a concentration and diatoms dominance inshore the Catalan Front. However, offshore of the front the diatoms were scarce and the phytoplankton assemblages were dominated by coccolithophorids. A taxonomic structure with a predominance of diatoms on the Mediterranean side and of dino-
217
flagellates and microzooplankton on the Atlantic side were also observed in the straits of Gibraltar (Gomez et al., 2000). Frontal structures are known to enhance phytoplankton production due to fertilization processes and to favour the growth of diatoms (Claustre et al., 1994) as well as dominance of the small-sized plankton (Casotti et al., 2000). Following this evidence of water mass control of phytoplankton communities at the Mediterranean, the present paper investigates the phytoplankton community in the Gulf of Gabes. Southern Mediterranean is particularly deficient in this type of analysis and this paper describes a high spatial resolution using the pigment biomarkers to characterize the community composition in relation to the water masses in the
Fig. 1. Sampling sites and the 50 m, 100 m and 200 m isobaths in the Gulf of Gabes.
218
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Table 1 Pigments markers, conversion factors and contribution of different phytoplankton groups to chlorophyll a Diatoms
Dinoflagellates
Prymnesiophytes
Cryptophytes
Chlorophytes
Pelagophytes
Cyanophytes
Pigment marker
Fucoxanthin
Peridinin
Hex
Alloxanthin
Chlorophyll b
But
Zeaxanthin
Conversion factor MMW (n = 54) MAW (n = 35)
(1.25)a 16.3 8.2
(1.00)a 5.1 6.6
(0.80)a 4.9 10.7
(1.60)a 2.5 3.5
(1.50)a 46.7 57.7
(1.20)b 13.0 6.0
(2.00)c 11.2 6.9
Conversion factors were used to determine the different amounts of the algal classes to chlorophyll a. Hex = 19′-hexanoyloxyfucoxanthin and But = 19′-butanoyloxyfucoxanthin. Values are derived from: a Casotti et al. (2000); b Peeken (1997); c Kana and Glibert (1987).
region. Our results indicate that water mass have a manifest influence on both the nutrient and phytoplankton communities field at the southern Mediterranean. 2. Methods 2.1. Stations locations Fig.1 shows the locality of the sampling sites. Three sectors were investigated: the offshore northeast sector including station 1 to station 11, the coastal southern sector from station 16 to station 23 and a transect joining the two previous areas comprising station 12 to station 15. Sampling was performed during a cruise on board the R/V Hannibal from 16 to 19 March 2007 in the Gulf of Gabes. Samples locations were selected in order to sample different types of water masses and in order to characterize variability across the Modified Atlantic Water (MAW), which was documented to be distributed within this area, east from 12°E longitude (Béranger et al., 2004; Poulain and Zambianchi, 2007). 2.2. Samples collection and CTD profiles Water samples were collected using 12 L Niskin bottles on a Seabird rosette sampler deployed with CTD (Seabird 9 underwater unit). Sampling occurred at three depths (2 m, 25 m and near the bottom) at the stations less than 50 m deep (i.e., coastal stations) or five depths at the stations deeper than 50 m (2 m, 10 m, 20 m, 50 m and near the bottom). This increase of the sampling resolution within the first 50 m of the offshore stations was aimed at better characterizing the MAW vertical variability, which was documented to flow in the surface layer during this period of the year (Béranger et al., 2004). Sub-samples (2 L) for the pigments analysis were filtered through 47 mm-diameter glass fibre filter Whatman, GF/F. Filters were then immediately stored at −20 °C for a subsequent pigment analysis. Samples for the nutrients determination were stored at −20 °C until analysis with an automatic analyser type 3 (BRAN + LUEBBE).
2.3. Pigments analysis In order to analyse phytoplankton chlorophylls and carotenoids, filters were cut into small pieces and sonicated in 100% acetone to extract the pigment. The homogenates were then centrifuged to remove cellular and glass filters debris and the supernatant was filtered through a nylon 0.45 µm filter. These extracts were then analysed for pigment content using the reverse phase High Performance Liquid Chromatography (HPLC) technique derived from (Van Heukelem et al., 1992). The analyses were performed on a HP 1100 system equipped with an Eurospher — 10 0 C18 (250 × 4.6 mm × 5 µm) column and with a multi-wave length UV detector. The pigments were separated using a non-linear binary gradient using a solvent A composed of 80% methanol:20% ammonium acetate (0.5 M adjusted at pH 7.2) and a solvent B composed of 100% acetonitrile. Chlorophylls and carotenoids were detected and quantified by absorbance at 440 nm. Amounts of pigments were estimated from the areas under the peak of the individual components. Calibrations were made using standard samples acquired from DHI Water and Environment Institute (Hørsholm, Denmark). The pigments names were abbreviated as follows: Chlorophyll a (Chl a), Chlorophyll b (Chl b), Chlorophyllids (a) Fucoxanthine (Fuco), 19'-hexanoyloxyfucoxanthin (Hex), 19'-butanoyloxyfucoxanthin (But), Peridinin (Peri), Alloxanthin (Allo) and Zeaxanthin (Zea). 2.4. Calculations deduced from pigment concentrations In order to evaluate the contribution of different phytoplankton groups to the chlorophyll a biomass, we used the ratio of chlorophyll a: diagnostic pigment extracted from different literature sources and already used in the north Ionian Sea by Casotti et al. (2000) (Table 1). The criteria for the adoption of these pigment ratios were based on the proximity of the investigated site and the similarity in the physical forcing, mainly influenced by the Atlantic water advection.
Fig. 2. Vertical profiles of (a) density (kg m− 3), (b) salinity (P.S.U) and (c) temperature (°C) according to a gradient of distance to the coast. Distance on x axis is scaled in km from the starting point of the section: 10.05 E, 33.90 N, the ending point is located at the most distant station: 13.05E, 35.05 N. The section width includes all the sampled stations.
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
219
220
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
stations to the east of 13°E longitude (i.e. stations 4, 5 and 6) and was characterized by salinities fluctuating between less than 37.5 PSU, in their upper surface water and to 38.5 PSU, in deep water. The density profiles clearly presented the variability between the three identified groups (Fig. 4). Groups A and C deeper than 20 m were composed of dense water with density values higher than 27.6 (Fig. 4a and c). This presumably reflected varying degrees of mixing of Mediterranean Waters with other shore water masses and we designated them as Mediterranean Mixed Waters (MMW). Group B stations and group C surface water were composed of less dense water (Fig. 4b and c). They corresponded to the salinity minima considered as characteristics of the Modified Atlantic Water (MAW). As for station 7, the less dense surface water was attributed to the MAW whereas the deep water was attributed to the MMW. 3.2. Nutrient and pigment distributions
Fig. 3. T–S data from the CTD profiles. Group (A) data represent coastal stations situated west from 12°E longitude (i.e. from station 12 to station 23) and are labelled with (+) symbol. Group (B) data represent stations situated between 12°E and 13°E longitude (i.e. stations 1, 2, 3, 7, 8, 9,10 and 11) and are labelled with (⁎) symbol. Group (C) data represent stations situated east from 13°E longitude (i.e. stations 4, 5 and 6) and are labelled with (ο) symbol.
2.5. Statistical analyses A single factor analysis of variance (ANOVA) was conducted to statistically assess variations in the mean fraction of chlorophyll a of each phytoplankton taxon and the mean nutrient concentrations within the identified water masses. The statistical analyses were performed with XLSTAT software for Windows. 3. Results 3.1. Physical water characterization A coast offshore (west–east) section allowed to show temperature, salinity and density fields Fig. (2). Density variations mainly correlated with salinity (Fig. 2b) (R2 = 0.926, P b 0.001), whereas no correlation was found with temperature (Fig. 2c). It may be noted that the 27.6 isopycnal, delimiting the zone of salinity minima, corresponded to the isohaline of 37.5 which was used to define the interface between the Atlantic and Mediterranean water in the Alboran Sea (Rodriguez et al., 1998). The T–S plot (Fig. 3) identified three major water groups. The first group, designated as A, included coastal stations situated to the west of 12°E longitude and was characterized by high temperature (N16.3 °C) and salinity (N37.5 PSU). The second group, designated as B, represented the stations situated between 12°E and 13°E longitude (i.e. stations: 1, 2, 3, 7, 8, 9 ,10 and 11) with low records in salinity (b37.5 PSU) and temperature. It is worth noting that for station 7, surface water characteristics were similar to those of group B, whereas the deep water had salinity values close to those of group A. The third group, designated as C, incorporates
Nitrate concentration showed some local maxima in the zones of minimum salinity; and in some bottom stations, it showed a signal of surface depletion in the coastal area (Fig. 5a). Phosphate concentration (Fig. 5b) generally low (b0.2 µM) was higher in the coastal bottom stations. The nitrate-to-phosphate ratio (N:P) was lower than 20 (Fig. 5c), the lowest values were recorded within the coastal zone and in the salinity minima area. Silica (Fig. 5d) exhibited high values in the offshore area, mainly within the zone limited by the 27.6 isopycnal, whereas minima were recorded in the west coastal side of this limit. Nitrate and the phosphate did not show statistically a significant difference in their mean value between both identified water masses, whereas the silica mean concentration in the MAW was statistically higher (P b 0.05) than that in the MMW level. Chlorophyll a concentrations were lower than 0.5 µg l− 1 and did not exhibit a clear spatial pattern (Fig. 5e) except for the presence of subsurface maxima. The Integration of pigments over the first 50 m in depth (Fig. 6) showed a mean chlorophyll a value around 4 mg m− 2. The highest values were recorded in the typical MAW stations with a maximum of 13 mg m− 2 in station 2. Moreover, the increasing chlorophyll a content in the typical MAW stations was mainly due to chlorophytes, whose characteristic pigment, chlorophyll b, showed a spatial pattern similar to chlorophyll a. This observation applies to some extent for the MMW coastal stations. However, the MMW stations adjacent to the MAW, namely from station 11 to station 14, exhibited the highest Chlorophyll a and the lowest chlorophyll b integrated values. The variations in fucoxanthin according to the water bodies showed some local increases in the coastal MMW, whereas their levels were rather low in the MAW. Besides, 19'-hexanoyloxyfucoxanthin (prymnesiophytes), Zeaxanthin (cyanobacteria) and Peridinin (dinoflagellates) were compounds of relative minor importance. The results of alloxanthin were not presented here since the integrated concentrations of this pigment never exceeded 0.3 mg m− 2. Chlorophyllid a concentrations fluctuated in the same order of magnitude as chlorophyll a. The highest integrated concentrations of this degraded pigment were observed in MMW stations closest to the MAW. In the MAW, the depth-
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 4. Density profiles at the investigated stations arranged along a coast-offshore direction. (a) Coastal stations situated west from 12°E longitude (i.e. from station 12 to station 23), (b) stations situated between 12°E and 13°E longitude (i.e. stations 1, 2, 3, 7, 8, 9,10 and 11) and (c) stations situated east from 13°E longitude (i.e. stations 4, 5 and 6). The density value of 27.6 is indicated by an arrow.
221
222 M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226 Fig. 5. Vertical profiles of (a) nitrate (µM), (b) phosphate (µM), (c) N:P ratio (d) Silicate (µM) and (e) Chlorophyll a (µg/l). The section details as Fig. 2. The sign (+) indicates the sampled depths. The 27.6 isopycnal is reported in the figures.
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
223
Fig. 5 (continued).
integrated chlorophyllid a did not show significant variations among the stations with concentrations values of about 5 mg m− 2. Table 1 shows the respective contribution of each taxonomic group (as estimated from the pigment ratio) to chlorophyll a. The chlorophytes contributed up to 46% of chlorophyll a at the MMW and about 58% at the MAW. Although the contribution of diatoms was twice higher at the MMW than at the MAW, it did not exceed 17% of chlorophyll a. The contribution of pelagophytes and cyanobacteria were also significantly higher at the MMW (contribution greater than 10%) than at the MAW. A single factor analysis of variance (ANOVA) was conducted to statistically assess differences in the phytoplankton community composition among MMW and MAW. It examined the mean fraction of chlorophyll a of each phytoplankton taxon with station groups MMW and MAW as the categorical variables. The results indicated significant differences between MMW and MAW in the mean fraction of chlorophyll a of cyanobacteria (p b 0.02) and pelagophytes (p b 0.05), whereas no significant differences were found for the other phytoplankton taxon. The respective vertical mean contributions of the main phytoplankton groups were estimated using chlorophyll a: diagnostic ratio approach (Fig. 7). The pigment ratios were assumed to be stable with depth which implicitly neglects the effect of the photo-adaptation or the nutrient status of the algae. Chlorophytes dominated over the different investigated groups in all depths. Their contributions were almost similar for depth less than 50 m; however, they decreased for MMW and increased for MAW in the 100 m deep water. Cyanophytes dominated over diatoms, pelagophytes and prymnesiophytes in the upper 20 m for both MMW and MAW, whereas their contribution dropped drastically in the deep water. The diatoms contribution did not exceed 20% at all depths. They represented the second source of chlorophyll a in the MMW deep water.
4. Discussion The chlorophyll a average integrated values found in both MMW and MAW waters were rather low compared to the typical values recorded in the Mediterranean and Atlantic waters (20 mg m− 2) of the Algerian current during the spring period (Claustre et al., 1994). They were also below the averaged value of 10 mg m− 2 recorded in the mid south western Mediterranean (Barlow et al., 1997), or the 12 mg m− 2 value found in the Sicily Straits during the summer oligotrophic conditions (Barlow et al., 1997). Even though the concentration of chlorophyll a did not exhibit significant differences between the two water masses identified, the depth-integrated chlorophyll a values showed an increase in the MAW stations. These results suggest that the MAW might present favourable conditions, in terms of nutrient content, for locally enhanced production. The lack of difference in the mean nitrogen and phosphate concentrations between the water masses suggests that nutrient brought by MAW advection were not sufficiently high to justify a difference in the trophic conditions. A difference was found for silica with significantly higher concentrations in the MAW than in the MMW. This was associated with N:P ratio (Fig. 5c) well below the accepted standard molar ratio of N: P = 16:1 set up for marine diatoms requirements (Redfield et al., 1963), suggesting a potential N-limitation of diatoms growth and might explain an incomplete utilization of silica by diatoms in the MAW. This statement can find support in the low proportion of chlorophyll a contributed by diatoms in the MAW which represented nearly half the diatoms contribution in the MMW (Table 1). The major feature of the Mediterranean basin in various regions and seasons is a phytoplankton biomass with a high contribution of prymnesiophytes (Latasa et al., 1992; Claustre et al., 1994; Bustillos-Guzman et al., 1995; Barlow et al., 1997; Vidussi et al., 2000). However, our results showed that
224
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 6. Integrated concentrations of selected diagnostic pigments arranged along a coast offshore direction. The stations numbers are indicated and the typical MMW and MAW stations are reported. The distribution of alloxanthin is not reported since the pigment concentration is below 0.3 mg m− 2.
phytoplankton composition was chlorophytes-dominated particularly within the MAW, which were consistent with the observations reported by Casotti et al. (2000) in the Gulf
of Naples (Tyrrhenian Sea) and those reported in the Gulf of Gabes during the summer period (Bel Hassen et al., 2008). In addition, the MAW was characterized by a phytoplankton
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 7. Vertical distributions of the respective mean contribution of diatoms, chlorophytes, cyanophytes, pelagothytes and prymnesiophytes to chlorophyll a biomass at each depth and calculated from pigment ratio (Table 1) and pigment concentrations.
community with a large proportion of nano-sized cells such as chlorophytes, pelagophytes, prymnesiophytes and cryptophytes which accounted for more than 77% of total chlorophyll a (Table 1). This percentage was more similar to those reported by Casotti et al. (2000) in a small coastal eddy (76.8%) and by Claustre et al. (1994 ) in the typical MAW stations of the Eastern Alboran Sea geostrophic front (65%), than that found in the Gulf of Gabes (49%) during the summer stratified conditions (Bel Hassen et al., 2008). The increasing contribution of a small-celled community generally succeeds that found during phytoplankton bloom conditions and was characteristic of oligotrophic phytoplankton community (Bustillos-Guzman et al., 1995; Vidussi et al., 2000). This indicates that the MAW phytoplankton community structure could be situated in post blooming conditions. Such a hypothesis is supported by the high level of chlorophyllid a pigment whose accumulation is indicative of senescencedeath phytoplankton (Louda et al., 2002). The vertical distribution of chlorophytes, the most abundant phytoplankton group in both MAW and MMW, did not greatly vary with depth. The coefficients of variation of chlorophyll a mean proportion contributed by chlorophytes at various depths were about 17% and 26% in MAW and MMW respectively. Moreover, the maximum chlorophyll a concentrations were mostly located near but not in the surface layer
225
(Fig. 4e). At this particular depth (10 m) chlorophytes contributions to chlorophyll a were about 45% in the MMW and 52% in the MAW. These numbers are similar to the mean depth-integrated contribution of chlorophytes (Table 1). The stable contribution of chlorophytes at different depths could be justified by the ability of this group to develop photoadaptation processes related to depth variations (Glover et al., 1986). In fact, a homogeneous distribution of flagellates over depth (mainly dominated by chlorophytes) was also described during the summer period characterized by a weak advection and a MAW confined to the bottom stratified layer (Bel Hassen et al., 2008). The stability of the chlorophytes vertical distribution within completely different hydrologic conditions suggests that chlorophytes are a cosmopolitan class of phytoplankton in this area, since they always represented a significant component of the biomass throughout surface waters and in depth profiles. The increased cyanobacteria concentrations in surface layers has been previously reported (Campbell and Carpenter, 1986; Claustre and Marty, 1995; Bustillos-Guzman et al., 1995) and might be due to their ability to be photosynthetically competent in high light intensities (Kana and Glibert, 1987) or to their ability to fix atmospheric nitrogen to meet their nitrogenous nutrient requirements (Haselkorn and Buikema, 1992). The pelagophytes increase with depth in connexion with the nutrient control of their vertical distribution (Claustre et al., 1994; Barlow et al., 1997; Marty et al., 2002). This vertical trend was clearly observed in the MMW; however, it was absent in the MAW (Fig. 7) where high nitrate concentrations were located in the surface and subsurface layers (Fig. 5a) confirming the role of nutrient in the pelagophytes vertical distribution. The MMW contributed significantly more to the mean chlorophyll a of cyanobacteria and pelagophytes than MAW. However, no significant difference in chlorophyll a contribution for these taxa was reported during the summer period between the two water masses (Bel Hassen et al., 2008). Indeed, MAW advection was rather weak during summer (Béranger et al., 2004), indicating that when MAW advection increased, cyanobacteria and pelagophytes better thrived in the MMW than in the MAW. This might suggest that the MAW could not be the source of these taxa and/or did not present favourable conditions for their development. In the Almerian– Oran front, Atlantic and Mediterranean waters did not show great differences in the abundance of cyanobacteria, diatoms and overall flagellates contents, but changes were evident in their Pelagophytes/Prymnesiophytes contents (Claustre et al., 1994). Moreover, in the North Ionian Sea, the MAW depicts a specific phytoplankton pattern, particularly rich in pelagophytes and chlorophytes (Casotti et al., 2000). Nevertheless, this differentiation between the typical Atlantic and Mediterranean water masses based on phytoplankton assemblages seems to be more nutrient dependent and could fluctuate in time within the same area (i.e. this study and Bel Hassen et al., 2008). Such an observation suggests that a refined criterion should be set up to identify a water mass biological marker, such as the occurrence of two populations of prochlorophytes typical of the MAW in the Gulf of Naples which was suspected to be salinity dependent (Casotti et al., 2000). Previous studies in this area of the Mediterranean mostly based on physical data modelling and statistical analyses
226
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
indicated the MAW flowing within the continental shelf area. To date there has been no comprehensive study of the physical water dynamic and their interactions with the phytoplankton community composition. Moreover, the phytoplankton distribution identified in this area showed a ‘moderate’ accumulation of the autotrophic biomass within the MAW. However, the physical setting prevailing in this area seemed not to strongly affect the phytoplankton community composition in terms of autotrophic biomass contribution. Further investigations are required to determine the phytoplankton composition peculiarity of each identified water mass. Acknowledgments This work was supported by the Tunisian funded project POEMM (LR02INSTM04). We thank Dr Salwa Sadok for her helpful comments on the original manuscript and the anonymous reviewer for his/her valuable remarks which helped to improve the manuscript. We extend our thanks to Professor Jamil JAOUA, Head of the English Unit at the Sfax Faculty of Science, who improved the English of this paper. References Barlow, R.G., Mantoura, R.F.C., Cummings, D.G., Fileman, T.W., 1997. Pigment chemotaxonomic distributions of phytoplankton during summer in the western Mediterranean. Deep-Sea Research Part II 44, 833–850. Bel Hassen, M., Drira, Z., Hamza, A., Ayadi, H., Akrout, F., Issaoui, H., 2008. Summer phytoplankton pigments and community composition related to water mass properties in the Gulf of Gabes. Estuarine, Coastal and Shelf Science 77, 645–656. Béranger, K., Mortier, L., Gasparini, G.P., Gervasio, L., Astraldi, M., Crepon, M., 2004. The dynamics of the Sicily Strait: a comprehensive study from observations and models. Deep-Sea Research 51, 411–440. Brandhost, W., 1977. Les conditions de milieu au large de la côte tunisienne. Bulletin de l'Institut National Scientifique et Technique d'Oceanographie et de Peche de Salammbo 4, 129–220. Bustillos-Guzman, J., Claustre, H., Marty, J.C., 1995. Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal northwestern Mediterranean Sea. Marine Ecology Progress Series. 124, 247–258. Campbell, L., Carpenter, E.J., 1986. Die1 patterns of cell division in marine Synechococcus spp. (Cyanobacteria): the use of the frequency of dividing cells technique to measure growth rate. Marine Ecology Progress Series 32, 139–248. Casotti, R., Brunet, C., Aronne, B., D'Alcala, M.R., 2000. Mesoscale features of phytoplankton and planktonic bacteria in a coastal area as induced by external water masses. Marine Ecology Progress Series 195, 15–27. Claustre, H., Kerherve, P., Marty, J.-C., Prieur, L., Videau, C., Hecq, J.H., 1994. Phytoplankton dynamics associated with a geostrophic front: ecological and biogeochemical implications. Journal of Marine Research 52, 711–742.
Claustre, H., Marty, J.C., 1995. Specific phytoplankton biomasses and their relation to primary production in the tropical north Pacific. Deep Sea Research. 42, 1475–1493. Estrada, M., Varela, R.A., Salat, J., Curzado, A., Arias, E., 1999. Spatio–temporal variability of the winter phytoplankton distribution across the Catalan and north Balearic fronts (NW Mediterranean). Journal of phytoplankton Research 21, 1–20. Glover, H.E., Keller, M.D., Guillard, P.R.L., 1986. Light quality and oceanic ultraphytoplankters. Nature 319, 142–143. Gomez, F., Echevarraia, F., Garcia, C.M., Prieto, L., Ruiz, J., Reul, A., JimenezGomez, F., Varela, M., 2000. Microplankton distribution in the strait of Gibraltar: a coupling between organisms and hyrodynamic structures. Journal of phytoplankton Research 22, 603–617. Haselkorn, R., Buikema, W.J., 1992. Nitrogen fixation by cyanobacteria. In: Stacey, G., Burris, R.H., Evans, H.J. (Eds.), Biological Nitrogen Fixation. Chapman & Hall, New York, pp. 166–190. Kana, T.M., Glibert, P.M., 1987. Effect of irradiance up to 2000 µE m− 2 s− 2 on marine Synechococcus WH7803-I. Growth, pigmentation and cell compostion. Deep Sea Research. 34, 179–495. Latasa, M., Estrada, M., Delgado, M., 1992. Plankton–pigment relationships in the Northwestern Mediterranean during stratification. Marine Ecology Progress Series 88, 61–73. Louda, J.W., Liu, L., Baker, E.W., 2002. Senescence- and death-related alteration of chlorophylls and carotenoids in marine phytoplankton. Organic Geochemistry 33, 1635–1653. Marty, J.C., Chiaverini, J., Pizay, M.D., Avril, B., 2002. Seasonal and inter-annual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep-Sea Research. 49, 1965–1985. Peeken, I., 1997. Photosynthetic pigment fingerprints as indicators of phytoplankton biomass and development in different water masses of the southern ocean during austral spring. Deep Sea Research. 44, 261–282. Pelegrí, J.L., Arístegui, J., Cana, L., Gonzalez-Davila, M., 2005. Coupling between the open ocean and the coastal upwelling region off northwest Africa: water recirculation and offshore pumping of organic matter. Journal of Marine Systems 54, 3–37. Poulain, P.M., Zambianchi, E., 2007. Near-surface circulation in the central Mediterranean Sea as deduced from Lagrangian drifters in the 1990's. Continental Shelf Research 27, 981–1001. Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influence of organisms in the composition of seawater. In: Hill, M.N. (Ed.), The sea, Vol II. Wiley, New York, pp. 26–77. Rodriguez, J., Blanco, J.M., Jimenez-Gomez, F., Echevarria, F., Gil, J., Rodriguez, V., Ruiz, J., Bautista, B., Guerrero, F., 1998. Patterns in the size structure of the phytoplankton community in the deep fluorescence maximum of the Alboran Sea (southwestern Mediterranean). Deep-Sea Research I. 45, 1577–1593. Van Heukelem, L., Lewitus, A.J., Kana, T.M., 1992. High-performance liquid chromatography of phytoplankton pigments using a polymeric reversedphase C18 column. Journal of Phycology 28, 867–872. Vidussi, F., Marty, J.C., Chiaverini, J., 2000. Phytoplankton pigment variations during the transition from spring bloom to oligotrophy in the northwestern Mediterranean Sea. Deep-Sea Research 47, 423–445.
Contents lists available at ScienceDirect
Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s
Phytoplankton dynamics related to water mass properties in the Gulf of Gabes: Ecological implications M. Bel Hassen a,⁎, Z. Drira a,b, A. Hamza a, H. Ayadi b, F. Akrout a, S. Messaoudi a, H. Issaoui c, Lotfi Aleya d, Abderrahmen Bouaïn b a b c d
Institut National des Sciences et Technologies de la Mer, 28 rue 2 mars 1934 2025 Salammbô. Tunisia Université de Sfax Route soukra Km 4 BP 1171 CP 3000 Sfax, Tunisia Centre de Biotechnologies de Sfax, B.P "K". 3038 Sfax, Tunisia Université de Franche-comté, Laboratoire de Chrono-Environnement, UMR CNRS 6249 1, Place Leclerc, F-25030 Besançon cedex, France
a r t i c l e
i n f o
Article history: Received 25 December 2007 Received in revised form 1 September 2008 Accepted 25 September 2008 Available online 10 October 2008 Keywords: Phytoplankton Photosynthetic pigments Atlantic Water Mediterranean Water Gulf of Gabes
a b s t r a c t The spatial distribution of chlorophylls and carotenoids was recorded throughout the Gulf of Gabes (South Ionian Sea) in March 2007, and was related to patterns of the physical structure and the nutrient concentrations. Two distinct water masses were identified based on the temperature and salinity (T–S) analysis: a cool and less salty Modified Atlantic Water (MAW) and a saltier Mediterranean Mixed Water (MMW). There was no significant difference in the mean nitrogen and phosphate concentrations between MMW and MAW, although the silica values were significantly higher in MAW. The Integrated chlorophyll a mean value was about 4 mg m− 2, with a maximum of 13 mg m− 2 at MAW stations. Higher Chlorophyll a records in typical MAW stations were mainly due to chlorophytes, which contributed up to 58% of the pigments concentrations in the MAW and about 46% in the MMW. The contribution of chlorophytes to total Chlorophyll a was found to be relatively stable throughout the water column. The contribution of diatoms, which were twofold higher in the MMW than in the MAW, did not exceed 17% of chlorophyll a and was mainly due to subsurface maxima. The chlorophytes, pelagophytes, prymnesiophytes and cryptophytes all together accounted for more than 77% of total chlorophyll a in the MAW and about 67% in the MMW. There were statistically significant differences between MMW and MAW in the pigment contribution of cyanobacteria and pelagophytes. These two taxa accounted for 13% and 24% of chlorophyll a respectively in the MAW and MMW indicating that these differences concerned phytoplankton classes at relatively low contributions to total chlorophyll a. © 2008 Published by Elsevier B.V.
1. Introduction The Gulf of Gabes, situated in the south Ionian Sea, occupies a wide continental shelf area. The existence of salinity minima in the region is attributed to the Modified Atlantic Water (MAW) was firstly described by Brandhost (1977). Using climatological datasets and high-resolution numerical simulations, Béranger et al. (2004) gave further support to these observations. These authors pointed out a ⁎ Corresponding author. Tel.: +216 71 730 420; fax: +216 71 732 622. E-mail address: [email protected] (M. Bel Hassen). 0924-7963/$ – see front matter © 2008 Published by Elsevier B.V. doi:10.1016/j.jmarsys.2008.09.004
seasonal variability along the Tunisian coast, describing that the Atlantic water was generally stronger during the winter and flowed in the upper 100 m, while they revealed a weakening of the advection during the summer. Similar observations were reported by Poulain and Zambianchi (2007) using Lagrangian drifters data. They particularly showed that, during winter, the MAW strongly flowed along the Tunisian coast through the shallow Gulf of Gabes. The physical forcing resulting from the MAW advection could confront distinct water masses and generate potential mixing of water from coastal and/or open-ocean origin. This water mixing may have an impact on the phytoplankton
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
populations, which experience large variations in their abundance, composition and size structure due to the dynamic nature of their environment (Pelegrí et al., 2005). Interactions between the physical processes and the biological features have been investigated in frontal regions showing that the physical forcing affects the abundance and composition of phytoplankton directly (Estrada et al., 1999; Gomez et al., 2000). Estrada et al. (1999) found high Chlorophyll a concentration and diatoms dominance inshore the Catalan Front. However, offshore of the front the diatoms were scarce and the phytoplankton assemblages were dominated by coccolithophorids. A taxonomic structure with a predominance of diatoms on the Mediterranean side and of dino-
217
flagellates and microzooplankton on the Atlantic side were also observed in the straits of Gibraltar (Gomez et al., 2000). Frontal structures are known to enhance phytoplankton production due to fertilization processes and to favour the growth of diatoms (Claustre et al., 1994) as well as dominance of the small-sized plankton (Casotti et al., 2000). Following this evidence of water mass control of phytoplankton communities at the Mediterranean, the present paper investigates the phytoplankton community in the Gulf of Gabes. Southern Mediterranean is particularly deficient in this type of analysis and this paper describes a high spatial resolution using the pigment biomarkers to characterize the community composition in relation to the water masses in the
Fig. 1. Sampling sites and the 50 m, 100 m and 200 m isobaths in the Gulf of Gabes.
218
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Table 1 Pigments markers, conversion factors and contribution of different phytoplankton groups to chlorophyll a Diatoms
Dinoflagellates
Prymnesiophytes
Cryptophytes
Chlorophytes
Pelagophytes
Cyanophytes
Pigment marker
Fucoxanthin
Peridinin
Hex
Alloxanthin
Chlorophyll b
But
Zeaxanthin
Conversion factor MMW (n = 54) MAW (n = 35)
(1.25)a 16.3 8.2
(1.00)a 5.1 6.6
(0.80)a 4.9 10.7
(1.60)a 2.5 3.5
(1.50)a 46.7 57.7
(1.20)b 13.0 6.0
(2.00)c 11.2 6.9
Conversion factors were used to determine the different amounts of the algal classes to chlorophyll a. Hex = 19′-hexanoyloxyfucoxanthin and But = 19′-butanoyloxyfucoxanthin. Values are derived from: a Casotti et al. (2000); b Peeken (1997); c Kana and Glibert (1987).
region. Our results indicate that water mass have a manifest influence on both the nutrient and phytoplankton communities field at the southern Mediterranean. 2. Methods 2.1. Stations locations Fig.1 shows the locality of the sampling sites. Three sectors were investigated: the offshore northeast sector including station 1 to station 11, the coastal southern sector from station 16 to station 23 and a transect joining the two previous areas comprising station 12 to station 15. Sampling was performed during a cruise on board the R/V Hannibal from 16 to 19 March 2007 in the Gulf of Gabes. Samples locations were selected in order to sample different types of water masses and in order to characterize variability across the Modified Atlantic Water (MAW), which was documented to be distributed within this area, east from 12°E longitude (Béranger et al., 2004; Poulain and Zambianchi, 2007). 2.2. Samples collection and CTD profiles Water samples were collected using 12 L Niskin bottles on a Seabird rosette sampler deployed with CTD (Seabird 9 underwater unit). Sampling occurred at three depths (2 m, 25 m and near the bottom) at the stations less than 50 m deep (i.e., coastal stations) or five depths at the stations deeper than 50 m (2 m, 10 m, 20 m, 50 m and near the bottom). This increase of the sampling resolution within the first 50 m of the offshore stations was aimed at better characterizing the MAW vertical variability, which was documented to flow in the surface layer during this period of the year (Béranger et al., 2004). Sub-samples (2 L) for the pigments analysis were filtered through 47 mm-diameter glass fibre filter Whatman, GF/F. Filters were then immediately stored at −20 °C for a subsequent pigment analysis. Samples for the nutrients determination were stored at −20 °C until analysis with an automatic analyser type 3 (BRAN + LUEBBE).
2.3. Pigments analysis In order to analyse phytoplankton chlorophylls and carotenoids, filters were cut into small pieces and sonicated in 100% acetone to extract the pigment. The homogenates were then centrifuged to remove cellular and glass filters debris and the supernatant was filtered through a nylon 0.45 µm filter. These extracts were then analysed for pigment content using the reverse phase High Performance Liquid Chromatography (HPLC) technique derived from (Van Heukelem et al., 1992). The analyses were performed on a HP 1100 system equipped with an Eurospher — 10 0 C18 (250 × 4.6 mm × 5 µm) column and with a multi-wave length UV detector. The pigments were separated using a non-linear binary gradient using a solvent A composed of 80% methanol:20% ammonium acetate (0.5 M adjusted at pH 7.2) and a solvent B composed of 100% acetonitrile. Chlorophylls and carotenoids were detected and quantified by absorbance at 440 nm. Amounts of pigments were estimated from the areas under the peak of the individual components. Calibrations were made using standard samples acquired from DHI Water and Environment Institute (Hørsholm, Denmark). The pigments names were abbreviated as follows: Chlorophyll a (Chl a), Chlorophyll b (Chl b), Chlorophyllids (a) Fucoxanthine (Fuco), 19'-hexanoyloxyfucoxanthin (Hex), 19'-butanoyloxyfucoxanthin (But), Peridinin (Peri), Alloxanthin (Allo) and Zeaxanthin (Zea). 2.4. Calculations deduced from pigment concentrations In order to evaluate the contribution of different phytoplankton groups to the chlorophyll a biomass, we used the ratio of chlorophyll a: diagnostic pigment extracted from different literature sources and already used in the north Ionian Sea by Casotti et al. (2000) (Table 1). The criteria for the adoption of these pigment ratios were based on the proximity of the investigated site and the similarity in the physical forcing, mainly influenced by the Atlantic water advection.
Fig. 2. Vertical profiles of (a) density (kg m− 3), (b) salinity (P.S.U) and (c) temperature (°C) according to a gradient of distance to the coast. Distance on x axis is scaled in km from the starting point of the section: 10.05 E, 33.90 N, the ending point is located at the most distant station: 13.05E, 35.05 N. The section width includes all the sampled stations.
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
219
220
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
stations to the east of 13°E longitude (i.e. stations 4, 5 and 6) and was characterized by salinities fluctuating between less than 37.5 PSU, in their upper surface water and to 38.5 PSU, in deep water. The density profiles clearly presented the variability between the three identified groups (Fig. 4). Groups A and C deeper than 20 m were composed of dense water with density values higher than 27.6 (Fig. 4a and c). This presumably reflected varying degrees of mixing of Mediterranean Waters with other shore water masses and we designated them as Mediterranean Mixed Waters (MMW). Group B stations and group C surface water were composed of less dense water (Fig. 4b and c). They corresponded to the salinity minima considered as characteristics of the Modified Atlantic Water (MAW). As for station 7, the less dense surface water was attributed to the MAW whereas the deep water was attributed to the MMW. 3.2. Nutrient and pigment distributions
Fig. 3. T–S data from the CTD profiles. Group (A) data represent coastal stations situated west from 12°E longitude (i.e. from station 12 to station 23) and are labelled with (+) symbol. Group (B) data represent stations situated between 12°E and 13°E longitude (i.e. stations 1, 2, 3, 7, 8, 9,10 and 11) and are labelled with (⁎) symbol. Group (C) data represent stations situated east from 13°E longitude (i.e. stations 4, 5 and 6) and are labelled with (ο) symbol.
2.5. Statistical analyses A single factor analysis of variance (ANOVA) was conducted to statistically assess variations in the mean fraction of chlorophyll a of each phytoplankton taxon and the mean nutrient concentrations within the identified water masses. The statistical analyses were performed with XLSTAT software for Windows. 3. Results 3.1. Physical water characterization A coast offshore (west–east) section allowed to show temperature, salinity and density fields Fig. (2). Density variations mainly correlated with salinity (Fig. 2b) (R2 = 0.926, P b 0.001), whereas no correlation was found with temperature (Fig. 2c). It may be noted that the 27.6 isopycnal, delimiting the zone of salinity minima, corresponded to the isohaline of 37.5 which was used to define the interface between the Atlantic and Mediterranean water in the Alboran Sea (Rodriguez et al., 1998). The T–S plot (Fig. 3) identified three major water groups. The first group, designated as A, included coastal stations situated to the west of 12°E longitude and was characterized by high temperature (N16.3 °C) and salinity (N37.5 PSU). The second group, designated as B, represented the stations situated between 12°E and 13°E longitude (i.e. stations: 1, 2, 3, 7, 8, 9 ,10 and 11) with low records in salinity (b37.5 PSU) and temperature. It is worth noting that for station 7, surface water characteristics were similar to those of group B, whereas the deep water had salinity values close to those of group A. The third group, designated as C, incorporates
Nitrate concentration showed some local maxima in the zones of minimum salinity; and in some bottom stations, it showed a signal of surface depletion in the coastal area (Fig. 5a). Phosphate concentration (Fig. 5b) generally low (b0.2 µM) was higher in the coastal bottom stations. The nitrate-to-phosphate ratio (N:P) was lower than 20 (Fig. 5c), the lowest values were recorded within the coastal zone and in the salinity minima area. Silica (Fig. 5d) exhibited high values in the offshore area, mainly within the zone limited by the 27.6 isopycnal, whereas minima were recorded in the west coastal side of this limit. Nitrate and the phosphate did not show statistically a significant difference in their mean value between both identified water masses, whereas the silica mean concentration in the MAW was statistically higher (P b 0.05) than that in the MMW level. Chlorophyll a concentrations were lower than 0.5 µg l− 1 and did not exhibit a clear spatial pattern (Fig. 5e) except for the presence of subsurface maxima. The Integration of pigments over the first 50 m in depth (Fig. 6) showed a mean chlorophyll a value around 4 mg m− 2. The highest values were recorded in the typical MAW stations with a maximum of 13 mg m− 2 in station 2. Moreover, the increasing chlorophyll a content in the typical MAW stations was mainly due to chlorophytes, whose characteristic pigment, chlorophyll b, showed a spatial pattern similar to chlorophyll a. This observation applies to some extent for the MMW coastal stations. However, the MMW stations adjacent to the MAW, namely from station 11 to station 14, exhibited the highest Chlorophyll a and the lowest chlorophyll b integrated values. The variations in fucoxanthin according to the water bodies showed some local increases in the coastal MMW, whereas their levels were rather low in the MAW. Besides, 19'-hexanoyloxyfucoxanthin (prymnesiophytes), Zeaxanthin (cyanobacteria) and Peridinin (dinoflagellates) were compounds of relative minor importance. The results of alloxanthin were not presented here since the integrated concentrations of this pigment never exceeded 0.3 mg m− 2. Chlorophyllid a concentrations fluctuated in the same order of magnitude as chlorophyll a. The highest integrated concentrations of this degraded pigment were observed in MMW stations closest to the MAW. In the MAW, the depth-
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 4. Density profiles at the investigated stations arranged along a coast-offshore direction. (a) Coastal stations situated west from 12°E longitude (i.e. from station 12 to station 23), (b) stations situated between 12°E and 13°E longitude (i.e. stations 1, 2, 3, 7, 8, 9,10 and 11) and (c) stations situated east from 13°E longitude (i.e. stations 4, 5 and 6). The density value of 27.6 is indicated by an arrow.
221
222 M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226 Fig. 5. Vertical profiles of (a) nitrate (µM), (b) phosphate (µM), (c) N:P ratio (d) Silicate (µM) and (e) Chlorophyll a (µg/l). The section details as Fig. 2. The sign (+) indicates the sampled depths. The 27.6 isopycnal is reported in the figures.
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
223
Fig. 5 (continued).
integrated chlorophyllid a did not show significant variations among the stations with concentrations values of about 5 mg m− 2. Table 1 shows the respective contribution of each taxonomic group (as estimated from the pigment ratio) to chlorophyll a. The chlorophytes contributed up to 46% of chlorophyll a at the MMW and about 58% at the MAW. Although the contribution of diatoms was twice higher at the MMW than at the MAW, it did not exceed 17% of chlorophyll a. The contribution of pelagophytes and cyanobacteria were also significantly higher at the MMW (contribution greater than 10%) than at the MAW. A single factor analysis of variance (ANOVA) was conducted to statistically assess differences in the phytoplankton community composition among MMW and MAW. It examined the mean fraction of chlorophyll a of each phytoplankton taxon with station groups MMW and MAW as the categorical variables. The results indicated significant differences between MMW and MAW in the mean fraction of chlorophyll a of cyanobacteria (p b 0.02) and pelagophytes (p b 0.05), whereas no significant differences were found for the other phytoplankton taxon. The respective vertical mean contributions of the main phytoplankton groups were estimated using chlorophyll a: diagnostic ratio approach (Fig. 7). The pigment ratios were assumed to be stable with depth which implicitly neglects the effect of the photo-adaptation or the nutrient status of the algae. Chlorophytes dominated over the different investigated groups in all depths. Their contributions were almost similar for depth less than 50 m; however, they decreased for MMW and increased for MAW in the 100 m deep water. Cyanophytes dominated over diatoms, pelagophytes and prymnesiophytes in the upper 20 m for both MMW and MAW, whereas their contribution dropped drastically in the deep water. The diatoms contribution did not exceed 20% at all depths. They represented the second source of chlorophyll a in the MMW deep water.
4. Discussion The chlorophyll a average integrated values found in both MMW and MAW waters were rather low compared to the typical values recorded in the Mediterranean and Atlantic waters (20 mg m− 2) of the Algerian current during the spring period (Claustre et al., 1994). They were also below the averaged value of 10 mg m− 2 recorded in the mid south western Mediterranean (Barlow et al., 1997), or the 12 mg m− 2 value found in the Sicily Straits during the summer oligotrophic conditions (Barlow et al., 1997). Even though the concentration of chlorophyll a did not exhibit significant differences between the two water masses identified, the depth-integrated chlorophyll a values showed an increase in the MAW stations. These results suggest that the MAW might present favourable conditions, in terms of nutrient content, for locally enhanced production. The lack of difference in the mean nitrogen and phosphate concentrations between the water masses suggests that nutrient brought by MAW advection were not sufficiently high to justify a difference in the trophic conditions. A difference was found for silica with significantly higher concentrations in the MAW than in the MMW. This was associated with N:P ratio (Fig. 5c) well below the accepted standard molar ratio of N: P = 16:1 set up for marine diatoms requirements (Redfield et al., 1963), suggesting a potential N-limitation of diatoms growth and might explain an incomplete utilization of silica by diatoms in the MAW. This statement can find support in the low proportion of chlorophyll a contributed by diatoms in the MAW which represented nearly half the diatoms contribution in the MMW (Table 1). The major feature of the Mediterranean basin in various regions and seasons is a phytoplankton biomass with a high contribution of prymnesiophytes (Latasa et al., 1992; Claustre et al., 1994; Bustillos-Guzman et al., 1995; Barlow et al., 1997; Vidussi et al., 2000). However, our results showed that
224
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 6. Integrated concentrations of selected diagnostic pigments arranged along a coast offshore direction. The stations numbers are indicated and the typical MMW and MAW stations are reported. The distribution of alloxanthin is not reported since the pigment concentration is below 0.3 mg m− 2.
phytoplankton composition was chlorophytes-dominated particularly within the MAW, which were consistent with the observations reported by Casotti et al. (2000) in the Gulf
of Naples (Tyrrhenian Sea) and those reported in the Gulf of Gabes during the summer period (Bel Hassen et al., 2008). In addition, the MAW was characterized by a phytoplankton
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
Fig. 7. Vertical distributions of the respective mean contribution of diatoms, chlorophytes, cyanophytes, pelagothytes and prymnesiophytes to chlorophyll a biomass at each depth and calculated from pigment ratio (Table 1) and pigment concentrations.
community with a large proportion of nano-sized cells such as chlorophytes, pelagophytes, prymnesiophytes and cryptophytes which accounted for more than 77% of total chlorophyll a (Table 1). This percentage was more similar to those reported by Casotti et al. (2000) in a small coastal eddy (76.8%) and by Claustre et al. (1994 ) in the typical MAW stations of the Eastern Alboran Sea geostrophic front (65%), than that found in the Gulf of Gabes (49%) during the summer stratified conditions (Bel Hassen et al., 2008). The increasing contribution of a small-celled community generally succeeds that found during phytoplankton bloom conditions and was characteristic of oligotrophic phytoplankton community (Bustillos-Guzman et al., 1995; Vidussi et al., 2000). This indicates that the MAW phytoplankton community structure could be situated in post blooming conditions. Such a hypothesis is supported by the high level of chlorophyllid a pigment whose accumulation is indicative of senescencedeath phytoplankton (Louda et al., 2002). The vertical distribution of chlorophytes, the most abundant phytoplankton group in both MAW and MMW, did not greatly vary with depth. The coefficients of variation of chlorophyll a mean proportion contributed by chlorophytes at various depths were about 17% and 26% in MAW and MMW respectively. Moreover, the maximum chlorophyll a concentrations were mostly located near but not in the surface layer
225
(Fig. 4e). At this particular depth (10 m) chlorophytes contributions to chlorophyll a were about 45% in the MMW and 52% in the MAW. These numbers are similar to the mean depth-integrated contribution of chlorophytes (Table 1). The stable contribution of chlorophytes at different depths could be justified by the ability of this group to develop photoadaptation processes related to depth variations (Glover et al., 1986). In fact, a homogeneous distribution of flagellates over depth (mainly dominated by chlorophytes) was also described during the summer period characterized by a weak advection and a MAW confined to the bottom stratified layer (Bel Hassen et al., 2008). The stability of the chlorophytes vertical distribution within completely different hydrologic conditions suggests that chlorophytes are a cosmopolitan class of phytoplankton in this area, since they always represented a significant component of the biomass throughout surface waters and in depth profiles. The increased cyanobacteria concentrations in surface layers has been previously reported (Campbell and Carpenter, 1986; Claustre and Marty, 1995; Bustillos-Guzman et al., 1995) and might be due to their ability to be photosynthetically competent in high light intensities (Kana and Glibert, 1987) or to their ability to fix atmospheric nitrogen to meet their nitrogenous nutrient requirements (Haselkorn and Buikema, 1992). The pelagophytes increase with depth in connexion with the nutrient control of their vertical distribution (Claustre et al., 1994; Barlow et al., 1997; Marty et al., 2002). This vertical trend was clearly observed in the MMW; however, it was absent in the MAW (Fig. 7) where high nitrate concentrations were located in the surface and subsurface layers (Fig. 5a) confirming the role of nutrient in the pelagophytes vertical distribution. The MMW contributed significantly more to the mean chlorophyll a of cyanobacteria and pelagophytes than MAW. However, no significant difference in chlorophyll a contribution for these taxa was reported during the summer period between the two water masses (Bel Hassen et al., 2008). Indeed, MAW advection was rather weak during summer (Béranger et al., 2004), indicating that when MAW advection increased, cyanobacteria and pelagophytes better thrived in the MMW than in the MAW. This might suggest that the MAW could not be the source of these taxa and/or did not present favourable conditions for their development. In the Almerian– Oran front, Atlantic and Mediterranean waters did not show great differences in the abundance of cyanobacteria, diatoms and overall flagellates contents, but changes were evident in their Pelagophytes/Prymnesiophytes contents (Claustre et al., 1994). Moreover, in the North Ionian Sea, the MAW depicts a specific phytoplankton pattern, particularly rich in pelagophytes and chlorophytes (Casotti et al., 2000). Nevertheless, this differentiation between the typical Atlantic and Mediterranean water masses based on phytoplankton assemblages seems to be more nutrient dependent and could fluctuate in time within the same area (i.e. this study and Bel Hassen et al., 2008). Such an observation suggests that a refined criterion should be set up to identify a water mass biological marker, such as the occurrence of two populations of prochlorophytes typical of the MAW in the Gulf of Naples which was suspected to be salinity dependent (Casotti et al., 2000). Previous studies in this area of the Mediterranean mostly based on physical data modelling and statistical analyses
226
M. Bel Hassen et al. / Journal of Marine Systems 75 (2009) 216–226
indicated the MAW flowing within the continental shelf area. To date there has been no comprehensive study of the physical water dynamic and their interactions with the phytoplankton community composition. Moreover, the phytoplankton distribution identified in this area showed a ‘moderate’ accumulation of the autotrophic biomass within the MAW. However, the physical setting prevailing in this area seemed not to strongly affect the phytoplankton community composition in terms of autotrophic biomass contribution. Further investigations are required to determine the phytoplankton composition peculiarity of each identified water mass. Acknowledgments This work was supported by the Tunisian funded project POEMM (LR02INSTM04). We thank Dr Salwa Sadok for her helpful comments on the original manuscript and the anonymous reviewer for his/her valuable remarks which helped to improve the manuscript. We extend our thanks to Professor Jamil JAOUA, Head of the English Unit at the Sfax Faculty of Science, who improved the English of this paper. References Barlow, R.G., Mantoura, R.F.C., Cummings, D.G., Fileman, T.W., 1997. Pigment chemotaxonomic distributions of phytoplankton during summer in the western Mediterranean. Deep-Sea Research Part II 44, 833–850. Bel Hassen, M., Drira, Z., Hamza, A., Ayadi, H., Akrout, F., Issaoui, H., 2008. Summer phytoplankton pigments and community composition related to water mass properties in the Gulf of Gabes. Estuarine, Coastal and Shelf Science 77, 645–656. Béranger, K., Mortier, L., Gasparini, G.P., Gervasio, L., Astraldi, M., Crepon, M., 2004. The dynamics of the Sicily Strait: a comprehensive study from observations and models. Deep-Sea Research 51, 411–440. Brandhost, W., 1977. Les conditions de milieu au large de la côte tunisienne. Bulletin de l'Institut National Scientifique et Technique d'Oceanographie et de Peche de Salammbo 4, 129–220. Bustillos-Guzman, J., Claustre, H., Marty, J.C., 1995. Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal northwestern Mediterranean Sea. Marine Ecology Progress Series. 124, 247–258. Campbell, L., Carpenter, E.J., 1986. Die1 patterns of cell division in marine Synechococcus spp. (Cyanobacteria): the use of the frequency of dividing cells technique to measure growth rate. Marine Ecology Progress Series 32, 139–248. Casotti, R., Brunet, C., Aronne, B., D'Alcala, M.R., 2000. Mesoscale features of phytoplankton and planktonic bacteria in a coastal area as induced by external water masses. Marine Ecology Progress Series 195, 15–27. Claustre, H., Kerherve, P., Marty, J.-C., Prieur, L., Videau, C., Hecq, J.H., 1994. Phytoplankton dynamics associated with a geostrophic front: ecological and biogeochemical implications. Journal of Marine Research 52, 711–742.
Claustre, H., Marty, J.C., 1995. Specific phytoplankton biomasses and their relation to primary production in the tropical north Pacific. Deep Sea Research. 42, 1475–1493. Estrada, M., Varela, R.A., Salat, J., Curzado, A., Arias, E., 1999. Spatio–temporal variability of the winter phytoplankton distribution across the Catalan and north Balearic fronts (NW Mediterranean). Journal of phytoplankton Research 21, 1–20. Glover, H.E., Keller, M.D., Guillard, P.R.L., 1986. Light quality and oceanic ultraphytoplankters. Nature 319, 142–143. Gomez, F., Echevarraia, F., Garcia, C.M., Prieto, L., Ruiz, J., Reul, A., JimenezGomez, F., Varela, M., 2000. Microplankton distribution in the strait of Gibraltar: a coupling between organisms and hyrodynamic structures. Journal of phytoplankton Research 22, 603–617. Haselkorn, R., Buikema, W.J., 1992. Nitrogen fixation by cyanobacteria. In: Stacey, G., Burris, R.H., Evans, H.J. (Eds.), Biological Nitrogen Fixation. Chapman & Hall, New York, pp. 166–190. Kana, T.M., Glibert, P.M., 1987. Effect of irradiance up to 2000 µE m− 2 s− 2 on marine Synechococcus WH7803-I. Growth, pigmentation and cell compostion. Deep Sea Research. 34, 179–495. Latasa, M., Estrada, M., Delgado, M., 1992. Plankton–pigment relationships in the Northwestern Mediterranean during stratification. Marine Ecology Progress Series 88, 61–73. Louda, J.W., Liu, L., Baker, E.W., 2002. Senescence- and death-related alteration of chlorophylls and carotenoids in marine phytoplankton. Organic Geochemistry 33, 1635–1653. Marty, J.C., Chiaverini, J., Pizay, M.D., Avril, B., 2002. Seasonal and inter-annual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep-Sea Research. 49, 1965–1985. Peeken, I., 1997. Photosynthetic pigment fingerprints as indicators of phytoplankton biomass and development in different water masses of the southern ocean during austral spring. Deep Sea Research. 44, 261–282. Pelegrí, J.L., Arístegui, J., Cana, L., Gonzalez-Davila, M., 2005. Coupling between the open ocean and the coastal upwelling region off northwest Africa: water recirculation and offshore pumping of organic matter. Journal of Marine Systems 54, 3–37. Poulain, P.M., Zambianchi, E., 2007. Near-surface circulation in the central Mediterranean Sea as deduced from Lagrangian drifters in the 1990's. Continental Shelf Research 27, 981–1001. Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influence of organisms in the composition of seawater. In: Hill, M.N. (Ed.), The sea, Vol II. Wiley, New York, pp. 26–77. Rodriguez, J., Blanco, J.M., Jimenez-Gomez, F., Echevarria, F., Gil, J., Rodriguez, V., Ruiz, J., Bautista, B., Guerrero, F., 1998. Patterns in the size structure of the phytoplankton community in the deep fluorescence maximum of the Alboran Sea (southwestern Mediterranean). Deep-Sea Research I. 45, 1577–1593. Van Heukelem, L., Lewitus, A.J., Kana, T.M., 1992. High-performance liquid chromatography of phytoplankton pigments using a polymeric reversedphase C18 column. Journal of Phycology 28, 867–872. Vidussi, F., Marty, J.C., Chiaverini, J., 2000. Phytoplankton pigment variations during the transition from spring bloom to oligotrophy in the northwestern Mediterranean Sea. Deep-Sea Research 47, 423–445.