Summer distribution and community structure of surface water mesozooplankton from the eastern Mediterranean Sea

The study was carried out at 70 stations between 11 August and 4 September 2006 and between 10 July and 13 August 2008 in the Mediterranean Sea around the Turkish peninsula with the help of R/V YUNUS-S (Figure 1, Table 1). The northern Aegean Sea (NA) group was represented by 11 stations, the southern Aegean Sea (SA) by 19 stations, the coastal waters of the Levantine Sea (LSC) by 31 stations and the open waters of the Levantine Sea (LSO) by 9 stations. Temperature and salinity were also measured at each station with a SEABIRD CTD probe. Chlorophyll-a concentrations were measured synchronously with zooplankton sampling by Altuğ et al. (2007) and Aktan (2011). All samples were vertically collected by using a WP2 net (mesh size: 200 μm) from a depth of 50 m to the surface of the water column or from near the bottom to the surface if the station depth was less than 50 m. The filtered volume was measured with a Hydro-Bios flowmeter. After the tow, the net was carefully washed, and the sample was split into two with a Folsom splitter. The first half was used fresh for biomass measurements as the wet weight; the other half of each sample was fixed and preserved in a seawater-buffered formaldehyde solution (4% final concentration) for later determination of composition and abundance. Specimens were identified under a dissecting microscope. Quantitative analyses of commonly found species were performed on subsamples taken with a 1 ml Stempel pipette (at least three times). Rare species were identified from the whole sample. Cladocerans and copepods were identified at the species or genus level. All other taxa were identified to the lowest possible taxa. The pIONeer 65 multi-probe was used to assess water temperature, salinity and dissolved oxygen using the practical salinity scale. Seawater was filtered via Whatman GF/C glass fiber filters for chlorophyll analysis and then frozen until spectrophotometric examination took place after acetone extraction.

Figure 1

Species diversity and dominance were estimated using the Shannon–Weaver formula (Zar 1984). The differences in physical and biological data (total zooplankton abundance and biomass) between areas were evaluated with ANOVA (SPSS v. 22). Differences in the zooplankton community were evaluated for spatial variation with similarities and multidimensional scaling (MDS) analysis by calculating log (x + 1)-transformed abundance data on the basis of the Bray–Curtis similarity index. The differences between the samples were assessed by a one-way analysis of similarities (ANOSIM) permutation test. Using the similarities percentage procedure according to SIMPER was performed to determine the dominant species that contributed to the spatial differences in community structure. The MDS, ANOSIM and SIMPER procedures were performed using the software package PRIMER 6 (Clarke and Warwick, 1994).

The data were collected over two summers from the Aegean and Levantine Seas. The overall means of the environmental parameters are presented in Table 2. The among-region differences were clear for temperature (F_3;69 = 137.29, p < 0.05) and salinity (F_3;69 = 35.22, p < 0.05). The highest temperatures were recorded in the coastal waters of the Levantine Sea, with an average of 27.21 ± 1.63°C. Surface salinity showed a north–south gradient, with mean values ranging from 37.38 ± 1.28 to 39.15 ± 0.08 PSU. The highest salinity value (39.6 ppm) was recorded in the Antalya Bay (in Station LSC37) in the coastal waters of the Levantine Sea. While lower chlorophyll-a levels were recorded in the northern Aegean Sea (0.23 ± 0.17 μg l⁻¹), chlorophyll-a levels were higher in the coastal waters of the southern Aegean Sea (0.89 ± 0.76 μg l⁻¹).

Taking all sampling stations into account, the zooplankton abundance values ranged between 123 and 23,931 ind m⁻³, while biomass values ranged between 80 and 3200 mg m⁻³ (Figure 2). The highest mean abundance (4562 ind m⁻³) and biomass (748 mg m⁻³) values were detected in the southern Aegean Sea (SA), especially in Station SA90, particularly due to Penilia avirostris and Centropages kroyeri, whereas the lowest mean abundance (307 ind m⁻³) and biomass (231 mg m⁻³) values were observed in the LSO (Table 4). A total of 157 taxa were registered in the study area, of which 112 were in Copepoda and 7 were in Cladocera. Copepods, cladocerans, doliolids, meroplankton and appendicularians represented the most important zooplankton groups in all stations. Among meroplankton, the most important groups were larvae of Decapoda, Polychaeta, Mollusca and Cirripedia, together comprising 2.7% of the total abundance. Salps and siphonophores were also abundant in some areas, especially in the Aegean Sea; however, their relative abundance never exceeded 5%.

Figure 2

Generally, Copepoda was the most abundant group in the LSO area (Table 4), but the maximum abundance (11,757 ind m⁻³; Station SA90) was recorded in the southern Aegean Sea (Figure 3). Paracalanus parvus, Acartia clausi, Centropages kroyeri and Temora stylifera were very important in the Aegean Sea; Clausocalanus furcatus, Oithona plumifera, Calocalanus pavoninus, Farranula rostrata and Calanopia elliptica were dominant in the stations of the Levantine Sea (Table 4). Candacia giesbrechti (Station NA15) and Acartia (Hypoacartia) adriatica (Stations NA17, SA2 and SA3) were found only in the Aegean Sea, while Sapphirina bicuspidata was recorded only on the eastern coasts of the Levantine Sea (Stations LSC11, LSC13, LSC61, LSC65 and LSC81). Calonopia elliptica and Parvocalanus elegans were only present in the coastal waters of the Levantine Sea, where Calonopia elliptica reached extremely high abundance (506 ind m⁻³) at Station LSC59. A total of 19 copepod species were recorded for the first time in the Aegean (15 species) and Levantine (8 species) coasts of Turkey. Five copepod species (Corycaeus (Onychocorycaeus) ovalis, Goniopsyllus clausi, Oncaea scottodicarloi, Sapphirina bicuspidate and Scaphocalanus curtus) were recorded for the first time in the Turkish coastal region, three (Centropages bradyi, Goniopsyllus clausi and Oncaea scottodicarloi) for the Aegean Sea and one (Goniopsyllus clausi) among the eastern Mediterranean fauna (Table 3).

Figure 3

Cladocera, with maximum abundance of 11,757 ind.m⁻³ at Station SA90, had a higher percentage of mesozooplankton at the NA and SA stations (Table 4), but a much lower mean relative abundance was observed at the LSC and LSO stations (Figure 3). A total of 7 Cladocera species (Penilia avirostris, Pseudevadne tergestina, Evadne spinifera, Evadne nordmanni, Pleopis polyphemoides, Podon intermedius and Pleopis schmackeri) were identified in the present study. Among Cladocera Penilia avirostris was the dominant species, especially in coastal bays and areas in the sub regions of the study area, with a maximum abundance of 8778 ind m⁻³ (at Station NA23) and of 8203 ind m⁻³ (at Station SA90). Other Cladocera (in order of importance) followed: Pseudevadne tergestina and Evadne spinifera. Pleopis schmackeri was observed at both the SA and LSC stations, with a maximum abundance of 5.3 ind m⁻³ (at Station SA101).

Although Doliolida species were also occasionally observed (a 50% occurrence), they did not significantly contribute to the total zooplankton abundance (Table 4, Figure 3). The abundance of meroplanktonic groups, including larvae of Bivalvia, Gastropoda, Polychaeta and Echinodermata, were higher in the gulfs and the coastal stations, whereas Appendicularia were an important group in SA, with a maximum abundance of 888 ind m⁻³ at Station SA90 (Figure 3).

With regard to regions, 96 species were found in the NA, 98 in the SA, 124 in the LSC and 91 in the LSO. The increasing number of species from NA to LSC was more evident, except in LSO. The variability in the number of species within areas was greater in the SA and LSC regions. The most species (65 species) was recorded at Stations SA3 and LSC79 (Figure 2). The diversity index values varied between 3.7 bits (Station SA3) and 2.1 bits (Station LSC59) (Figure 2). The dominant species from the coastal waters differed from those in open waters.

Cluster analysis (Figure 4) and MDS ordination (Figure 5) of the combined data from the subregions showed that the samples were clearly differentiated by region. The among-region differences were stronger when zooplankton abundance (F_3;69 = 19.885; p < 0.05) and biomass (F_3;69 = 7.629; p < 0.05) were considered. The Tukey test indicated a difference in total biomass between the southern Aegean Sea and all other areas, while the zooplankton community structure in the subregions (NA and SA) of the Aegean Sea had significantly higher values than those of the Levantine Sea (LSC and LSO). While the highest zooplankton abundance value was recorded in the SA region, with an average of 4562 ± 5523 ind m⁻³, lower values were recorded in LSO (307 ± 132 ind m⁻³) and LSC (628 ± 300). ANOSIM analysis (global R value = 0.517, p = 0.1%) showed significant correlations between the study sites regarding the zooplankton communities. It was determined that the structure of the zooplankton community in the LSO region differed from that of the NA region (ANOSIM R = 0.946). The within-group similarity (using SIMPER; Table 5) depending on the dominant species revealed a higher average similarity (more than 60%) within the LSO group, with Clausocalanus furcatus significantly contributing along with Farranula rostrata and Calocalanus pavoninus, due to their higher abundance. The lowest average similarity (49.84) was observed in the SA region. Paracalanus parvus, Temora stylifera and Penilia avirostris were relatively consistent species within SA.

Figure 4

Figure 5

SIMPER analysis showed that Appendicularia, Doliolidae, some Copepoda (such as Paracalanus parvus, Acartia clausi, Centropages kroyeri and Centropages typicus) and Cladocera (such as Penilia avirostris, Pseudevadne tergestina and Evadne spinifera) mostly contributed to dissimilarity among groups (Table 6). The species contributing to the dissimilarities between pairs of station groups revealed that the LSO was significantly dissimilar to both the NA and SA (total average dissimilarity: 72.61% and 67.05%, respectively), due to the rarity and relative scarcity of some zooplankton species compared to those of other groups, including Penilia avirostris, Pseudevadne tergestina, Paracalanus parvus, Clausocalanus furcatus, Acartia clausi, Centropages typicus, Calocalanus pavoninus and Doliolidae. The average of the Bray–Curtis dissimilarities between all pairs of NA and SA groups was relatively lower (54.84%). The species that contributed the most to dissimilarity was A. clausi because of its high frequency (7.82%) and relatively higher abundance in the NA region, especially at stations NA23 (950 ind m⁻³) and NA18 (707 ind m⁻³). Additionally, the low-frequency species Oithona setigera (<1% occurrence in all regions) exhibited the highest abundance only in Station NA17 (154 ind m⁻³) of the northern Aegean Sea and Paracartia latisetosa was found only at two stations in the coastal waters of Levantine Sea (52 ind m⁻³ at Station LSC67 and 13 ind m⁻³ at Station LSC68), but there was no significant contribution to the dissimilarity (<1%) between regions.