Temporal variation of the soft-bottom molluscan fauna in north-western İskenderun Bay (Levantine Sea)

İskenderun Bay, with big international harbors and jetties for crude oil and coal transportation, is located in the eastern part of the Turkish Levantine coast. This location facilitates the transfer of alien species into the region by ship traffic. In addition, due to its proximity to the Suez Canal, İskenderun Bay is one of the important areas preferred by the Lessepsian species for their colonization. The impact of alien species on their new environment includes restructuring of established food webs, importing new diseases and competition with native organisms for food and space (Çınar et al. 2005).

Previous studies performed in the region have focused mainly on alien molluscan species (Çevik & Öztürk 2001; Çeviker 2001; Delongueville & Scaillet 2006a,b; Albayrak & Çağlar 2006; Albayrak 2010). Bitlis Bakır et al. (2012) listed 424 molluscan species from Iskenderun Bay, including 77 alien species (18%). Some new alien mollusks [Pseudorhaphitoma iodolabiata (Hornung & Mermod, 1928), Plocamopherus tilesii Bergh, 1877, Nudiscintilla cf. glabra Lützen & Nielsen, 2005, Eunaticina papilla Gmelin, 1791, Martesia striata (Linnaeus, 1758), Lodderia novemcarinata (Melvill, 1906), Eratoena sulcifera (Gray in Sowerby G.B.I, 1832), Zafra obesula (Hervier, 1899) and Zafra pumila (Dunker, 1858)] have also been added to the inventory of the molluscan fauna in the area (Öztürk 2012; Yokeş et al. 2012; Mifsud & Ovalis 2012; Öztürk & Bitlis-Bakır 2013; Çevik et al. 2015; Öztürk et al. 2015). On the other hand, some studies relate to ecological and faunistic features of mollusks in İskenderun Bay (Houart 2000; Çevik & Sarıhan 2004; Çevik & Ergüden 2004; 2008; Öztürk et al. 2008) have also been carried.

In the present study, the temporal variation of mollusks recorded on the soft bottoms in the north-western part of İskenderun Bay was analyzed.

Benthic samples were collected from the soft substrates (mud, sandy mud and silt) at 12 stations by means of the van Veen grab sampler at a depth ranging from 3 to 37 m in July 2012, August 2013 and July 2014 (Table 1, Figure 1). The sampled material was sieved through a mesh (0.5 mm) and fixed in a 4% formalin solution in the field. The molluscan specimens were separated from the other taxa using also a stereomicroscope and preserved in 70% ethanol in the laboratory. Next, the specimens were identified and counted. The total wet weight of each sample was estimated by using a 0.0001 g sensitive balance.

Figure 1

To analyze the community structure, Soyer’s frequency index (F), Shannon-Weaver’s diversity index (log₂ base) (H’) and Pielou’s evenness index (J’) were calculated for each station in 2012, 2013 and 2014. According to Soyer’s frequency index, the species with the frequency value (F) greater than or equal to 50% were considered as “Constant”, those with the F value between 25% and 49% as “Common” and species with the F value below 25% were considered as “Rare”. The dominance of mollusks in the samples was also calculated. The abundance data from the stations in each sampling period were analyzed using cluster and multidimensional scaling (MDS) techniques, based on Bray-Curtis similarity using the PRIMER package (Clarke & Warwick, 2001) in order to determine the temporal variation. Prior to the cluster and multidimensional scaling analyses, the raw data (the number of individuals) were transformed using the transformation yji=log(xji+1). SIMPER analysis was applied to indicate the percentage contribution of each species to all similarities or dissimilarities in each of the groups identified through the cluster analysis. Density values of some important mollusk species were processed on the map using the SURFER programme.

The investigated material was deposited at the Museum of the Faculty of Fisheries, Ege University (ESFM), İzmir, Turkey.

The analysis of grab samples revealed a total of 133 molluscan species, including 64 species identified in the material sampled in 2012, 64 species – in the material of 2013 and 86 mollusk species – in the material of 2014 (Table 2). Although the number of species increased in the subsequent years, the number of individuals and the total biomass values decreased to reach 2927 ind. and 887.53 g m^-2 in 2012, 2539 ind. and 413.08 g m^-2 in 2013, and 2318 ind. and 137.24 g m^-2 in 2014 (Table 2). Of the species identified in the present study, the most abundant species were Bittium reticulatum (da Costa, 1778) (39%) in 2012, Cerithidium diplax (Watson, 1886) (43%) in 2013 and Finella pupoides Adams, A., 1860 (41%) in 2014. As for the frequency index values, the most frequent species were Corbula gibba (Olivi, 1792) (83%), C. diplax (75%) and Nassarius pygmaeus (Lamarck, 1822) (75%) in 2012, F. pupoides (100%), C. diplax (100%) and B. reticulatum (75%) in 2013, followed by F. pupoides (92%), B. reticulatum (83%) and N. pygmaeus (83%) in 2014 (Table 2).

Temporal variation in terms of the community parameters (the number of species, the number of individuals, the biomass value, the diversity index value and the evenness index value) at all the stations is presented in Table 3. In 2012 and 2013, the largest number of species and individuals was encountered at station 4 (44 species and 11910 ind. m^-2), and at station 10 (28 species, 7490 ind. m^-2). In 2014, the largest number of species was encountered at stations 1 and 10 (33 species), whereas the largest number of individuals was found at station 4 (4330 ind. m^-2).

The highest biomass values were determined at stations 4 and 11 due to the presence of Gonomurex persicus (Swainson, 1821) (max 204.371 g m^-2 at station 4) and (max 378.08 g m^-2 at station 11) in 2012 and 2013, respectively. The highest diversity index values were calculated at stations 10 (3.94) in 2014 and at station 1 (3.74) in 2012 and 2013. The highest evenness values were determined at station 9 (0.95), at station 12 (0.85) and at station 7 (0.79) in 2012, 2013 and 2014, respectively (Table 3).

A total of 26 alien species were identified in the study area. The majority of the alien species (22 species) have entered the Mediterranean via the Suez Canal, the others (C. diplax, C. perparvulum, G. persicus and Ergalatax junionae Houart, 2008) are known to be introduced by shipping traffic (Çınar et al. 2011). Although the number of alien species found in 2012 and 2013 were 14 and 13 respectively, it increased to 24 species in 2014.

Based on Bray-Curtis similarity values higher than 40%, seven groups of stations (A-G) can be distinguished in MDS (Figure 2). Five species affect the similarity (dissimilarity) between the years and the stations. Cerithidium diplax was the species with the strongest effect on the similarity (dissimilarity) among the samples collected in different years (Table 4).

Figure 2

In 2012, 2013 and 2014, the density of C. diplax and F. pupoides was examined at different stations in the region (Figure 3). The density values of C. diplax varied between 20 ind. m^-2 (station 9) and 2660 ind. m-2 (station 10) in 2012, 50 ind. m^-2 (station 8) and 3870 ind. m^-2 (station 2) in 2013 and 10 ind. m^-2 (station 8) and 1170 ind. m^-2 (station 2) in 2014. The density of F. pupoides at station 10 in 2012 (1290 ind. m^-2) and 2013 (2110 ind. m^-2) was much higher than at the other stations. However, two stations (4 and 9) were represented by the highest density of F. pupoides, 2940 ind. m^-2 and 2130 ind. m^-2 respectively in 2014 (Figure 3).

Figure 3

A total of 133 molluscan species belonging to 58 families were identified in the present study carried out in İskenderun Bay. Gastropoda was the richest class, with 36 families and 94 species, followed by Bivalvia (21 families, 37 species) and Scaphopoda (1 family, 2 species). Among them, C. gibba, N. pygmaeus and T. communis are known as pollution indicators (Diaz & Rosenberg 1995; Çınar et al. 2006; Moreira et al. 2010). C. gibba and N. pygmaeus also had a wide distribution in the study area. It is a known fact that C. gibba is one of the indicators of anoxic conditions and environment rich in organic matter (Diaz & Rosenberg 1995). Çınar et al. (2006) reported that the species forms large populations (15860 ind. m^-2) in the inner part of İzmir Bay (Aegean coast of Turkey), which is the most polluted area of the bay. In the same study, Nassarius pygmaeus was also reported as a species forming a dense population in the polluted areas of İzmir Bay. Turritella communis, which was encountered only in the samples collected in 2013, is known as a species distributed in semi-polluted waters (Moreira et al. 2010).

The temporal variation of the soft bottom molluscan fauna in İskenderun Bay was found to be somewhat similar to that reported by Çınar et al. (2012) from Mersin Bay (Levantine coast of Turkey), where B. reticulatum, C. diplax, C. gibba, N. pygmaeus and T. communis were the most abundant species. The authors also reported that in the more polluted stations in Mersin Bay, C. diplax and F. pupoides were found to form larger populations compared to those of native species such as C. gibba, N. pymaeus and T. communis.

According to Çınar et al. (2012), alien species can affect the composition of the local molluscan fauna in the polluted areas as it was observed in İskenderun Bay where C. diplax and F. pupoides were the dominant components of the molluscan fauna, and C. gibba, N. pygmaeus and T. communis did not form dense populations in the region.

Furthermore, C. gibba, N. pygmaeus, F. pupoides, C. diplax and B. reticulatum which were widely distributed in the sampling area, contributed extensively to the similarity or dissimilarity of the stations in different years.

Gonomurex persicus is one of the alien species reported in the present study, which attracts attention due to its high biomass value. Similarly, in the study conducted by Mutlu & Ergev (2008), this large gastropod was the most dominant species of the soft-bottom at a depth from 1 and 10 m, accounting for 97% of the total biomass in Mersin Bay.

The number of species encountered in 2014 was higher compared to 2012 and 2013 in the present study. Ten of the species that caused the increase in the number of species in 2014 were alien species previously known from the area. Although the increase in the total species number in any area could be accepted as an indicator of the biodiversity, the increase in the number of alien species might be considered as a threat to the populations of native species.

This study is the first attempt to explain the temporal variation of the soft-bottom molluscan fauna in the north-western part of İskenderun Bay. Further studies should be carried out, including also deeper stations to better understand the components of the biodiversity and the effect of alien species in the region.