Macro-benthic invertebrates associated with the black sponge Sarcotragus foetidus (Porifera) in the Levantine and Aegean Seas, with special emphasis on alien species

Estuarine, Coastal and Shelf Science 227 (2019) 106306

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Macro-benthic invertebrates associated with the black sponge Sarcotragus foetidus (Porifera) in the Levantine and Aegean Seas, with special emphasis on alien species

T

Melih Ertan Çinara,*, Kerem Bakira, Alper Doğana, Sermin Açikb, Güley Kurtc, Tuncer Katağana, Bilal Öztürka, Ertan Dağlia, Tahir Özcand, Fevzi Kirkima Ege University, Faculty of Fisheries, Department of Hydrobiology, Bornova, İzmir, Turkey Dokuz Eylül University, Institute of Marine Sciences and Technology, İnciraltı, İzmir, Turkey Sinop University, Faculty of Art and Sciences, Department of Biology, Sinop, Turkey d Iskenderun Technical University, Faculty of Marine Sciences and Technology, Hatay, Turkey a

b c

A B S T R A C T

The fauna associated to the sponge Sarcotragus foetidus was studied in two eco-regions of the Mediterranean Sea, the Aegean and Levantine Seas. A total of 134 species belonging to 8 taxonomic groups were determined. Different species assemblages were encountered in the eco-regions, mainly due to the importance of some alien species (Red Sea invaders) on sponge communities. Among community parameters, only the number of species differed significantly among the sub-regions. The number of species and the number of individuals were significantly and positively correlated with the sponge volume. The species assemblage patterns determined were significant correlated with a set of environmental variables such as nitrogen, phosphate and dissolved oxygen. Some alien species such as the ophiuroid Ophiactis savignyi and the polychaete Leonnates indicus densely invaded porous systems of sponges in the Levantine Sea, indicating the magnitude of impacts of alien species on the eastern Mediterranean ecosystem. In the Levantine Sea, the alien species accounted for 34% of total number of individuals of macro-invertebrates associated with sponges, but the percentage rose up to 64% in Iskenderun Bay (eastern-most point of studied area). The biotic index ALEX detected a moderate ecological status in the area in terms of the impacts of alien species on native biodiversity.

1. Introduction Sponges with large surface areas and complex canal systems are densely inhabited by many marine species. They provide their associated fauna a secure shelter from predators (Klitgaard, 1995; Çinar et al., 2002), food (Fauchald and Jumars, 1979; Pawlik, 1983) as well as a spawning ground for many fish (Tyler and Böhlke, 1972; Konecki and Targett, 1989) and invertebrates (Erdman and Blake, 1987; Sardá et al., 2002; Ribeiro et al., 2003). The life cycle of some associated species (e.g. Haplosyllis spongicola) solely occurs in the host (Neves and Omena, 2003). Sponges as a biogenic substratum, and the morphofunctional diversity of their associated biota constitute a unique benthic community, whose structures are governed by a number of factors, but mainly by the morphology of sponges (Koukouras et al., 1985; Klitgaard, 1995), the zoogeographic region (Pavloudi et al., 2016), nearby habitats (Voultsiadou-Koukoura et al., 1987; Çinar et al., 2002; Ávila and Ortega-Bastida, 2015), environmental conditions (Duarte and Nalesso, 1996; Peattie and Hoare, 1981) and species interactions within complex canal systems (Çinar et al., 2002). However, the structure of different layers existing on sponges such as cortex and choanosome

*

(Gherardi et al., 2001) and the bioactivity of sponges (Skilleter et al., 2005) were also proved to largely affect the composition of associated fauna. The faunal associates might show a clear seasonality (Pansini, 1970; Koukouras et al., 1996). One of the large-sized sponges of the Mediterranean Sea, the black sponge Sarcotragus foetidus, preferably lives in hard-substrata of the shallow waters and exceeds a diameter of 100 cm (Manconi et al., 2013). Its surface and complex canal system made it a suitable biogenic habitat for a number of invertebrates. The associated fauna of the sponge (also cited as Ircinia/Sarcotragus muscarum) were specifically investigated in the both sides of the Aegean Sea (Koukouras et al., 1985, 1992; Çinar and Ergen, 1998; Çinar et al., 2002), and along the coasts of Tunisia (Rützler, 1975), Italy (Pansini and Daglio, 1980), Israel (Ilan et al., 1994) and Cyprus (Pavloudi et al., 2016). Among the abovementioned studies, only Ilan et al. (1994) and Pavloudi et al. (2016) reported faunal compositions of S. foetidus from the Levantine Sea. In addition, Çinar (2003, 2005) determined a number of polychaete species on S. foetidus collected from the northern Cypriot coasts. Based on data of the present study, some sipunculans (Açik, 2011), polychaetes (Çinar, 2009; Kurt Sahin and Çinar, 2009, 2017) and crustaceans

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

https://doi.org/10.1016/j.ecss.2019.106306 Received 7 January 2019; Received in revised form 25 June 2019; Accepted 28 July 2019 Available online 09 August 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.

Estuarine, Coastal and Shelf Science 227 (2019) 106306

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Fethiye Bays) parts (Kurt-Sahin and Çinar, 2017). Within the framework of a project (TUBITAK Project, Title: Zoobenthic community structures along the Levantine coasts of Turkey and impacts of Lessepsian species on them, Code number: 104Y065), different hard-bottom habitats (i.e. algae, mussels, sponges) were sampled at 55 stations along the coasts of Levantine (53 stations) and Aegean (2 stations) Seas in SeptemberOctober 2005. Due to availability, colonies of Sarcotragus foetidus were sampled only at 10 stations (8 stations in the Levantine Sea, 2 stations in the Aegean Sea). The sponge colonies at stations were collected by snorkeling or scuba-diving at 2–3 m depths. Three sponge colonies were randomly taken from each station. The sponge colonies were carefully removed from hard substrata (bare rocks) using a knife and immediately placed into cloth bags under sea-water. The sponge's volume was measured by water displacement method in the field as proposed by Koukouras et al. (1985). The total sponge volumes gathered at stations and the regions varied, almost 11000 ml (mean: 738 ml ± 609 SD) in the eastern Levantine Sea, 5995 ml (mean: 666 ml ± 459 SD) in the western Levantine Sea and 7590 ml (mean: 1265 ml ± 759 SD) in the Aegean Sea. The sponge colonies were then put into different jars and fixed with 4% formaldehyde. In the laboratory, the colonies were first rinsed in freshwater and then carefully cut into small pieces to gather macro-benthic individuals living within canals. The individuals taken from sponges were sorted according to major taxonomic groups and then preserved in 70% ethanol. The faunal components of the sponges were then identified and counted. The macro-benthic individuals identified were deposited at ESFM (Ege University Faculty of Fisheries Museum).

(Ozcan and Katağan, 2011; Bakir and Katağan, 2014) were previously reported in association with S. foetidus (cited as S. muscarum or Sarcotragus sp.) distributed along the northern part of the Levantine Sea. The shallow-water benthic habitats of the Levantine Sea have been intensively invaded by alien species, especially those introduced from the Red Sea via the Suez Canal (i.e. Lessepsian species, Zenetos et al., 2010, 2017; Çinar et al., 2011). The importance of Lessepsian species in benthic communities decreases when moving from the eastern to the northern and western parts of the Mediterranean Sea (Çinar et al., 2011), and with increasing depth (Çinar et al., 2012). They were found both in hard and soft substrata, and in hard substrata, they dominated facies of different algal species (Çinar, 2009; Bakir and Katağan, 2014) and mussels (Çinar et al., 2017). The presence of alien species on sponges along the Levantine Sea was first reported by Ilan et al. (1994), who reported Leonnates indicus (cited as L. jousseaumei) and Hydroides heterocerus on Sarcotragus cf. muscarum and Ircinia cf. retidermata collected from the bathyal environment (830 m) off Haifa (Israel). In subsequent works (i.e. Çinar, 2005, 2009; Kurt Sahin and Çinar, 2017), some other alien species were reported on Sarcotragus foetidus (cited as Sarcotragus sp., or S. muscarum). The present study aims 1) to define the structure of faunal associations of Sarcotragus foetidus distributed along the coasts of the Levantine and Aegean Seas, representing different eco-regions within the Mediterranean Sea (Spalding et al., 2007), and 2) to assess if the spatial variability in the composition of the associated invertebrates is governed by the environmental variables of the habitat as well as by the volume of the sponge. The reason for choosing different eco-regions was to determine possible variability in the species assemblages in space and to encounter the importance of alien species on the faunal associations of sponges inhabiting “densely invaded” (Levantine Sea) and relatively “less invaded” (Aegean Sea) areas.

2.2. Statistical analyses Based on the species-sample (sponge colony) data matrix constructed, the community parameters such as the number of species (S), the number of individuals (N), the Shannon-Weiner's diversity index (H′) and the Pielou's evenness index (J′) were estimated to characterize the community structures at stations and in the eco-regions. ALEX index was used to estimate ecological status of stations based on the importance of alien species on the community (Çinar and Bakir, 2014). The variability in community parameters (using Euclidean distance resemblance matrix) and species assemblages (using Bray-Curtis resemblance matrix) between eco-regions was estimated by using PERMANOVA. Pair-wise routine was run to evaluate the significance of the

2. Material and methods 2.1. Study area and sampling The sampling area includes two-ecoregions, namely the Aegean and Levantine Seas (Fig. 1). Furthermore, according the intensity of alien species on the benthic habitats, the northern part of the Levantine Sea (Turkish coast) was divided into two parts, eastern (including Mersin and İskenderun Bays) and western (including Antalya, Finike and

Fig. 1. Map of the studied area with the location of sampling sites. 2

Estuarine, Coastal and Shelf Science 227 (2019) 106306

M.E. Çinar, et al.

correlation values between the sponge volume, and the abundances of the amphipod Tritaeta gibbosa (r = 0.63, P < 0.05), and the nereidid polychaetes Composetia costae (r = 0.50, P < 0.05) and Leonnates indicus (r = 0.45, P < 0.05) were positive and statistically significant.

geographical regions. The assemblage multivariate pattern was explored and visualized using non-metric multidimensional scaling analysis (nMDS), applied on the Bray-Curtis resemblance matrix. The BrayCurtis analysis was applied to differentiate species assemblages in the region (Bray and Curtis, 1957) and the result at two similarity levels (30% and 40%) was visualized in the nMDS graph. Prior to analysis, the raw data were transformed by using the transformation log (x+1). Finally, the similarity percentages analysis (SIMPER) was applied to the species matrices in order to identify the species which significantly contributed to the similarity of groups of samples. Relationships between multivariate community structures and environmental variables were assessed using the BIOENV procedure. Spearman's rank correlation coefficient analysis was used to determine relationships between environmental variables and community parameters; and Pearson's product-moment correlation coefficient analysis was used to determine relationships between sponge volume and community parameters (Gaddis and Gaddis, 1990). All analyses were performed by using the packages PRIMER v7 (Clarke and Gorley, 2006) and STATISTICA.

3.4. Species assemblages According to the Bray-Curtis Similarity Index analysis, three groups of species associations were identified at around 40% and 30% similarity levels (Fig. 6). At 40% similarity, the eco-regions were separated, but the sub-regions did not show any recognizable pattern, with stations located in different sub-regions in the Levantine Sea being grouped together. According to SIMPER analysis, ten species were mainly responsible for the groupings at the 40% and 30% similarity levels (Table 4). At 40% similarity level, Ophiactis savignyi and Synalpheus gambarelloides made more than 30% contributions to the constructions of the groups A1 and B1. SIMPER analysis showed that the Levantine Sea stations had lower similarity when compared to the Aegean Sea stations (Table 5). The average abundances of some dominant and wide-spread species of the sponge associations, such as S. gambarelloides, T. gibbosa and Composetia costae in the Levantine Sea were two or three times lower that those estimated in the Aegean Sea. The abundances of these species also contributed much in the discriminations of sub-regions of the studied area. Variations in species associations were significant between ecoregions and among sub-regions (PERMANOVA, P < 0.01) (Table 3). Among environmental variables, total inorganic nitrogen (r = 0.56) and silica (r = 0.43) were moderately correlated with the first MDS axis, whereas phosphate (r = 0.62) and silica (r = 0.37) had the highest correlation values in relation to the second MDS axis (Fig. 6). The BIOENV analysis showed that three environmental variables (total inorganic nitrogen, silica and oxygen) were best matched with the community data (r = 0.44).

3. Results 3.1. Species composition of associated fauna Within canals and on surfaces of the colonies of Sarcotragus foetidus collected from the Levantine and Aegean Seas, a total of 134 macrobenthic species and 2892 individuals belonging to 8 taxonomic groups (Platyhelminthes, Nemertea, Sipuncula, Polychaeta, Crustacea, Mollusca, Echinodermata and Tunicata) were encountered (Table 1). The most speciose group was Polychaeta, accounting for 55% of the total number of species, followed by Crustacea (30%) and Mollusca (5%) (Fig. 2). Crustacea were the most abundant on sponges, constituting 62% of the total number of individuals, followed by Polychaeta (20%) (Fig. 2). The dominant species in the studied area were Synalpheus gambarelloides (26% of total number of individuals), Tritaeta gibbosa (23%) and Ophiactis savignyi (11%) (Fig. 3). The dominant species on S. foetidus varied among the ecoregions; S. gambarelloides and T. gibbosa comprised 76% of the faunal populations in the Aegean Sea, whereas they accounted for only 37% of the faunal populations in the Levantine Sea. The dominant species (O. savignyi and Leonnates indicus) on the Levantine Sea's sponges (comprising 22% of the total number of individuals) were aliens and totally absent in the Aegean Sea.

3.5. Alien species A total 16 alien species belonging to four taxonomic groups (Polychaeta, Crustacea, Mollusca and Echinodermata) were found on sponges; 12 polychaete, 1 crustacean, 2 bivalves and 1 ophiuroid species (see Table 1). Three species dominantly occurred within sponge canals, namely, Ophiactis savignyi (61%), Leonnates indicus (24%) and Ceratonereis mirabilis (5%), comprising 90% of total number of individuals of alien species on sponges. The ratio between the number of alien and native species in the studied area is 0.12 (mean: 0.19 ± 0.12 SD), and that between the number of individuals of alien species and native species is 0.21 (mean: 0.34 ± 0.56 SD). In total, the alien species accounted for 17% of populations of the associated fauna. This percentage rose up to 34% in the Levantine Sea. The importance of alien species both in terms of the number of species and individuals varied among stations, but they attained their maximum values at station 1 located in İskenderun Bay, where alien species represented 64% of total number of individuals associated with sponges at this station (Fig. 7). A weak positive correlation (r = 0.18) was estimated between the abundances of alien and native species on the Levant Sea's sponge samples. Alien species occurred solely on sponge samples collected from the Levant Sea, no alien species was found on sponges collected from the Aegean Sea (Fig. 8). The number of alien species and individuals in the Levantine Sea ranged from 1 (station 7) to 8 (station 39), and 1 (station 7) to 167 (station 1), respectively. The ecological status of stations in terms of the importance of alien species in benthic communities was investigated by using the index ALEX that classified one station (station 1) as moderate, three stations (stations 3, 6 and 8) as good, and others as high (Fig. 9).

3.2. Community parameters The number of macro-benthic species (S) on sponge samples ranged from 2 to 33, the number of individuals (N) from 19 to 267, the diversity index value (H′) from 0.24 to 4.47, the evenness index value (J′) from 0.24 to 0.92. The highest mean number of species (23 species) was estimated at station 8, the highest mean number of individuals (189 individuals) at station 9, the highest mean diversity index value (H' = 3.7) at station 8 and the highest mean evenness index value (J' = 0.84) at station 2 (Fig. 4). The community parameters did not differ significantly between eco-regions and among sub-regions, except for the number of individuals (PERMANOVA, P < 0.05) (Table 2). The mean value of H' (2.34 ± 0.35 SE) in the Levantine Sea is slightly higher than that (H' = 2.29 ± 0.35 SE) estimated in the Aegean Sea, whereas the mean number of species (S = 14 ± 2.3) in the Levantine Sea was lower than that (S = 17 ± 0.7) found in the Aegean Sea. 3.3. Relationships between sponge volume and community parameters The relationships between the volume of sponge (V) and the community parameters (S, N, H′ and J′) were depicted in Fig. 5. Among them, only the number of species and the number of individuals were significantly and positively correlated with the sponge volume (r > 0.60, P < 0.05). Among the dominant species, only the 3

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Table 1 List of species and their total abundances (sum of three replicates) found on the colonies of Sarcotragus foetidus collected at stations from the Levantine and Aegean Seas. *denotes alien species. E-LS: Eastern Levantine Sea, W-LS: Western Levantine Sea. Ecoregions

Levantine Sea

Subregions

E-LS

Stations

1

2

3

4

5

6

7

8

9

10

1

2

–

–

–

–

–

–

–

–

–

1

–

–

–

–

–

7

–

–

– – 8 11

– – 38 15

– – – 22

– – 7 6

– – 5 –

– – 7 1

– – – –

1 2 1 3

– – 4 2

– – 3 4

– – – – – – – – – – – 11 – – – – 30 – – – – 1 1 – 1 1 – – – – – – – – – – – – 6 – – 2 – – 1 – – 1 – – – – – – – – – – –

– – – 1 – – – 1 – – – 4 – – 1 – 1 – – – – – – – – – 1 – – – 1 – – 2 – 1 – – 4 – – – – – 3 – – – – – 2 – – 3 – – 1 – –

1 1 2 – – – 1 – – 4 – 32 – – – 1 5 2 – 1 – 1 – 1 – – – – 1 – – 2 1 – – 9 4 17 70 – – 4 – – – – – – – – – – – – 1 1 – 1 4

– – – – – 2 – – – – – – – – – – – – – – – – – – – – – – – – 2 – – – – – – 1 7 – – 3 – – – – – – – – – – – 1 – – 1 – –

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – 1 – – – – – 3 – – 9 – – 2 – 2 – – 1 – – – – – – 8 – – – – 3

– – – – – 1 – – – – – 2 – – – – – – – – – – – – – – – – – – – – – – 1 – – 3 – – – 1 – – 2 – – – – – – – – – – – 2 – –

– – – – – 1 – – – – – – – – – – – – – – – – – – – – – – – – 6 – – – – 1 – – 1 – – – – – – – – – – – – 1 – – – – – – –

– 8 – – 3 2 – 1 1 – 4 23 2 1 3 – 5 – – 1 1 – – – – – – 2 – 1 3 – – – – 7 – 5 23 6 – 2 6 – – 1 – – – 1 – – – 2 – – – – –

– – – 4 7 – – – – – – – – – – – 1 – 1 1 – – – – – – 1 – 1 1 1 – 3 – – 6 – – – – 5 – – – – – – – – – – – 1 – 1 1 1 – –

– 3 – – 8 – – – – – – – – – – – 1 – – – – – 1 – – – – – 1 – – – – – 2 30 1 – – – – – – – – – – – 1 – – – – – – – – – –

PLATYHELMINTHES Turbellaria (sp.) NEMERTEA Nemertea (sp.) SIPUNCULA Golfingia (Golfingia) vulgaris (de Blainville, 1827) Phascolion (Isomya) tuberculosum Théel, 1875 Phascolosoma (Phascolosoma) stephensoni (Stephen, 1942) Aspidosiphon (Aspidosiphon) misakiensis Ikeda, 1904 POLYCHAETA Pontogenia chrysocoma (Baird, 1865) Harmothoe spinifera (Ehlers, 1864) Harmothoe sp. Lepidonotus clava (Montagu, 1808) Lepidasthenia elegans (Grube, 1840) Chrysopetalum debile (Grube, 1855) *Eurythoe complanata (Pallas, 1766) *Linopherus canariensis Langerhans, 1881 Eulalia tripunctata McIntosh, 1874 Psamathe fusca Johnston, 1836 Syllidia armata Quatrefages, 1865 Branchiosyllis exilis (Gravier, 1900) Brania pusilla (Dujardin, 1851) Eusyllis lamelligera Marion & Bobretzky, 1875 *Exogone breviantennata Hartmann-Schröder, 1959 Exogone dispar (Webster, 1879) Haplosyllis spongicola (Grube, 1855) Myrianida convoluta (Cognetti, 1953) Odontosyllis ctenostoma Claparède, 1868 Odontosyllis fulgurans (Audouin and Milne Edwards, 1833) Paraehlersia ferrugina (Langerhans, 1881) Proceraea aurantiaca (Claparède, 1868) Proceraea paraurantiaca Nygren, 2004 Salvatoria clavata (Claparede, 1863) Sphaerosyllis austriaca Banse, 1959 Sphaerosyllis pirifera Claparède, 1868 Syllis armillaris (O. F. Müller, 1776) Syllis ferrani Alós and San Martín, 1987 Syllis garciai (Campoy, 1982) Syllis gerlachi Hartmann-Schröder, 1960 Syllis gracilis Grube, 1840 Syllis jorgei San Martín & López, 2000 Syllis prolifera Krohn, 1852 Syllis sp. Trypanosyllis zebra (Grube, 1860) Composetia costae (Grube, 1840) Composetia hircinicola (Eisig, 1870) *Ceratonereis mirabilis Kinberg, 1866 *Leonnates indicus Kinberg, 1866 Nereis zonata Malmgren, 1867 Platynereis dumerilii (Audouin and Milne Edwards, 1833) *Pseudonereis anomala Gravier, 1900 Lumbrineris coccinea (Renier, 1804) Lumbrineris latreilli Audouin and Milne Edwards, 1834 *Lumbrineris perkinsi Carrera-Parra, 2001 Eunice vittata (Delle Chiaje, 1828) *Leodice antennata Savigny in Lamarck, 1818 Lysidice ninetta Audouin and Milne Edwards, 1833 Lysidice unicornis (Grube, 1840) Marphysa fallax Marion & Bobretzky, 1875 Palola siciliensis (Grube, 1840) *Palola valida (Gravier, 1900) Dorvillea rubrovittata (Grube, 1855) *Dorvillea similis (Crossland, 1924) Arabella iricolor (Montagu, 1804) Prionospio maciolekae Dağli & Çinar, 2011 Dasybranchus gajolae Eisig, 1887 Leiocapitella dollfusi (Fauvel, 1936) Notomastus lineatus Claparède, 1869

Aegean Sea W-LS

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Table 1 (continued) Ecoregions

Levantine Sea

Aegean Sea

Subregions

E-LS

Stations

1

2

3

4

5

6

7

8

9

10

*Notomastus mossambicus Thomassin, 1970 Dodecaceria sp. Polyophthalmus pictus (Dujardin, 1839) Sabellaria spinulosa (Leuckart, 1849) Amphitrite cf. rubra (Risso, 1826) Amphitrite variabilis (Risso, 1826) Amphitritides gracilis (Grube, 1860) Amaeana trilobata (Sars, 1863) *Polycirrus twisti Potts, 1928 Polycirrus sp. Amphiglena mediterranea (Leydig, 1851) Branchiomma bombyx (Dalyell, 1853) Parasabella langerhansi (Knight-Jones, 1983) Serpula concharum Langerhans, 1880 Spirobranchus polytrema (Philippi, 1844) CRUSTACEA Apseudopsis latreillii (Milne-Edwards, 1828) Chondrochelia savignyi (Kroyer, 1842) Tanais dulongii (Audouin, 1826) Ampithoe ramondi Audouin, 1826 Apherusa chiereghinii Giordani- Soika, 1950 Caprella sp. Colomastix pusilla Grube, 1861 Elasmopus pocillimanus (Bate, 1862) Gammarella fucicola (Leach, 1814) Hyale schmidti (Heller, 1866) Leptocheirus bispinosus Norman, 1908 Leucothoe richardii Lessona, 1865 Leucothoe spinicarpa (Abildgaard, 1789) Leucothoe venetiarum Giordani- Soika 1950 Maera grossimana (Montagu, 1808) Maera inaequipes (Costa, 1857) Maera pachytelson Karaman & Ruffo, 1971 Podocerus variegatus Leach, 1814 Tritaeta gibbosa (Bate, 1862) Urothoe grimaldii Chevreux, 1895 Cyathura carinata (Krøyer, 1847) Cymodoce truncata Leach, 1814 Carpias stebbingi (Monod, 1933) Cymodoce emarginata Leach, 1818 Cymodoce tuberculata Costa in Hope, 1851 Dynamene edwardsi (Lucas, 1849) Dynamene torelliae Holdich, 1968 Gnathia vorax (Lucas, 1849) Gnathia maxillaris (Montagu, 1804) Janira maculosa Leach, 1814 Eudorella truncatula (Bate, 1856) *Alpheus rapacida de Man, 1908 Alpheus dentipes Guérin-Méneville, 1832 Athanas nitescens (Leach, 1814) Cestopagurus timidus (Roux, 1830) Periclimenes scriptus (Risso, 1822) Pilumnus hirtellus (Linnaeus, 1761) Pisidia bluteli (Risso, 1816) Porcellana platycheles (Pennant, 1777) Synalpheus gambarelloides (Nardo, 1847) MOLLUSCA Melanella polita (Linnaeus, 1758) Arca tetragona Poli, 1795 Striarca lactea (Linnaeus, 1758) *Brachidontes pharaonis (P. Fischer, 1870) Musculus costulatus (Risso, 1826) *Malvufundus regula (Forsskål in Niebuhr, 1775) Venerupis corrugata (Gmelin, 1791) ECHINODERMATA Amphipholis squamata (Delle Chiaje, 1828) Amphiura chiajei Forbes, 1843 *Ophiactis savignyi (Müller &Troschel, 1842) Ophioderma longicauda (Bruzelius, 1805) Ophiura sp. TUNICATA

– – 1 – – – – – – – 2 – – – –

– – 2 1 – – – 1 – – – – – – –

1 – 3 – 2 – – – 2 – – – – 1 –

– – – – – – – – – – – – – – –

– – – – – – – – – 1 – – – – –

– – – – – – 1 – – – – – – – –

– – – – – – – – – – – – – – –

– – 12 – 1 – – – – 12 – – 1 – –

– 1 1 1 – 2 – – – – 1 2 – – 1

– – – – – 6 – – – – – – – – –

2 3 – – – – – 3 – – – – 1 – – 1 – – – – – – – – – – 3 10 – 1 – – – – – – – – – –

10 1 1 – – 1 – 5 – – – – – – – – – – – – – – – – – – – – – – – – 1 – – 1 – – 1 –

– – – – – – – – 1 2 – 6 – – 1 24 1 – 183 1 2 1 – – – – – – – 1 – 2 2 – – – 1 – – 61

1 – – – – – – 1 – 1 – – – 48 – – – – 18 – – – – – – – – – – – – – 2 – – – – – – 73

– – – – – – 2 – – – – – 40 – – 3 – – 78 – – – – – – – – – – – – – – – – – – – – 77

5 1 1 – – – – 5 – 1 – – 7 – 1 2 – – 1 – – – 1 – – – 5 – 7 13 – – – – – – 2 – – 111

– – – – – – 4 – – – – – 7 – – 1 – – – – – – – – – – – – – – – – – – – – – – – 122

– 4 9 – 1 – 1 – – 3 1 – 15 – – 1 – – – – – – – – – 1 – – 1 – 1 1 2 2 1 1 3 2 – –

– 1 – – – – – 4 – 2 – – 49 – – 2 – 1 265 – – – – – – – – – – 3 – – – – – – – – – 188

– 2 – 1 – 2 1 1 – 2 – – 14 – – 7 – – 130 – – – 2 1 4 – – – – 7 – – – – – – – – – 121

– – – 2 – 1 –

– 1 5 – – – 1

– – – – – – –

3 – – – – – –

– – – – – – –

– – – – – – –

– – – – – – –

– – – – – – –

– – – – – – –

– – – – 1 – –

– – 155 – 1

– – – – –

– – 3 – –

– 1 – – –

– – – – –

2 2 148 – –

– – – – –

– – – 1 –

– – – – –

2 – – – –

W-LS

(continued on next page) 5

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Table 1 (continued) Ecoregions

Levantine Sea

Aegean Sea

Subregions

E-LS

Stations

1

2

3

4

5

6

7

8

9

10

Microcosmus polymorphus Heller, 1877 Ascidiacea (sp.)

– –

– 3

1 –

– –

– –

– –

– –

– –

– –

– –

W-LS

3.6. Correlations between environmental variables and community parameters The correlation values between the environmental variables, and community parameters and ALEX were depicted in Table 6. Only 10 correlation coefficient values were statistically significant. Significant, but weak (rs = 0.20–0.39) and moderate (rs = 0.40–0.59) correlations were estimated between evenness index, and temperature and salinity; between diversity index and salinity; between ALEX, and dissolved oxygen and phosphate. Strong correlations (rs = 0.60) were calculated between ALEX, and temperature and total nitrogen.

4. Discussion The colonies of Sarcotragus foetidus collected from the Aegean and Levantine Seas hosted a variety of invertebrates (134 species), among which Polychaeta was the dominant group in terms of the number of species. In the previous studies, Koukouras et al. (1985) and Çinar et al. (2002) listed 90 and 148 species, respectively, on colonies of this sponge collected from the Aegean Sea. In the Levantine (Cyprus) and Aegean Seas, Pavloudi et al. (2016) identified 90 species in association with S. foetidus. Sponge species (Agelas oroides, Aplysina aerophoba and Axinella cannabina) abundantly occurring in the shallow-water rocky habitats of the Aegean Sea also provide a good shelter for a number of invertebrates (265 species: Koukouras et al., 1996). In general, polychaetes were represented by higher number of species, but crustaceans occurred abundantly on sponge canals. However, Pavloudi et al. (2016) found that sponges collected from the north Aegean Sea (Sitonia) were mainly occupied by polychaete species in contrast to those collected from the Cypriot coast. In cave ecosystem of the Mediterranean Sea, crustaceans were dominant on sponges (Gerovasileiou et al., 2016). However, in tropical waters, polychaetes (especially Haplosyllis spongicola) were the most dominant component of the sponge associated fauna, comprising almost 96% of total faunal populations (Magnino and Gaino, 1998; Magnino et al., 1999; Neves and Omena, 2003). However, the reports of H. spongicola on sponges from tropical waters are questionable and Lattig and Martín (2011) identified three different species of Haplosyllis on sponges in the region. In a way that supports this view, Beepat et al. (2014) found a dense population of H. djiboutiensis (comprising 71% of the individuals collected) on the sponge Neopetrosia exigua along the coasts of Mauritius (tropical Indian Ocean). The species found in the present study can be regarded as facultative inhabitants representing the fauna commonly distributed in the eastern Mediterranean Sea. However, the Red Sea invaders, Leonnates indicus and Ophiactis savignyi, might represent as obligate sponge associates, as these species have never been reported in other habitats of the Mediterranean Sea so far. However, the presence of these species in the shallow-water benthic habitats (e.g. algae and coral debris) was reported in their native regions (Mladenov and Emson, 1988; Hutchings and Reid, 1991). The associated species found in the present study seem to utilize sponges as habitats. However, the syllids Branchiosyllis exilis and Haplosyllis spongicola, the snapping shrimp Synalpheus gambarelloides, and the amphipod Leucothoe spinicarpa, which were common and abundant on the sponges found in the studied area, are known to consume the sponge's tissues (Connes, 1967; Rützler, 1975; Martin and

Fig. 2. The dominance of taxonomic groups by the number of species (A) and the number of individuals (B).

Fig. 3. The most dominant species of associated fauna of Sarcotragus foetidus.

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Fig. 4. The mean number of species, abundance, and the diversity (H′) and evenness (J′) indices at stations, with + standart error.

Diversity values of the sponge faunal communities were found to be high at some stations (H' > 3), where the dominant species such as Tritaeta gibbosa, Synalpheus gambarelloides and Ophiactis savignyi were absent. Diversity values estimated in the Aegean Sea by Çinar et al. (2002) were higher (generally H' > 3–4) than those estimated in the present study. The diversity and evenness values showed a weak correlation with the sponge volume. This could be explained by the fact that larger sponges collected from the area were densely occupied by the amphipod Tritaeta gibbosa. This species is an epibiotic amphipod that lives in self-constructed pits on the outer surface of various hosts such as sponges, alcyonarian corals, ascidians and echinoderms (Scholtz, 2018). Sponges with large surface seem to enable this species to build up dense populations. Çinar et al. (2002) also indicated that there is no relationship between these community indices and the sponge volume. Previous studies emphasized that the number of species and/or individuals were correlated with the sponge volume (Westinga and Hoetjez, 1981; Koukouras et al., 1992; Duarte and Nalesso, 1996; Gherardi et al., 2001; Çinar et al., 2002; Ávila and Ortega-Bastida, 2015), which are in accordance with the present study. On the other hand, no link between sponge volume and the number of inhabitants was found in some other studies (Pansini and Daglio, 1980; Koukouras et al., 1985; Voultsiadou-Koukoura et al., 1987). Duarte and Nalesso (1996) emphasized that larger volume of sponges provided larger surfaces of canals that increased the probability of rare species occurrence. Fiore and Jutte (2010) stated that canal diameter influenced faunal density negatively but diversity positively. Ávila and Ortega-Bastida (2015) proved that not only sponge volume but also sponge height and mean oscular diameter of sponges were positively related to the richness and abundance of associated fauna. The dominancy of the species associated with Sarcotragus foetidus varied among eco-regions. In the western Aegean Sea, Koukouras et al. (1985) found that the cavities of the sponge S. foetidus (cited as S. muscarum) were mainly inhabited by Hiatella arctica (10%), Ceratonereis costae (10%), Leucothoe spinicarpa (7%) and Gammaropsis maculata (5%). In the eastern Aegean Sea, Çinar et al. (2002) reported the dominance of Tritaeta gibbosa and Synalphaeus gambarelloides on S.

Table 2 Results of PERMANOVA showing the significance of community parameters with regards two factors, ecoregions and subregions. Bold number is statistically significant (P < 0.05). EL: Eastern Levantine Sea, WL: Western Levantine Sea, AS: Aegean Sea. Source

df

SS

Number of Species Ecoregions 1 35.21 Residual 28 1578 Subregions 2 37.54 Residual 27 1576 Pair-wise test WL = EL = AS Number of Individuals Ecoregions 1 25085 Residual 28 131380 Subregions 2 25582 Residual 27 130880 Pairwise test WL = EL = AS Diversity Index Ecoregions 1 0.01 Residual 28 26.55 Subregions 2 0.42 Residual 27 26.13 Pairwise test WL = EL = AS Evenness Index Ecoregions 1 0.02 Residual 28 0.87 Subregions 2 0.04 Residual 27 0.86 Pairwise test WL = EL = AS

MS

Pseudo-F

P(perm)

Unique perms

35.21 56,37 18.77 58.37

0.62

0.44

48

0.32

0.72

633

25085 4692 12791 4848

5.35

0.02

320

2.63

0.08

990

0.01 0.95 0.21 -.97

0.01

0.92

964

0.22

0.80

999

0.02 0.03 0.02 0.03

0.63

0.42

966

0.59

0.58

998

Df: Degree of Freedom, SS: Sum of Squares, MS: Mean Squares.

Britayev, 2018) and thus could be regarded as facultative or obligatory parasites. However, the relationships between associated fauna and the host have not been fully understood. For example, excessive sponge spicules found in the gut content of Synalpheus species might indicate a parasitism, but Erdman and Blake (1987) postulated that this species feeds exclusively on necrotic tissue and therefore has a commensal relationship with the host. 7

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Fig. 5. The relationships between sponge volume, and the number of species, number of individuals, and the diversity and evenness indices. Table 3 Main and pair-wise tests of PERMANOVA based on log transformed speciesabundance data. Ecoregions and different parts of the study area were used as different fixed factors. Bold number is statistically significant (P < 0.05). EL: Eastern Levantine Sea, WL: Western Levantine Sea, AS: Aegean Sea. Source

df

SS

MS

Pseudo-F

P(perm)

Unique perms

Ecoregions Residual Subregions Residual

1 28 2 27

8387 78579 15350 71616

8387 2806 7675 2652

2,99

0.002

998

2,89

0.001

999

t

P(perm)

Unique perms

1,52 1,96 1,65

0.016 0.002 0.004

999 990 896

Pair-wise test for subregions

EL, WL EL, AS WL, AS

foetidus, together comprising almost 60% of the total number of individuals living inside the sponge. In the present study, the Aegean Sea's sponges were dominantly occupied by T. gibbosa and S. gambarelloides, whereas the Levantine Sea's sponges by S. gambarelloides and Ophiactis savignyi. The latter species, which was considered as a Lessepsian invader, was previously found in high abundance within the canals of sponges collected from Marmaris (southern Aegean Sea) (Çinar et al., 2002) and very common on sponges collected from Cyprus (Pavloudi et al., 2016). This species was also mentioned as the main component of the associated fauna of many sponge species from the Red Sea and the West Atlantic Ocean (Fishelson, 1966; Mladenov and Emson, 1988). Duarte and Nalesso (1996) reported that O. savignyi was the dominant endobiotic species, accounting for 64% of all individuals inhabiting the sponge Zygomycale parishi. The clonal aggregation reported for this species was primarily linked to its reproductive strategy on sponges (asexual), which were frequently occupied by all-male aggregations of this species (Mladenov and Emson, 1988). Darkness inside sponge canals provides a suitable habitat as, like most ophiuroids, it is characterized by a negative phototaxis (Hendler, 1984). High abundance of this ophiuroid species on sponges resulted in lower species diversity of

Fig. 6. The nMDS graph showing the relationship among stations, and the correlation of environmental variables with nMDS axes, represented by superimposed vectors. The similarity of stations was assessed using the Bray-Curtis similarity index and secondarily superimposed on the nMDS plot. Green line showing 30% similarity, blue dotted line showing 40% similarity.

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Table 4 Species contributing to similarity and dissimilarity among groups determined in Fig. 6. SIMILARITY

DISSIMILARITY

Similarity Levels 40%

30%

40%

30%

Groups in Fig. 6

A1

B1

B2

A

B

C

A1xB1

A1xB2

B1xB2

AxB

AxC

BxC

Mean Similarity/Dissimilarity

43

42

59

35

41

33

74

70

63

75

76

73

Branchiosyllis exilis Composetia costae Elasmopus pocillimanus Leonnates indicus Lepidasthenia elegans Leucothoe spinicarpa Ophiactis savignyi Phascolosoma stephensoni Synalpheus gambarelloides Tritaeta gibbosa

– – 8 – – – 30 12 –

– – – 11 – – – – 46 8

– – – – – 10 – – 18 19

– – 11 – – – 12 15 –

– – – – – 12 – – 37 15

14 9 – 14 – – – –

– – – – – – 11 – 5 5

– – – – – – 9 – 5 8

– 5 – – 5 – – – – 7

– – – – – – 6 – 6 6

– – – 3 – – 4 – – 3

5 – – 4 – – – – – 4

Table 5 Species contributing to similarity between ecoregions and subregions, and their average abundance. LS: Levantine Sea, AS: Aegean Sea, EL: Eastern Levantine Sea, WL: Western Levantine Sea, AA: Average Abundance, C% = percent contribution. Eco-Regions

Sub-Regions

LS

AS

EL

WL

AS

27

59

28

23

59

Regions

Similarity (%)

Branchiosyllis exilis Composetia costae Leonnates indicus Lepidasthenia elegans Leucothoe spinicarpa Phascolosoma stephensoni Synalpheus gambarelloides Tritaeta gibbosa

AA

C%

AA

C%

AA

C%

AA

C%

AA

C%

1.5 0.9 2 – 1.4 1.6

4 3 11 – 6 8

– 2.7 – 2.1 3.3 –

– 7 – 8 10 –

1.5 – 2.4 – – 2

4 – 17 – – 13

– – – – 2.3 –

– – – – 24 –

– 2.7 – 2.1 3.3 –

– 7 – 8 10 –

2.8

18

5

18

2.6

12

3.2

25

5

18

1.7

4

5.2

19

2.5

9

–

–

5.2

19

the associated fauna, mainly due to predation (Çinar et al., 2002). Ilan et al. (1994) reported that almost 75% of total number of individuals living inside S. foetidus (cited as S. muscarum) and Ircinia retidermata collected in deep-water environments (830 m) off the Israeli Mediterranean coast belonged to two Lessepsian invaders, Leonnates indicus and Hydroides heterocerus. As these two species are only known from the shallow-waters in the Mediterranean (Çinar, 2006, 2009) and world's oceans (Qiu and Qian, 2000; Ben-Eliahu and Ten Hove, 2011; see also Table 3 in the paper by Ilan et al., 1994), their presence in the deep water off Israel seems doubtful. In addition, the sponges S. foetidus and I. retidermata have never been reported in such deep waters in the Mediterranean (range: 0–400 m) (Pansini et al., 2011). The presence of these sponges in such a deep depth might be possibly due to discards from a fishing boat. Non-economic sponges such as Ircinia and Sarcotragus spp. captured by bottom-trawling (Petović et al., 2016) are regarded as by-catch and thrown into the sea after the fishing operation is complete (Voultsiadou et al., 2011). The area off the Israeli coast where sponge colonies were found is just 8 nautical miles away from the coastline of Haifa. The sponges might have been possibly fished in shallow-waters and discarded into the offshore area while sailing. Therefore, this report of the sponge species and their associated fauna in the deep water of the Mediterranean should be cited with a reservation. A relatively high number of alien species (totally 16 species) was found within canals of colonies of Sarcotragus foetidus collected from the

Fig. 7. The ratio between the native and alien species by the number of species (upper graph) and the number of individuals (lower graph) at stations.

Levantine Sea. These species were previously known from shallowwater benthic habitats such as algae (Kurt Şahin and Çinar, 2017) and mussels (Çinar et al., 2017), but their importance on sponges was unknown up to date. It seems that Red Sea invaders had been already invaded all available niches in the shallow-waters of the Levantine Sea. Two alien species, Ophiactis savignyi and Leonnates indicus prefer inhabiting large sponges such as Sarcotragus spp. in the region (Ilan et al., 1994; Çinar et al., 2002; Çinar, 2009). Interestingly, some alien species 9

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dominantly occurring in hard-bottom (i.e. Pseudonereis anomala and Dorvillea similis) and soft-bottom (i.e. Notomastus mossambicus) habitats (Çinar, 2005, 2009) occurred within the canals of sponges, indicating their wide-habitat preferences. However, their densities on sponges were not as high as those estimated in the other habitats. For example, the nereidid polychaete P. anomala can reach a population density of 2500 ind.m−2 on the alga Jania rubens along the Mediterranean coast of Turkey (Çinar and Altun, 2007), whereas it was only represented by 1–3 individuals on sponge colonies. The value of ALEX index decreased with increasing abundance of the alien species found in the present study and eventually classified one station as moderate ecological status, indicating the strong impact of alien species on the benthic community structures in the Levantine Sea. The ALEX values were positively and strongly correlated with total nitrogen and temperature. It seems that these variables are main factors that strongly govern the distribution of alien species. In soft and hard substrata, ALEX values were found to be also significantly correlated with the total nitrogen (Çinar and Bakir, 2014; Çinar et al., 2017). Temperature is a crucial factor for alien species in the Mediterranean introduced from the warm water of the Red Sea. This explains why the Levant Sea's sponges have been densely occupied by the Red Sea invaders. The average winter temperature of the surface water of the Levantine Sea is around 17 °C (Hecht et al., 1988; Çinar et al., 2012), which is almost the same recorded from the northern part of the Red Sea (Gulf of Suez) (El-Shanawy and El-Shanawy, 2006) and three degree higher than that in the central Aegean Sea (Shaltout and Omstedt, 2014). Therefore, most of Red Sea invaders were confined to the Levantine Sea or at least to the Lessepsian province (sensu Por, 1989). It was shown for the Red Sea species that a critical minimal temperature is crucial for the regulation of the reproductive periodicities (Pearse, 1969). However, Red Sea invaders gradually or rapidly (e.g. Fistularia commersoni) expand their distributional range westwards and northwards mainly due to their highly adaptive capacities (Bernardi et al., 2016) and human-induced global warming (Lejeusne et al., 2010). The concentrations of nutrients in sea-water, especially total inorganic nitrogen in the case of the present study, are also known to have a great impact on the distribution of alien species. In Izmir Bay, for example, dense aggregations of alien species in the inner Bay were mainly explained by high nutrient concentrations (Çinar et al., 2006). Anthropogenic disturbances are known to favor the settlement of alien species by creating empty niches because of the removal of highly competitive native species from the system. It seems that disturbed areas provide golden opportunities to alien invaders to build up dense populations, which were previously explained by the empty-niche and biotic-resistance hypotheses (Byers, 2002; Jeschke, 2014; Çinar et al., 2017). Changes of the species composition of sponge infauna in relation with a nutrient gradient make it a good candidate for assessing the ecological quality status of water bodies in accordance with the requirements of the Water Framework Directive of the EU. In the present study, there are limited data to prove this assumption. Therefore a further study is required to test if sponge infauna can be used for this purpose. Sponges collected in the eco-regions studied here had different species assemblages, mainly due to the occurrence of many alien species on sponges from the Levantine Sea. Abundances of two species, Leonnates indicus and Ophiactis savignyi, contributed much to the dissimilarity of the species assemblages between the ecoregions. The assemblages in the Levantine Sea did not show an east-west pattern, indicating that different factors might have played roles in structuring the assemblage. The species assemblages, however, showed a moderate correlation with a set of environmental variables such as nitrogen, silica and dissolved oxygen. These factors are known to have great impacts on the bottom fauna (Çinar et al., 2006, 2012). In the east Atlantic, current regime and depth played an important role in the structure of species assemblages on the sponge Halichondria panicea (Peattie and Hoare, 1981). Ávila and Ortega-Bastida (2015) found that salinity influenced

Fig. 8. The total number of species and individuals of alien species at stations.

Fig. 9. The mean values of ALEX at stations, with + standart error. Table 6 Spearman's rank correlation coefficients between environmental variables, and community parameters and ALEX. Bold numbers are statistically significant (P < 0.05).

Temperature Salinity Dissolved Oxygen pH Total Nitrogen Phosphate Silica

Number of Species

Number of Individuals

Diversity Index(H′)

Evenness Index (J′)

ALEX

0.04 0.25 0.05

0.28 0.01 0.15

0.31 0.41 0.02

0.40 0.38 0.02

0.60 0.20 0.47

0.28 0.07 0.19 0.06

0.35 0.12 0.12 0.30

0.04 0.25 0.30 0.10

0.20 0.32 0.31 0.09

0.12 0.60 0.41 0.04

10

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the structure of species assemblages on sponges. Beside these factors, amount of detritus accumulated on surface and canals of sponges, and biomass of microorganisms living inside sponges might affect abundances of sponge associated fauna (Klitgaard, 1995; Neves and Omena, 2003). In addition, as sponges have a limited space to live in, intra- and inter-specific interactions might greatly affect the assemblages (Hendler, 1984; Çinar et al., 2002; Abdo, 2007). Sponges are also known to secrete chemicals that attract the settlement of some associated fauna (Frith, 1976; Pawlik, 1983). In addition, toxic components produced by unicellular heterotrophic bacteria associated with sponges inhibit settlement of canals by various species (Magnino et al., 1999).

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