(Annelida: Polychaeta) on the polluted soft substrate

Cah. Biol. Mar. (2009) 50 : 11-17

Distribution of polychaete species (Annelida: Polychaeta) on the polluted soft substrate of the Golden Horn Estuary (Sea of Marmara), with special emphasis on alien species Melih Ertan ÇINAR1, Hüsamettin BALKIS2, Serhat ALBAYRAK2, Ertan DAGLI1 and Selahattin Ünsal KARHAN2 (1) Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100 Bornova, Izmir, Turkey. E-mail: [email protected] (2) Istanbul University, Faculty of Science, Department of Biology, 34134 Vezneciler, Istanbul, Turkey

Abstract: The present study deals with the polychaete assemblages inhabiting polluted soft substrate of the Golden Horn Estuary (Sea of Marmara) and the importance of alien species in polychaete communities. A total of 15 species belonging to 7 families were determined among the benthic materials collected at 4 stations between the depths 4 and 40 m in December 2005. The materials were composed of species tolerant to pollution. Higher diversity and evenness index values were encountered at stations where dissolved oxygen values were relatively high and total organic carbon values were low. The material included four alien species: Desdemona ornata, Ficopomatus enigmaticus, Polydora cornuta and Streblospio gynobranchiata. The most dominant alien species in the area was P. cornuta, with 4340 individuals per square meter. Alien species comprised 46% of total polychaete populations and their distributions were strongly affected by the abiotic factors such as dissolved oxygen, total organic carbon and depth. Résumé : Distribution d’annélides polychètes (Annelida : Polychaeta) dans un sédiment pollué de l’estuaire de la Corne d’Or (Mer de Marmara), colonisation par des espèces invasives. Le présent travail étudie les assemblages de polychètes habitant les sédiments meubles pollués de l’estuaire de la Corne d’Or (Mer de Marmara) et l’importance des espèces introduites dans les communautés de polychètes. 15 espèces appartenant à 7 familles ont étés récoltées parmi le matériel benthique, à 4 stations situées à des profondeurs de 4 et de 40 m en décembre 2005. Le matériel échantillonné est composé d’espèces tolérantes à la pollution. De plus fortes valeurs de diversité H’ et de régularité J’ ont été calculées aux stations où les valeurs d’oxygène dissoute étaient relativement fortes et les valeurs de carbone organique total étaient basses. Le matériel étudié inclut quatre espèces introduites : Desdemona ornata, Polydora cornuta, Ficopomatus enigmaticus et Streblospio gynobranchiata, la plus abondante dans la région étant P. cornuta, avec 4340 individus par mètre carré. Les espèces introduites représentaient 46% de la communauté totale de polychètes et leurs distributions étaient dépendantes des facteurs abiotiques tels que d’oxygène dissous, le carbone organique total et la profondeur. Keywords: Alien species

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Polychaeta

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Pollution

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Impact

Reçu le 11 avril 2008 ; accepté après révision le 4 décembre 2008. Received 11 April 2008; accepted in revised form 4 December 2008.

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Golden Horn Estuary

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Sea of Marmara

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Turkey

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POLYCHAETES fROM THE GOLDEN HORN

Introduction The biotic introduction is known to be one of the major factors adversely affecting the biodiversity (Elton, 1958; Vitousek, 1992). Increasing trades between countries under the current wave of globalization has triggered the speed of organism exchange between different zoogeographic regions (Levine & D’Antonio, 2003). The opportunistic species that adapt easily to a new environment and increase their population densities in a short time tend to expand their distributional ranges by the transport by shipping. These species are also resistant to unsuitable conditions through the transport (i.e. ballast water) (Carlton, 1985). They prefer estuarine and polluted environments where food is amble and competition is relatively weak. When they become established in a new area and constitute proliferating populations, the food web in the area begins to be restructured. The recent studies (Çinar et al., 2005a & 2006; Dagli & Çinar, 2008) showed how alien spionid species could change the community structure of polluted soft bottom substrate in and near Alsancak Harbour (Aegean Sea, Turkey), where azoic conditions were previously reported. They seem to have replaced pollution indicator (opportunistic) species previously reported to be key components of the ecosystem. The alien species inhabiting the coasts of Turkey were reviewed by Çinar et al. (2005b). According to this study, a total of 14 polychaete species have become established in the region. In recent years, 11 other alien polychaete species were reported by Çinar (2006 & 2007), Çinar & Ergen (2007) and Dagli & Çinar (2008), bringing the total number of established alien polychaetes known from the Turkish coasts to 25. Among these species, only Ficopomatus enigmaticus (fauvel, 1923) and Polydora cornuta Bosc, 1802 were reported to occur in the Sea of Marmara (Demir, 1952-54; Dagli & Ergen, 2008). Although Rullier (1963) reported 11 polychaete species in the Bosphorus Strait with Indo-Pacific affinity, these species were regarded as questionable or excluded by Çinar et al. (2005b) as their taxonomical identities were not properly documented and their occurrences in the Mediterranean have not been subsequently approved by other polychaete experts. Increase in settlements and industrial facilities around the Golden Horn since the 1950s were accompanied with severe pollution, particularly from wastewaters of pharmaceutical, detergent, dye and leather industries and domestic discharges (Yüksek et al., 2005). In addition, dams built on streams considerably blocked freshwater inputs, while the dry docks of shipyards located at the middle part of the estuary and floating bridges at various points inhibited water circulation greatly. In 1999, after the construction of northern and southern sewerage trunk systems, the

pollution in the estuary was diminished. Afterwards, an extensive rehabilitation study was initiated for the estuary. During that study, about 4.5 million m3 mud was dredged and transported to abandoned stone mine areas. Thus, water-depth through the estuary increased approximately 45 m (Gonullu et al., 2006). The aim of this study is to determine native and alien species on the polluted soft substrate of the Golden Horn Estuary (Sea of Marmara), and to assess abiotic factors influencing the distribution of the alien species.

Material and Methods Benthic materials were collected from five stations in Golden Horn Estuary by using a van Veen grab (0.1 m2 sampling area) in December 2005 (fig. 1). Three replicates were collected at each station. Obtained materials were rinsed through a 1 mm mesh sieve and then placed in jars containing 4% formaldehyde solution in seawater. In the laboratory, samples were washed with tap water and sorted according to major systematic groups under a stereomicroscope. The sorted animals were then preserved in 70% ethanol. Polychaete specimens were identified and counted under stereo- and compound microscopes.

Figure 1. Map of the investigated area and percentages of abundance of alien and native species in samples. Figure 1. Carte de la région étudiée et pourcentages d’abondance des espèces introduites et indigènes dans les échantillons.

M.E. ÇINAR, H. BALKIS, S. ALBAYRAK, E. DAGLI, S.Ü. KARHAN

In order to determine the physico-chemical properties of sea water, samples were taken by a 3 litre water sampler just above the bottom. Temperature was measured by a thermometer on the water sampler, salinity by MohrKnudsen method and dissolved oxygen by Winkler method. Small amounts of bottom material were taken off from the surface of sediment. Silt-clay percentage of the sediment was determined by sieve analysis (folk, 1974), while total organic carbon (TOC) by Loring & Rantala (1992) method. The community parameters such as number of species, number of individuals, diversity index H’ (ShannonWiener, log2 base) and evenness index J’ (Pielou) were calculated for each sample. The relationship between the abundance of four alien species and environmental parameters was assessed by using Pearson correlation analysis.

Results Physico-chemical analysis The temperature value was constant at the shallow water stations (stations 1-4, 12ºC) and increased at the deepest station (station 5, 15ºC) (Table 1). Similarly, the salinity values (17.6-19.7) at the shallow water stations were lower than that at the deepest station (35.6). Dissolved oxygen value attained its minimum level at station 5 (2 mg.l-1) and maximum level at station 3 (6.1 mg.l-1). Total organic carbon (TOC) was found to be 26.1 mg.g-1 at station 3 and 51.2 mg.g-1 at station 1. Stations 1 and 2 located in the inner-most part of the Golden Horn Estuary had the highest silt-clay percentage (more than 93.5%). Faunistic analysis The faunistic analysis of benthic samples taken in December 2005 revealed a total of 15 polychaete species and 1817 individuals belonging to 7 families (Table 2). Spionidae accounted for 40% of the total species and 64%

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of the total individuals in the area, followed by Capitellidae (28% of total individuals). Among the species encountered, Desdemona ornata Banse, 1957 is being reported for the first time from the Turkish coasts, and Mysta picta (Quatrefages, 1865), Streblospio shrubsolii (Buchanan, 1890) and Streblospio gynobranchiata Rice & Levin, 1998 from the Sea of Marmara. The most dominant species in the area were Polydora cornuta (44% of total individuals), Heteromastus filiformis (Claparède, 1864) (28%) and Malacoceros fuliginosus (Claparède, 1868) (19%). These species accounted for up to 92% of the total polychaete populations. Polydora cornuta formed a dense population (max. 4340 ind.m-2) at station 2, comprising 80% of total individuals. Heteromastus filiformis and M. fuliginosus dominated stations 3 (max. 2670 ind.m-2) and 4 (1130 ind.m-2), respectively. The species found in and more than 50% of samples were M. fuliginosa (83% of samples), Neanthes succinea (frey & Leuckart, 1847) (58%) and H. filiformis (50%). A total of 5 species were found only in one sample. The community parameters [number of species and individuals, and the values of diversity (H') and evenness indices (J')] for each station are shown in figure 2. All parameters attained their maximum values at station 2 and were always low at stations 1 and 5. No polychaete species was found at station 4. At this station, only one nematode, two oligochaete and one bivalve species were found, with low abundances. The diversity index value ranged from 0 to 1.55 (station 3). The polychaete density ranged from 80 (station 1) to 4890 ind.m-2 (station 2). Among the environmental parameters measured (see Table 1), only oxygen value was positively correlated with the community parameters (for H', r = 0.95, n = 4, P < 0.05), the others were negatively correlated. The correlation value between TOC and H' was -0.83 (n = 4, P < 0.05). The material collected from polluted soft substrate of the Golden Horn Estuary included four alien species: Polydora cornuta, Streblospio gynobranchiata, Desdemona ornata and Ficopomatus enigmaticus. These species accounted for 46% of the polychaete populations in the area. The

Table 1. Depth and physico-chemical characteristics of stations. T: Temperature, DO: Dissolved oxygen, TOC: Total organic carbon. Tableau 1. Profondeur et caractéristiques physico-chimiques des stations échantillonnées. T: Température, DO : Oxygène dissous, TOC : Carbone organique total. Station 1 2 3 4 5

Depth (m)

T (ºC)

Salinity

DO (mg.l-1)

TOC (mg.g-1)

Silt-clay percentage (%)

4 5 6 30 40

12 12 12 15 15

17.6 19.3 19.7 36.2 35.6

3.6 5.3 6,1 2.2 2

51.2 34.1 26.1 45.8 42.7

98.4 93.6 84.1 99.5 86,5

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1959. However, he did not find any polychaete species at two stations located in the inner-most part of the estuary. Among the species he found in the area, STATIONS Capitella capitata (fabricius, 1780) was Species 1 2 3 5 represented by high number of individuals. Ünsal (1988) detected five POLYNOIDAE Harmothoe imbricata (Linnaeus, 1767) 230 polychaete species [Capitella capitata, PHYLLODOCIDAE Malacoceros fuliginosus, Nereis zonata Mysta picta (Quatrefages, 1865) 20 (Malmgren, 1867) Polydora ciliata Phyllodoce mucosa Oersted, 1843 10 (Johnston, 1867) and Exogone naidina NEREIDIDAE (Oersted, 1845) (as E. gemmifera)] in the Neanthes succinea (frey & Leuckart, 1847) 10 160 410 estuary and postulated that these species SPIONIDAE constituted 89% of the total zoobenthic Malacoceros fuliginosus (Claparède, 1868) 60 700 30 1130 populations and 86% of biomass in the Polydora cornuta Bosc, 1802 4340 940 area. Gillet & Ünsal (2000) found 8 Prionospio sp. 10 10 Spio decoratus Bobretzky, 1870 60 polychaete species at 40 m in the area. Streblospio gynobranchiata Rice & Levin, 1998 10 50 The inner part of the Golden Horn Streblospio shrubsolii (Buchanan, 1890) 10 Estuary was previously known to have CAPITELLIDAE heavily polluted sediment with azoic Capitella capitata (fabricius, 1780) 10 conditions and the release of odorous Heteromastus filiformis (Claparède, 1864) 10 2670 10 biogenic sulfurous gases (Kiratli & SABELLIDAE Balkis, 2001; Yüksek et al. 2006). Desdemona ornata Banse, 1957 60 Yüksek et al. (2006) postulated that the SERPULIDAE water quality and biodiversity of the Ficopomatus enigmaticus (fauvel, 1923) 10 Pomatoceros triqueter (Linnaeus, 1767) 10 estuary have gradually recovering after taking proper precautions to reduce pollution sources pouring into the area. In the inner-most part of the estuary, the percentage ratio between the alien and native species highest PO was reported to be 55.35 µM in 1998 and 4 changed according to stations (fig. 1). The alien species decreased to 12.58 µM in 2001. The azoic parts of the area comprised 83% of the total polychaete individuals at station have been gradually defaunated, at least by opportunistic 2, 14% at station 3 and 13% at station 1. The deepest station species (Yüksek et al., 2006). This study shows that the (station 5, 40 m) had no alien species. The main factors bottom water of the estuary has dissolved oxygen influencing the distribution of alien species in the area were concentration ranging from 2 to 6.1 mg.l-1 and that all found to be dissolved oxygen value (positively affected) stations sampled had zoobenthic organisms. and depth (negatively affected). The presence of alien Stressed environments are known to be easily colonized species was also negatively affected by the depth-related by alien species (Zibrowius, 1992; Occhipinti-Ambrogi & parameters such as temperature and salinity. Savini, 2003; Çinar et al., 2006). During the defaunation Eggs were observed in coelomic cavities of specimens process of azoic sediments, opportunistic and alien species of Streblospio gynobranchiata, at the base and inside of the are the pioneering ones (Çinar et al., 2006 & 2008). In the strap-like brooding structures, measuring 68-110 µm in inner part of Izmir Bay, where azoic conditions were diameter. Specimens of Desdemona ornata had eggs in previously reported, the recovery in sediment and water their coelomic cavities, measuring 70-125 µm in diameter. qualities due to the establishment of waste water treatment plant favored the establishment of alien species in the area, Discussion constituting more than 85% of total zoobenthic abundance (Çinar et al., 2006). The same scenario seems to be The benthic samples taken from polluted soft substrate of happened in the Golden Horn Estuary. A total of four alien the Golden Horn Estuary in December 2005 included 15 species, which were not previously reported from the polychaete species. Polychaetes inhabiting the estuary were estuary, suddenly appeared in the area as soon as a recovery previously studied by Rullier (1963), Ünsal (1988) and in sediment and water qualities is observed. These species Gillet & Ünsal (2000). Rullier (1963) reported a total of 11 were Polydora cornuta, Streblospio gynobranchiata, species at two stations in the area collected by Caspers in Desdemona ornata and Ficopomatus enigmaticus. Among Table 2. List of species found and their maximum density (ind.m-2) at stations. Tableau 2. Liste des espèces récoltées et leur densité maximum (ind.m-2) aux différentes stations.


Figure 2. Mean community parameters (number of species, number of individuals, diversity index and evenness index) at stations (± standard error). Figure 2. Paramètres essentiels des communautés (nombre d’espèces, nombre d’individus, index de diversité et index de régularité) aux stations (± erreur standard).

the species, Demir (1952-54) and Dagli & Ergen (2008) previously reported F. enigmaticus and P. cornuta from the Sea of Marmara, respectively. Polydora cornuta formed a dense population at station 2, with 4340 ind.m-2. This species is believed to have been widely transported through the ballast water (Radashevsky & Hsieh, 2000; Çinar et al., 2005a) and occurred in different parts of the world (see Radashevsky, 2005), including the Mediterranean (Tena et al., 1991; Çinar et al., 2005a & 2006), the Sea of Marmara (Dagli & Ergen, 2008) and the Black Sea (Radashevsky, 2005). This species reached a population density of 3170 ind.m-2 in Izmir Bay

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(Aegean Sea) (Çinar et al., 2005a) and a density of 170 ind.m-2 in Izmit Bay (Sea of Marmara) (Dagli & Ergen, 2008). The arrival time of P. cornuta to the estuary is unknown at this stage. However, the polychaete specimens, which were collected from the area in 1985-1986 and identified as Polydora ciliata by Ünsal (1988), should be re-examined. The other spionid alien polychaete in the area is Streblospio gynobranchiata, which was first reported from Izmir Bay in the Mediterranean Sea (Çinar et al., 2005a). This species was reported to have been introduced to the Mediterranean from the south Atlantic coast of the US by ballast water (Çinar et al., 2005a). In the Golden Horn estuary, this species formed a scarce population, with 50 ind.m-2 at station 2. Unlike this, the species occurred more dominantly on the polluted soft substrate of Izmir Bay, reaching a population density of 60480 ind.m-2 in April 2004. The sabellid polychaeta Desdemona ornata, which was originally described from the South Africa by Banse (1957), was first reported from the Elba Island (Italy) in the Mediterranean Sea by Lardicci & Castelli (1986). They found 9 specimens in an estuary, with a salinity ranged between 25 and 30. This species was subsequently reported from the Greek coast (Elefsis Bay, Saronikos Gulf) in the Mediterranean (Panagopoulos & Nicolaidou, 1989). Although D. ornata is known to be an estuarine species (Banse, 1957; Day, 1967; Hartmann-Schröder, 1974), Panagopoulos & Nicolaidou (1989) found it in a heavily polluted marine environment (salinity: 28.2-39.5) and suggested that it preferred estuaries due to high organic matter in the sediment, rather than their low salinity. Therefore, they considered it as a pollution indicator species along the Greek coasts, where it formed a relatively dense population, with a density of 440 ind.m-2. Similarly, Ceberio et al. (1998) reported this species from the estuary and marine harbor environments of the European Atlantic coast (Bay of Biscay) and considered it as an opportunistic species for the region. Rossi (2002) carried out a population study on D. ornata in the Elba Island and found a dense population of it (16666 ind.m-2), with peaks in winter and spring. He also emphasized that chlorophyll a could be an important factor in regulating the abundance of D. ornata, which is generally deposit feeder. The establishment of this southern distributed species in the Mediterranean and eastern Atlantic was thought to be due to the transport by vessels (Lardicci & Castelli, 1986; Ceberio et al., 1998). The present study extends its distributional range to the Sea of Marmara. This species was found only at station 2 (60 ind.m-2), with a salinity value of 19.3. The presence of eggs in coelomic cavity of a specimen in the estuary shows that it has formed a proliferating population there.

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The alien species comprised 46% of total polychaete populations in the Golden Horn Estuary, with a maximum percentage (83%) calculated at station 2. Lee II et al. (2003) reported that the alien species accounted for 90% of total populations in the San francisco Estuary. In Izmir Bay (Aegean Sea), the alien benthic species represented more than 75% of total individuals on polluted soft substrate (Çinar et al., 2006) and 31% of total individuals on the mussel Mytilus galloprovincialis (Çinar et al., 2008). More strikingly, Çinar (2006) studied serpulid tube worms in the northern Levantine Sea and concluded that alien species had more than 95% of total populations in shallow-water benthic habitats. The fate of alien species in the estuary should be monitored and they would probably enlarge their population densities when the recovery in sediment and water qualities increases. Çinar et al (2005a) showed that alien spionid polychaetes competed with the opportunistic species such as Capitella capitata and Malacoceros fuliginosus and were tended to replace them in Izmir Bay. In the Golden Horn Estuary, a similar finding was observed. Ünsal (1988) found a dense population of C. capitata (11791 ind.m-2) in the area in 1985, whereas we found its density in the area as 10 ind.m-2. However, he used a smaller mesh (0.5 mm) for sorting the material than we did (1 mm). Therefore, many specimens of C. capitata might not have been captured during the present study, probably resulting in a big difference in the abundance of C. capitata between the studies. The highest number individuals of M. fuliginosus were found at station 5 where no alien species was found. However, seasonal fluctuations of these species should be investigated as to certain if this assumption can be applied for the whole year. The minimum (station 1) and maximum (station 5) depths in the estuary drastically affected the polychaete communities. The lowest diversity and evenness index values were recorded at these depths. The alien and native species much preferred stations 2 and 3 where the dissolved oxygen concentrations were high and TOC values were low. However, Streblospio gynobranchiata occurred at station 1 where the highest TOC value was determined. The importance of TOC on distribution of benthos was summarized by Hyland et al. (2005). As TOC increases toward the higher end of the scale, the benthos is exposed to increasing amounts of physiological stress from oxygen depletion (due to higher biological oxygen demand, BOD) and related byproducts of the organic decomposition process (ammonia and sulphides) (Hyland et al., 2005). The abundance of Streblospio gynobranchiata was found to be negatively correlated with salinity in Izmir Bay (Çinar et al., 2006). In the present study, it also inhabited stations with low salinity values. Sarkar et al. (2005) studied polychaete distribution in a tropical estuary and found that textural composition of the sediments, together with hydrodynamic and geotechni-

cal properties, seem to have the greatest control to quantify the differences of the polychaete community. They also stated that hypoxic conditions (< 2 mg.l-1 dissolved oxygen) had important effects on benthic communities, leading to diminished populations and depleted trophic groups. In coastal lagoons along the Italian coast, the most important abiotic factors influencing the distribution of polychaetes were reported to be salinity value and chlorophyll a concentration (Gravina et al., 1988). However, some authors (Wilson, 1990; Giangrande et al., 1994) indicated the importance of biotic factors in structuring benthic communities.

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