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The Influence of Sewage Pollution on Polychaetes associated with Mussel Beds of the Southern Romanian Black Sea Coast Victor SURUGIU(1) (1) “Alexandru Ioan Cuza” University of Iaşi, Faculty of Biology, Bd. Carol I, 20A, 700507 Iaşi, Romania,

e-mail: [email protected]

Abstract: A study of the response of the polychaete community associated with the rocky mussel beds to a sewage discharge was carried out in the area of Eforie Sud during summer 2005 and summer 2006. Three stations and a control site were randomly sampled around the Eforie Sud effluent. In each station water quality variables were also measured. A total of 15 species were encountered. The most impacted station, situated at the effluent, had the lowest species richness and diversity. Here only Alitta succinea (Frey & Leuckart, 1847) and Polydora websteri Hartman, 1943 were present. These two opportunistic species peaked at the station nearest to the effluent, where low inter-specific competition for food and space and high organic matter input prevailed. The control station, situated 5 km from the effluent, had the highest number of species, diversity and evenness. In this site dominant species were Salvatoria clavata (Claparède, 1863) and Platynereis dumerilii (Audouin & Milne-Edwards, 1833). Uni- and multivariate methods were employed to assess the degree of sewage-induced disturbance on the rocky mussel community. The distribution pattern of the polychaete community was governed especially by pH and dissolved oxygen concentration. Keywords: Polychaeta, mussel beds, sewage pollution, Black Sea, Romanian coast.

Introduction Organic enrichment is probably the most common, and hence the most extensively studied, disturbance on marine environments (Pearson & Rosenberg, 1978). The discharge of domestic waste into the sea leads to a local increase in the quantity of the particulate and dissolved organic matter. This organic matter serves as food for many benthic surface or sub-surface deposit-feeders. If the quantity of domestic waste is large the bottom-dwelling organisms cannot assimilate this increase. As a result of bacterial decomposition of this unassimilated organic matter the concentration of dissolved oxygen diminishes to critical levels. Because oxygen deficiency is the main ecological factor causing severe stress to the macrobenthos, the number of species and the number of individuals will decrease until they disappear altogether. The use of benthic organisms to assess the impact of human-mediated changes is favoured by the fact that they are relatively sedentary: they cannot avoid the pollution in the way that fishes can; they integrate environmental quality

conditions over longer periods of time compared to plankton; they comprise species with different tolerances to stress; and have an important role in the cycling of nutrients and other chemicals at the water-sediment interface (Reish, 1960, 1973; Gray & Pearson, 1982; Bellan, 1991). However, sorting and identifying of all benthic organisms is very laborious and time-consuming. Thus marine ecologists are searching for cost-effective methods to detect the impact of pollution without the necessity of identifying the whole benthic community. Among bottom-dwelling organisms, polychaetes are considered one of the most useful indicators of the quality of the marine environment (Reish, 1960, 1963; Pocklington & Wells, 1992; Elías et al., 2003, 2006; Surugiu, 2005). They have been used successfully as bioassay organisms, as monitors for toxic compounds and as pollution indicators at species, as well at population and community, levels (Pocklington & Wells, 1992). The use of polychaetes in biomonitoring studies is of special value because they are extremely responsive to changes in environmental conditions over time, even over a

GEO-ECO-MARINA 15/2009 Sedimentary Processes and Deposits within River-Sea Systems

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V. Surugiu – The Influence of Sewage Pollution on Polychaetes associated with Mussel Beds of the Southern Romanian Black Sea Coast wide geographic area. The presence or absence, but especially the mass proliferation of certain polychaete species, constitutes a good indicator of the health of benthic habitats. Thus, the species of the family Capitellidae (e.g., Capitella capitata complex) and Spionidae (e.g., Polydora cornuta, Streblospio benedicti, Malacoceros fuliginosus etc.) have been widely accepted as indicators of marine organic pollution (Reish, 1957, 1960, 1963; Grassle & Grassle, 1974; Pérès & Bellan, 1972; Pearson & Rosenberg, 1978; Anger, 1975; Losovskaya, 1977; Rygg, 1985; Tsustsumi, 1990; Tsustsumi et al., 1990; Vallarino et al., 2002). In many studies the establishment of the degree of organic pollution was based on the analysis of polychaete communities (Reish, 1955, 1957; Bellan, 1964, 1980; Cognetti & Talierico, 1969; Cognetti, 1972; Dauer & Conner, 1980; Losovskaya, 1983; Elías et al., 2003). Bellan (1980) even proposed an Annelid Index of Pollution to assess the degree of pollution due to municipal sewage. The Southern Romanian Black Sea coast, situated between Constanta and Mangalia, has high densities of people and industry. As a result, large volumes of polluted water are discharged into the sea in this zone. According to the objectives of the national strategy for the protection of the marine environment, certain actions are required for the preservation of biological diversity and sustainable use of its components. Rehabilitation and protection of the Romanian Black Sea coast and its adjacent marine waters can be achieved only by the reduction of pollution from point sources along the coast and off-shore. The Water Framework Directive (WFD 2000/60/EC) stipulates liabilities to assess biological effects along coastal waters, especially with respect to toxic pollutants. However, studies of the influence of pollution on the benthos in the Romanian littoral zone are very scarce. Ţigănuş (1982) studied the composition and distribution of zoobenthos from softbottom substrates affected by harbour pollution. Later, she analysed the influence of industrial wastewater discharge on benthic populations and strengthened the importance of the knowledge of benthic communities’ status in the assessment of marine pollution (Ţigănuş, 1986, 1997). Thus the aims of this study are: (a) to conduct a detailed analysis of the distribution pattern of polychaetes along an organic pollution gradient, and (b) to investigate the key environmental variables affecting the polychaete community structure.

Material and methods Study area In order to assess the influence of sewage pollution on polychaete populations, the sampling area was located in the vicinity of the Eforie Sud seaside resort, were an outfall pipe of the local wastewater treatment plant is situated (Fig. 1). This treatment plant uses mechanical and biological processes and receives domestic sewage from the Eforie Nord, Eforie Sud, and Techirghiol towns (a total of about 20,000 inhabitants). Annually it discharges an average of 12.062·109 m3 of 78

sewage, including 178.5 tonnes of ammonia, 10.47 tonnes of nitrites, 62 tonnes of nitrates, 997.5 tonnes of suspended materials and 586 tonnes of Biochemical Oxygen Demand loading into the sea (Petran, 1997). The outlet of the drain-pipe, 70 cm in diameter, is situated at the level of the shoreline (44°01‘15.7“N; 28°39‘36.9“E) and discharges approximately 0.25 m3 effluent per second. The substrate around the sewage outfall is rocky, consisting of submerged, almost horizontal, Sarmatian limestone platforms.

Sampling procedure Sampling strategy was of systematic type, having as the final objective the determination of changes in the polychaete community structure in relation to the degree of pollution (i.e., the distance of a station from the outfall). The quantitative sampling was carried out in August 2005, June 2006 and July 2006 at three locations, situated at different distances south of the outfall pipe: one at the effluent outlet (station 1), one 50 m from the sewage outlet (station 2), and one 100 m away (station 3). An additional control site (station C) was also sampled at Agigea, situated approximately 5 km north of the outfall (Fig. 1). In each site 3 replicate samples were taken from 1.5 m depth by removing the mussel epibiosis from an area of 400 cm2 with a knife. In order to minimise the loss of organisms during their transportation ashore, the samples were placed in situ in polyethylene bags. Samples were immediately fixed in 4% formaldehyde (~10% formalin), rinsed in the laboratory with freshwater and then sieved through a 0.5 mm mesh. The retained polychaetes were sorted under the stereomicroscope, identified to the species level and counted. Sorted and identified animals were preserved in 80% ethyl alcohol. Some physical and chemical variables of the water column were also measured at each sampling site. The temperature, pH and dissolved oxygen were measured with a portable CONSORT Model C535 Water Quality Meter. The salinity was determined by titration of chloride with a special Aquamerck® kit and subsequent conversion of chlorinity to salinity by means of Almazov’s formula (Bondar et al., 1973). The concentration of nitrates, nitrites, ammonia and phosphates was determined spectrophotometrically with a Merck RQFlex Plus device, which uses special Reflectoquant® strips.

Data analysis The structure of the polychaete community was analysed in terms of species composition (S), population density (A), dominance (D), frequency (F) and diversity. Density was estimated from the average of the three replicates taken at each station. Dominance was calculated as the percentage of the total abundance of a given polychaete species relative to the total number of polychaetes. The diversity was calculated by the Shannon-Wiener diversity index (H’) on a log 2 base (Shannon & Weaver, 1963). The equitability (J’) was expressed as Pielou’s evenness index (Pielou, 1966). The hierarchical agglomerative clustering (Bray-Curtis similarity coefficient, group-average linking) and the non-metric


V. Surugiu – The Influence of Sewage Pollution on Polychaetes associated with Mussel Beds of the Southern Romanian Black Sea Coast

Fig. 1 Sampling area with the location of sampling sites around sewage effluent of Eforie Sud (44°01’15.7”N; 28°39’36.9”E) Multi-Dimensional Scaling (MDS) were used to investigate faunal similarities among sampling sites (Clarke & Warwick, 1994). Square-root transformation was applied prior to calculating similarities in order to down weight the influence of dominant species.

Spearman’s harmonic rank correlation coefficient (ρW ), as proposed by Clarke & Ainsworth (1993) and implemented within PRIMER’s routine BIO-ENV (Clarke & Gorley, 2001), was used to determine which environmental parameters best correlated with the distribution pattern of the polychaete fauna

The similarity breakdown, as proposed by Clarke & Warwick (1994) and implemented in the SIMPER routine (“similarity percentages”) within the PRIMER program, was used to define indicator species for areas subjected to sewage pollution and those from unpolluted areas, by analysing contributions of each species to the average similarity (S) within groups of sites exposed to different levels of organic enrichment. Discriminating species between unaffected and sewage-polluted sites were defined in the same way, by breaking down the average dissimilarity (δ) between different sites into the separate contributions from each species.

Clustering, ordination, similarity breakdown and the calculation of correlation coefficients were carried out using PRIMER v5.0 software package developed at the Plymouth Marine Laboratory.

Results Environmental variables The values of dissolved oxygen concentration, salinity and pH gradually increased with increasing distance from the effluent outlet (Fig. 2). The highest nutrient concentrations


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V. Surugiu – The Influence of Sewage Pollution on Polychaetes associated with Mussel Beds of the Southern Romanian Black Sea Coast (nitrates, nitrites, ammonia, and phosphates) were recorded at the effluent outlet (station 1), and the lowest values at the control site (Fig. 3). Differences in nutrient levels between station 1 and the other stations were highly significant (p