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Marine Pollution Bulletin 64 (2012) 1861–1873

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Marine Pollution Bulletin

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Spatial distribution of intertidal sandy beach polychaeta along an estuarine and morphodynamic gradient in an eutrophic tropical bay ⇑ E.P. Omena , H.P. Lavrado, R. Paranhos, T.A. Silva

Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Ilha do Fundão, 21941-913 Rio de Janeiro (RJ), Brazil article info abstract

Keywords: The spatial distribution of polychaeta along pollution gradients often reﬂects different degrees of distur- Polychaeta bance. In order to evaluate polychaeta fauna of an organically polluted tropical bay, 20 sandy beaches dis- Sandy beaches tributed in ﬁve areas were sampled. The relationship between community structure, slope, beach index, Estuarine gradient exposure, sediment and water quality parameters were analysed. Multivariate analysis of variance (PER- Tropical bay MANOVA) showed differences among areas and beaches. Scolelepis chilensis dominated at mouth of bay Organic pollution beaches whereas Streblospio gynobranchiata and Capitella capitata complex, at inner beaches. Highest Beach morphodynamics polychaete density was recorded at areas 3 and 5 with the dominance of Saccocirrus sp. and the organic indicator species C. capitata complex and Polydora sp. The most important factors obtained from canonical analysis were sorting, slope, mud and organic matter percentage. Marine biotic index (AMBI) showed that areas 3 and 5 were highly affected by anthropogenic factors, given that a poor polychaeta fauna, dominated by opportunistic species, were found. Polychaete assemblages were affected by eutrophication along an estuarine gradient as well as by morphodynamic condition of the beaches. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction sediment. The AZTI’s marine biotic index (AMBI), largely used in the European coast, is based essentially upon the distribution of Estuaries and shallow bays are among the coastal ecosystems five ecological groups of soft-bottom macrofauna in relation to most threatened by anthropogenic activities, organic and inorganic their sensitivity to an increasing stress gradient (Grall and Glema- pollutants and habitat changes (McLuski and Elliot, 2006). They rec, 1997; Borja et al., 2000). have for long been depositories of effluent from industrial pro- Macrofauna of shallow estuarine bays and lagoons have been cesses and domestic waste or areas of industrial or urban develop- focus of many studies about the effect of anthropogenic impacts ment. Several anthropogenic activities promote organic matter on coastal areas (Carvalho et al., 2005; Ferrando and Mendez, accumulation in bottom sediments, which is believed to play an 2011; Lardicci and Rossi, 1998). However, in estuarine areas, major important role on benthic communities influencing its trophic shifts in the physico-chemical water parameters mask the pollution structure and biomass. Organic enrichment influences community effects on macrobenthic assemblages (Rakocinski et al., 1997). In a composition, reducing diversity by exclusion of low-tolerance spe- typical estuarine gradient, macrofauna density and diversity in- cies and increasing the biomass associated with the dominance of a creases from inner to inlet areas (Lardicci and Rossi, 1998). This few opportunistic species (Pearson and Rosenberg, 1978; Bigot et general pattern can be altered by many anthropogenic factors such al., 2006; Diaz-Castaneda and Harris, 2004; Lardicci et al., 1993). as the discharge of sewage effluents, man-made alterations of the Many studies have been using macrobenthic organisms as bioindi- channel or coast line, fish farms and aquaculture (Ferrando and cators of ecological quality in marine environment (Borja et al., Mendez, 2011; Nalesso et al., 2005). An opposite pattern, with high- 2000; Rosenberg et al., 2004). Macrofauna species are sedentary, er macrofauna density and species richness at the inner estuarine have a relatively long life span, consist of different species that ex- area was also recorded (Cardoso et al., 2012; Carvalho et al., hibit different tolerances to stress, thus they can integrate condi- 2005; Taurusman, 2010). Sheltered habitats and organic rich mud- tions over a period of time rather than reflecting conditions only dy sediments that cover inner areas of these systems might be a at the time of sampling (Dauer, 1983). This property makes them favorable condition to macrofaunal colonization, especially deposit more useful in assessing local effects in monitoring programs than feeding polychaetes (Carvalho et al., 2005). classical approaches such as physico-chemical analyses of Polychaetes are excellent indicators of organic pollution due to their high abundance and sensitivity to different contents of organic matter in sediments. Some species have a strong dominance in ⇑ Corresponding author. Tel.: +55 21 25626306; fax: +55 21 25626302. disturbed environments, caused mainly by urban sewage (Pearson E-mail address: [email protected] (E.P. Omena).

1862 E.P. Omena et al. / Marine Pollution Bulletin 64 (2012) 1861–1873 and Rosenberg, 1978; Hily and Glémarec, 1990; Olsgard and and trace metal contamination of sediments have been evident Somerfield, 2000). The capitellid polychaetes, specially the Capitel- in the last few decades (Carreira et al., 2002; Kjerfve et al., 1997; la capitata ‘‘complex’’, are classified as r-strategists, having the abil- Machado et al., 2008). Concentrations of coprostanol in sediments ity to colonize new habitats quickly (Tsutsumi, 1990). In as high as 40 lgg1 indicate areas of severe sewage contamination undisturbed conditions these r-strategist species are replaced by (Carreira et al., 2004). For more than 20 years, land reclaims on the k-strategist ones which, with rare exception, numerically dominate margins of the bay have been increasing sediment deposition, the community. Also some studies suggest the use of polychaetes bathymetric reduction and alteration of tidal induced currents as a representative taxa in environmental monitoring programs (Amador, 1997). Water quality data show an eutrophic gradient as they closely follows the whole macrofaunal community distri- (e.g., ammonium and phosphate concentrations) in Guanabara bution patterns (Del-Pilar-Ruso et al., 2009; Papageorgiou et al., Bay waters from the eastern area, close to the environmental pro- 2006). tection area of Guapimirim (EPAG) to the western area of the bay, Several recent studies have focused on the impact of human at the estuary of São João de Merití River, by 1–2 orders of magni- activities on community composition and structure of the macrofa- tude. This is due to a greater sewage runoff and less efficient water unal communities at sandy beaches. The influence of freshwater renewal on the western margin than on the eastern one (Kjerfve et effluent was evident on Uruguayan beaches where salinity, cou- al., 1997; Mayr et al., 1989). The greater eutrophication in western pled with slope and beach/swash zone, were the main environ- estuaries is supported also by total coliforms and faecal coliforms mental variables that induced changes in the macrobenthic in sediment (Silva et al., 2008) and by the isotopic composition community (Lercari and Defeo, 2003). A loss of more than two of particulate matter collected in Iguaçu and São João de Merití Riv- thirds of the total species richness after an oil spill was recorded ers which presented sewage-enriched particulate organic matter on Galician sandy beaches, in which polychaetes were among the (Carreira et al., 2002, 2004). most affected taxonomic group (Junoy et al., 2005). A negative rela- According to the hydrological characteristics of Guanabara Bay, tionship between human recreational activities (e.g., trampling) Mayr et al. (1989) suggested a classification into different sections and density of macroinfaunal species was observed on Brazilian in which natural and anthropogenic factors act in distinct man- exposed beaches (Veloso et al., 2006). A lower polychaete diversity ners: area 1: the central channel; area 2: the margins at the mouth and occurrence of some indicator species on a sandy beach could of the bay; area 3: the area around Governador Island; area 4: the be related to the influence of organic enrichment from domestic in- northeastern section, within the Guapimirim environmental pro- put and to salinity variation (Rizzo and Amaral, 2001). tection area (EPAG); and area 5: the western area. Greater inputs Guanabara Bay is a tropical estuarine system that has under- of urban and industrial effluents are recorded at areas 3 and 5. gone intense degradation, mainly due to pollution by untreated domestic sewage (Mayr et al., 1989). The general pattern of macro- 2.2. Field sampling and laboratory procedures benthic species distribution along the bay reflects a negative gradient of diversity and biomass towards the inner parts of the bay and We sampled at 20 sandy beaches (sites) located in different sheltered areas (Lavrado et al., 2000; Van Der Ven et al., 2006; Santi areas of the bay: as indicated in Mayr et al. (1989) (Fig. 1): Paquetá and Tavares, 2009). Three zones can be depicted by analyzing the Island (area 1), mouth of the bay area (area 2), Governador Island polychaeta sublittoral fauna: the mouth-of-the-bay zone with high (area 3), inner bay (area 4) and western area (area 5). Sampling polychaete diversity, the middle-bay zone with low diversity and was undertaken during low neap tides on three occasions: dry sea- high biomass, and the inner-bay zone, a very poor polychaete son (September 2005 and October 2006) and wet season (March assemblage, sometimes azoic (Santi and Tavares, 2009). Similar re- 2006) and consisted of three transects arranged from the low tide sults were found for crustaceans, where the absence of fauna was watermark to the mean high water neap tide mark at each beach. recorded at hypoxic sediments from inner sectors, suggesting In each transect, we collected three replicates in each one of the harmful effects on the local fauna (Van Der Ven et al., 2006). The three different intertidal levels (low, middle and high) using a core depletion of oxygen is one of the effects of the eutrophication im- of 0.2 m2, making a total of 27 samples in each beach. Samples pact, preventing the survival of aerobic organisms (Diaz and were washed in seawater and sieved with 0.5 mm mesh screens Rosenberg, 1995). It has been suggested that hypoxic conditions and the organisms anesthetized with magnesium chloride, fixed combined with slow water renewal in the inner bay seemed to play in 4% formaldehyde, and later preserved in 70% ethanol. For the a key role in the polychaete diversity and biomass (Santi and analyses of granulometry and organic matter concentration, three Tavares, 2009). However, in spite of the intense habitat degrada- samples along each transect were collected. Sediments were pro- tion and the reduced number of species of commercial value, cessed following the methodology described by Suguio (1973) Guanabara Bay still supports an important fishery (Jablonsky et and Wentworth scale was used for grain classification (mm). Or- al., 2006). ganic content of dry sediment was estimated as the loss of weight This study aims to evaluate how polychaeta assemblage is after ashing. The carbonate percentage was calculated by weighing responding to eutrophication along an estuarine gradient and nat- a fraction of the sediment before and after it was treated with chlo- ural factors such as morphodynamic condition in 20 sandy beaches. ridic acid (Suguio, 1973). We used a method proposed by Emery (1961) for estimating 2. Materials and methods slope profile of each transect. The total length of the beach and its distance from the mouth of the bay were also estimated. The beach 2.1. Study area index (BI) (McLachlan and Dorvlo, 2005) was calculated for each beach as a measure of its morphodynamic state, BI = (mean grain Guanabara Bay is an estuary of 384 km2 located in the center of size tide)/slope. The exposure index proposed by McLachlan the metropolitan region of Rio de Janeiro city (22°44’–22°570S and (1980) was used to categorize the beaches in relation to wave 42°330–43°190W). A sub-tropical climate prevails in summer be- energy. tween December and April with 2500 and 1500 mm of rainfall A set of water quality parameters was measured to evaluate respectively. The mean annual air temperature is between 20 possible relationships between polychaete assemblage and their and 25 °C(Nimer, 1989). environment: temperature, salinity, transparency, ammonia, Guanabara Bay receives the discharge from a drainage basin im- nitrite, nitrate, total phosphorus, chlorophyll a, dissolved oxygen pacted by over 7.8 million inhabitants, in which organic pollution and dissolved organic carbon. For water quality parameters a Author's personal copy

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Fig. 1. Location of the 5 areas and 20 beaches studied along Guanabara Bay: Paqueta Island (area 1), mouth of the bay (area 2), Governador Island (area 3), inner area (area 4) and West area (area 5). The classiﬁcation of the different areas followed the hydrological characteristics of Guanabara Bay (Mayr et al., 1989).

different number of sampling sites for each area were considered: by spectrophotometry. Dissolved oxygen was analyzed by Winkler three sites at inner area, two sites at mouth and West area, and one method and dissolved organic carbon was determined by CHN ana- site at Governador and Paquetá Islands. Samples were obtained lyser (Carlo Erba). Standard methods were used to evaluate all from 0.5 mm deep in dry (2005–2006) and wet (2006) seasons, inorganic nutrients (Grasshoff et al., 1999). on the same period of the biological data. Temperature and salinity This paper uses data (water, sediment and biological) collected were evaluated by using salinity meters from YSI (handheld pH as part of a multidisciplinary project entitled ‘‘Environmental and conductivity meter). Water transparency was measured by a Assessment of Guanabara Bay’’ which was coordinated by Petro- Secchi disk. Chlorophyll a were extracted in acetone and analyzed bras Research Center (CENPES). Author's personal copy

1864 E.P. Omena et al. / Marine Pollution Bulletin 64 (2012) 1861–1873 ), exposure index Sorting coefficient Classification (Wentworth) McLachlan and Dorvlo, 2005 Sorting (mm) ofile (1/m), beach index ( Organic matter (%) Silt–clay (%) (mm) Exposure Classification Grain size Beach Index Slope (1/m) Length (m) (km) ) and sediment parameters: mean grain size (mm), percentage of silt–clay, percentage of organic matter and sorting. Paquetá (area 1) 1 Moreninha2 RelógioMouth (area 2) 25.23 Vermelha4 Urca 24.35 Botafogo6 Flamengo 976.4 5.87 Icaraí8 Charitas 2016.59 7.8 Jurujuba 10.8 6.6 7.810 Eva 276.6 1.15 7.4Governador (area 5.8 6.6 3) 11 Bica 6.6 780.6 1357.5 0.95 112.212 4.2 10 Bananal 8.5Inner 10.9 1674.9 1915.8 bay 0.77 (area 16.0 6.9 4) 913 Limão 21.9 337.2 19.814 1.58 Mauá 1.63 Sheltered 1.33 1115 131;8 8.9 Anil 7.916 Remanso 6.317 29.9 São 9 1.34 10 1.46 Sheltered 1494.2 Gabriel 1393.6 918 1.03 Luz (0.15) 30.3 1.33 7.1 31.1 Exposed 169.9 24.7 30.7 10West 10 (area 62.6 2.33 5) (2.54) 1.57 1.2619 (0.42) 2262.4 Catalão 10 2.69 Sheltered Sheltered20 Ramos Sheltered 2.07 1920.3 22.5 0.17 0.43 0.93 (0.29) (0.25) (0.06) 11 79.2 1130.6 148.7 Sheltered Sheltered 19.0 9 169.9 0.27 0.50 (0.06) (0.00) 9 0.00 2.28 0.33 Sheltered (0.00) 0.67 21.4 (0.06) (0.32) 62.6 60.3 1.27 38.6 2.63 (0.15) 599.8 0.00 0.10 (0.00) (0.17) 0.43 0.37 Exposed (0.06) (0.06) 0.00 (0.00) 0.17 2.43 2.18 (0.06) 9 370.8 Sheltered 0.30 1.96 Very (0.00) coarse 1.27 sand 87.5 Sheltered (0.15) 0.00 0.00 675.8 0.30 9 0.30 (0.00) (0.00) (0.00) (0.20) 0.20 (0.10) 7 0.10 59.0 8 0.43 (0.17) Poorly (0.21) 2.61 Very sorted 0.53 coarse 9 (0.06) 0.40 sand 11.0 (0.17) 0.30 0.27 (0.00) Sheltered (0.06) 1.10 (0.20) 2.02 0.00 0.73 0.67 0.33 (0.00) (0.06) (0.06) (0.15) Coarse Poorly Sheltered 0.83 sand 0.43 1.20 sorted (0.06) 7 (0.75) 0.33 Sheltered (0.23) Sheltered 10 Medium Coarse 0.77(038) sand sand Sheltered 0.90 0.90 0.40 (0.17) (0.10) Medium (0.35) sand 0.43 (0.21 9 0.50 0.80 (0.00) (0.10) 0.40 Well (0.00) sorted 11.67 Medium Medium 0.57 (2.17) 0.73 sand sand Sheltered (0.15) (0.23) Moderately 1.01 sorted (0.36) 5.50 Medium Moderately Well (1.47) Sheltered sand 0.90 sorted sorted (0.26) 2.10 20.40 (0.56) 12.60 0.97 (8.60) (3.64) (0.21) 0.73 Sheltered 8.47 (0.12) Moderately Moderately (7.05) sorted 0.30 sorted Medium (0.17) 1.77 sand (0.40) Moderately 1.83 1.33 0.77 Medium sorted (1.19) (0.25) (0.06) sand Very coarse sand 30.10 1.23 1.80 (8.71) (0.32) (0.10) 0.87 (0.15) 1.37 Moderately (0.51) sorted 1.43 Moderately (0.15) sorted 2.50 Moderately Coarse 1.03 (0.36) sorted sand 1.83 (0.12) 0.83 (0.15) (1.27) 1.43 0.73 (0.21) Coarse (0.35) sand Coarse Coarse sand sand 0.43 (0.15) 1.73 Coarse (0.06) sand Poorly sorted 0.90 (0.00) Poorly sorted Coarse sand Poorly Poorly sorted sorted 0.93 (0.15) Coarse Poorly sand sorted Coarse sand Poorly sorted Moderately sorted Moderately sorted Beach Distance McLachlan, 1980 ( Table 1 Environmental characterization of 20 studied beaches of Guanabara Bay: distance from the mouth of the bay (km), total length of the beach (m), slope pr Author's personal copy

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2.3. Data analysis Permutational multivariate analysis of variance (PERMANOVA: Anderson, 2001, 2005) was used to test the null hypothesis of no We considered three spatial scales to describe the variations on differences among assemblages at different spatial scales, accord- sediment properties and polychaete association parameters: areas, ing to a three factors (area, beach, tidal zone) nested design through beaches and tide levels. The design consisted of three factors: areas 9999 permutations of residuals under a reduced model (Anderson (five levels, fixed and crossed), beach (20 levels, random and and ter Brak, 2003). Factors are: area (fixed and crossed with 5 lev- nested in area) and level (three levels fixed and crossed). A els); beach (random and nested in area with 10 levels) and tidal three-factor nested ANOVA, followed by Tukey’s HSD, was per- zone (fixed and crossed with 3 levels). To obtain a balanced design formed with grain size, sorting coefficient percentage of sand, per- between areas, two beaches from each area were random selected. centage of silt clay and percentage of total organic matter. The The same analysis was done to test temporal variation of poly- same analysis was done for community descriptors, such as species chaete assemblages. The experimental design was: time (fixed number, total abundance, diversity (H0) and evenness (J0) of poly- and crossed with three levels), area (fixed and crossed with 5 levels) chaete fauna pooling replicates for each site. Before running the and beach (random and nested with 2 levels). This analysis was analyses, homogeneity of variances was examined using Cochran’s done with samples from low tide level of selected beaches. p C-test. Data were arcsen x or log(x + 1) transformed to homoge- We used the statistical software package CANOCO 4.0 for Win- nize variances. dows (Ter Braak and Smilauer, 1998) to explore with multivariate We applied the AZTI’s marine biotic index (AMBI) from Borja techniques any potential relationship between polychaete species et al. (2000) to estimate the polychaete assemblage disturbance densities and environmental parameters, we performed some level and to establish the ecological status of sandy beaches of Canonical Correspondence Analyses relating species abundance Guanabara Bay. The classification of the identified species into five data (response variables) to environmental factors (explanatory ecological categories was based on the updated list of the AMBI variables). The environmental parameters tested as explanatory software. Species not considered on the list were classified accord- variables in the multivariate analyses were: grain size, slope pro- ing to the literature and to the authors’ knowledge. file, sorting, organic matter, water temperature, salinity, transpar- Non-parametric multivariate techniques were used to compare ency, ammonia, nitrites, nitrates, total phosphorus, chlorophyll a, the abundance of different taxonomic groups present at each site oxygen and organic carbon. The significance of the first three for three sampling times. All multivariate analyses were performed canonical axes was verified by a Monte-Carlo test. using the PRIMER version 6 statistical package (Clarke and Warwick, 2001; Clarke et al., 2006). Similarity matrices were calcu- 3. Results lated through the Bray–Curtis similarity coefficient using transformed abundance data (fourth-root).The graphic representation Most of the Guanabara Bay beaches can be classified as shel- of multivariate patterns of polychaeta assemblages was obtained tered beaches where tidal currents effects are more important than by non-metric multidimensional scaling (nMDS). wave influence. A more gentle slope and a high contribution of fine

Table 2 Results of three-factor nested ANOVA (area, beach, level) based on sediment properties (percentage of sand, percentage of silt–clay, particle size, sorting coefﬁcient, percentage of organic matter) and community structure parameters (species richness, abundance, Shannon diversity and evenness).

Dry/2005 Rainy/2006 Dry/2006 Tukey’s HSD FPFPFP % Mud Area 42.17 *** 50.17 *** 45.45 *** 4>1=2=3=5 Beach 2.46 ** 3.08 *** 1.92 NS Level 22.98 *** 22.19 *** 15.09 *** % OM Area 36.63 *** 47.75 *** 40.01 *** 4>1=2=3=5 Beach 6.20 *** 1.93 NS 2.24 ** Level 15.31 *** 26.13 *** 20.25 *** Diam Area 28.87 *** 31.38 *** 24.81 *** 1>3=4=5>2 Beach 7.56 *** 10.43 *** 5.49 *** Level 0.49 NS 4.92 ** 7.43 ** Sort Area 38.60 *** 66.24 *** 58.36 *** 1 = 4 > 2,3,5 Beach 3.67 *** 3.58 *** 7.55 *** Level 6.90 ** 19.34 *** 18.50 *** S Area 23.45 *** 34.34 *** 4.27 * 1=5=3>2=4 Beach 7.97 *** 7.52 *** 1.91 NS Level 1.00 NS 5.30 NS 2.13 NS N Area 23.67 *** 18.60 *** 12.61 *** 3>1=4=5>2 Beach 6.95 *** 11.00 *** 2.20 ** Level 1.22 NS 5.33 NS 0.87 NS J Area 7.31 *** 7.62 *** 0.94 NS NS Beach 4.98 *** 7.87 *** 3.23 ** Level 0.50 NS 1.56 NS 1.16 NS H Area 13.59 *** 18.82 *** 2.81 NS 1 > 3 = 4 = 5 > 2 Beach 6.90 *** 7.69 *** 3.61 ⁄⁄⁄ Level 0.19 NS 1.29 NS 0.31 NS

Signiﬁcant a posteriori testing results (Tukey’s HSD) were also showed. 1 = Paquetá; 2 = Mouth area; 3 = Governador; 4 = Inner area; 5 = West area; NS = not signiﬁcant; N = 540. * P < 0.01. ** P < 0.001. *** P < 0.0001. Author's personal copy

1866 E.P. Omena et al. / Marine Pollution Bulletin 64 (2012) 1861–1873 sediments were also common at sheltered places. The occurrence A great variation on water quality parameters along areas of the of exposed beaches was limited to the mouth of the bay (Table bay was noticed. Salinity, transparency, nitrate and total phospho- 1). Highest beach indices were obtained for sites located at Inner rus reached the highest values in the mouth of the bay (area 2) and Bay and Governador Island, and the lowest ones were found at the lowest ones at West area (area 5). At area 5 we recorded very the entry of the bay. high ammonia concentration, which was 100 times higher than of In general, the intertidal zones of beaches were mainly com- ones for mouth area. The highest dissolved organic carbon values posed of sands with a high contribution of medium and coarse sand were found at area 5 too. fractions (Table 1). At the entry of the bay there is a considerable A total of 39 taxa of polychaetes were recorded on the beaches amount of medium sand, while coarse and very-coarse sands occur of Guanabara Bay (Table 3). Six species were common to all studied at the inner sector. Paquetá Island beaches (area 1) were classified areas: Saccocirrus sp., Prionospio sp., Polydora sp., Allita succinea, as very-coarse and poorly-sorted sands with low percentage values Laeonereis acuta, C. capitata complex. Inner sites had the greatest of silt–clay and organic-matter (0.2–0.9%). Governador Island bea- number of exclusive species: Streblospio gynobranchiata, Namane- ches (area 3) had two different conditions, a very-coarse-sand reis sp., and Naineris setosa. Otherwise Pisionidens sp. was only ob- beach and a medium-sand one both with low silt–clay and organ- served at the mouth of the bay. ic-matter percentages. Sediments of West beaches (area 5) were There was a great variation of polychaete density among sandy composed of coarse and moderately-sorted sands, with low silt– beaches (Table 4). Higher polychaete densities were found at sites clay and organic-matter content. Inner-bay beaches (area 4) were placed in the middle bay area (West, Governador and Paquetá) in mainly composed of coarse and poorly-sorted sands with great con- comparison to mouth and inner beaches. Governador area had sig- tent of silt–clay and organic matter. Values higher than 30% of silt– nificant higher density than mouth and inner areas (Table 2). clay were recorded at the inner beaches, such as sites 15 and 18. Paquetá Island beaches had the richest polychaete fauna with Also, in comparison with mouth-of-the-bay and island beaches, significantly higher values of species richness and diversity the inner ones had gentle slopes with a maximum value reaching (Fig. 2; Table 2). Otherwise the lowest species richness and diver- 1/170 in site 16, a mangrove-covered tidal flat located at the mouth sity values were obtained for mouth-of-the-bay and inner bay bea- of the Surui River (Fig. 1). Significant differences of sand percent ches. The variation of biological parameters such as abundance, and grain size values were obtained for areas, beaches (nested in species number, diversity and evenness were significant different areas) and levels (Table 2). between areas as well as beaches (nested in areas) (Table 2).

Table 3 Polychaeta species list, the ecological group classiﬁcation (EG) and its occurrence in sandy beaches of ﬁve areas from Guanabara Bay.

Species Family EG Paquetá 1 Mouth 2 Governador 3 Inner 4 West 5

Capitella capitata complex Capitellidae V Notomastus sp. Capitellidae III Spiochaetopterus nonatoi Chaetopteriidae III Timarete sp. Cirratulidae IV Dorvilleidae Dorvilleidae Nematonereis hebes Eunicidae II Diopatra tridentata Eunicidae I Glycera americana Glyceridae II Goniada maculata Goniadidae II Ophiodromus sp. Hesonidae II Gyptis sp. Hesonidae II Maldanidae sp. Maldanidae Allita succinea Nereididae III Laeonereis acuta Nereididae IV Namanereis sp. Nereididae Perinereis sp. Nereididae III Armandia agilis Opheliidae I Scoloplos sp. Orbiniidae I Naineris setosa Orbiniidae I Paraonis sp. Paraonidae II Eteone sp. Phyllodocidae II Pisionidens sp Pisionidae I Poecilochaetus australisa Poecilochaetidae I Polygordius sp. Polygordiidae I Polynoidae spp. Polynoidae Sabellidae Sabellidae Saccocirrus sp. Saccocirridae Serpula sp. Serpulidae Streblospio gynobranchiataa Spionidae III Prionospio sp. Spionidae IV Polydora sp. Spionidae IV Scolelepis chilensisa Spionidae III Spio sp. Spionidae III Spiophanes sp. Spionidae III Syllis sp. Syllidae II Syllis amica Syllidae II Syllis cornuta Syllidae II Odontosyllis fulgurans Syllidae II Exogone sp. Syllidae II

a Species assigned at the present work. Author's personal copy

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Table 4 Density (ind/0.02 m2), species richness (number of taxa), diversity (H0) and eveness (J) of polychaeta fauna from sandy beaches of Guanabara Bay.

Beach Dry season/2005 Rainy season/2006 Dry season/2006 Density Richness Diversity Evenness Density Richness Diversity Evenness Density Richness Diversity Evenness mean (SE) mean (SE) mean (SE) Paquetá 1 18.1 (12.6) 9 1.21 0.55 82.25 (25.3) 8 0.90 0.43 56.2 (39.3) 6 1.51 0.84 2 156.2 (69.2) 15 0.70 0.26 51.3 (8.2) 19 1.79 0.61 29.6 (13.5) 10 0.65 0.28 Mouth 3 83.5 (64.1) 4 0.19 0.14 424.5 (193.7) 7 0.37 0.19 270.6 (259.8) 4 0.14 0.10 4 243.0 (154.9) 7 0.09 0.04 45.8 (26.4) 5 0.31 0.19 13.0 (5.6) 4 1.08 0.78 5 3.6 (0.5) 2 0.17 0.24 2.7 (0.3) 2 0.13 0.19 7.8 (1.7) 4 0.43 0.31 6 6.6 (1.9) 2 0.08 0.12 4.1 (0.6) 3 0.61 0.55 20.9 (20.0) 2 0.14 0.21 7 0 (0) 1 0.00 0.00 1 (0) 2 0.64 0.92 1 (0) 0 0.00 0.00 8 26.4 (7.0) 4 0.72 0.20 15.1 (7.3) 3 0.10 0.09 5.9 (2.2) 2 0.11 0.17 9 18.8 (5.1) 13 1.45 0.56 4.6 (0.8) 3 0.24 0.22 4.6 (1.6) 5 1.11 0.69 10 39.2 (9.6) 4 0.13 0.09 15.9 (4.1) 1 0.00 0 3.3 (0.9) 3 0.68 0.62 Governador 11 1281.8 (550.1) 8 0.39 0.19 2519.9 (837.8) 7 0.03 0.01 1520 (555.2) 6 0.07 0.04 12 80.9 (25.5) 10 1.27 0.55 23 (8.5) 9 1.42 0.68 56.7 (30.5) 12 1.61 0.65 Inner 13 26.5 (8.0) 5 0.34 0.21 37.2 (16.2) 5 0.86 0.53 44.7 (21.8) 5 0.27 0.17 14 29.1 (6.2) 7 0.89 0.46 46.3 (11.1) 7 0.88 0.45 60.9 (25.4) 4 0.90 0.50 15 27.6 (7.3) 5 0.72 0.45 86.8 (23.4) 6 0.45 0.25 3.2 (1.0) 6 0.31 0.23 16 18.1 (12.6) 7 0.91 0.47 70.2 (20.4) 8 0.73 0.35 12.8 (4.4) 5 1.27 0.79 17 33.1 (13.1) 4 0.84 0.61 69.8 (21.7) 8 1.05 0.5 28.9 (8.9) 5 1.54 0.96 18 129.1 (51.4) 6 1.03 0.58 62.8 (35.8) 9 0.98 0.44 3.8 (2.8) 8 1.53 0.74 West 19 67.9 (20.1) 9 1.59 0.72 42.9 (15.6) 5 0.86 0.53 108.5 (37.3) 9 1.01 0.46 20 88.1 (30.0) 7 0.74 0.38 52.6 (12.7) 8 0.64 0.31 25.7 (16.2) 6 0.98 0.55

among beaches (area). Results of pair-wise ‘a posteriori’ comparison test detected a significant difference between mouth-of-the- bay and inner-bay sites, as well as Paquetá and mouth-of-the-bay sites during the rainy season (Tukey’s HSD: P < 0.05). So the null hypothesis that polychaeta fauna occurs independently of water quality and morphodynamic condition of the beaches was rejected. Otherwise, the effect of tidal zone on polychaete assemblages could not be detected, except for an interaction between beaches (area) tide in the dry season of 2006. Temporal distribution of polychaete assemblages was also verified through this analysis (Table 7). Differences among polychaeta assemblages and among different sampling times were detected. Also, a significant interac- Fig. 2. Mean species richness and diversity of polychaeta sandy beach assemblages tion between periods and areas showed that differences among at different areas of Guanabara Bay, RJ. areas could be dependent of sampling time. The most significant differences occurred between dry/05 and rainy/06, as well as between two dry seasons (Tukey’s HSD: P < 0.05). Guanabara Bay beaches can be characterized by the few domi- According to the disturbance classification evaluated by AMBI, nant species with more than 50% of polychaete abundance (Table sandy beaches of Guanabara Bay can be classified as heavily-dis- 5). Saccocirrus sp. and Scolelepis chilensis were the dominant species turbed, moderately-disturbed and slightly-disturbed (Fig. 5). in the mouth of the bay beaches, accounting for more than 90% of Paquetá and mouth-of-the-bay beaches had lower AMBI values total individuals collected. Paquetá beaches were mainly com- than other sites, indicating that most of the sampling stations were posed by Syllis amica and C. capitata complex. Inner beaches were classified as slightly disturbed sites with the predominance of spe- dominated by S. gynobranchiata, C. capitata complex and Polydora cies tolerant to organic matter (EG III). Most of Governador Island, sp. The Governador Island site was densely populated by Saccocir- western area and inner beaches were classified as moderately rus sp. Differences in the community structure along beaches and disturbed sites, with two beaches classified as heavily disturbed, intertidal levels were stressed by the multivariate analysis Ramos (20) in West site and Bananal (12) in Governador Island. (Fig. 3). The results suggested differences at polychaeta assem- Most of these beaches showed a predominance of opportunistic blages among sites, mainly at mouth-of-the-bay and inner bay bea- species (EG IV and V). The mean percentage of organisms not-as- ches placed at opposite sides of n-MDS plot. The species which signed to any ecological group was 27.8% at dry/2005; 18% at mostly contributed to characterizing Paquetá sites (very coarse rainy/06 and 23.5% at dry/2006 seasons. The following species sands) were S. amica and Saccocirrus sp. Medium sand beach at were assigned to one of the five ecological groups: S. gynobranchi- the mouth of bay were characterized by S. chilensis. The species ata (III); S. chilensis (III); Poecilochaetus australis (I). It is important which most contributed to similarities between the coarse-sand to highlight that a very abundant species Saccocirrus sp. which was beaches of Governador Island and the western areas were Saccocir- found at both mouth-of-the-bay and western-area beaches was rus sp., C. capitata complex and Polydora sp. Inner beaches, com- not assigned to any ecological group. posed mainly of coarse sand with mud, were characterized by S. The CCA evidenced significant ecological correlations amongst gynobranchiata and C. capitata complex. polychaete associations and environmental variables. The main The three-factor PERMANOVA evidenced significant differences axis of CCA (axis I) could explain 75.5% the structural variation of among areas of the bay and beaches (area) during three sampling the assemblage (Fig. 4, Table 8). Sorting coefficient, mud percent, times (Table 6). Polychaete associations varied among areas and organic matter and slope contributed significantly to explain the Author's personal copy

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Table 5 Dominant species of polychaete assemblages of sandy beaches of Guanabara Bay, RJ.

Beach Dry/2005 Rainy/2006 Dry/2006 Species dominance % Species dominance % Species dominance % Paquetá (1) 1 C. capitata complex 46 S. amica 56 C. capitata complex 31 2 S. amica 82 S. amica 35 Saccocirrus sp. 84 Mouth (2) 3 Saccocirrus sp. 96 Saccocirrus sp.. 92 Saccocirrus sp. 97 4 Saccocirrus spp. 99 Saccocirrus sp. 93 Saccocirrus sp. 60 5 S.chilensis 96 S.chilensis 97 S.chilensis 90 6 S.chilensis 98 S.chilensis 76 S.chilensis 100 7 Polydora sp. 100 S.chilensis 67 S.chilensis 8 S.chilensis 62 S.chilensis 98 S.chilensis 100 9 C. capitata complex 48 S.chilensis 95 S.chilensis 60 10 S.chilensis 98 S.chilensis 100 S.chilensis 70 Governador (3) 11 Saccocirrus sp. 89 Saccocirrus sp. 100 Saccocirrus spp. 99 12 Saccocirrus sp. 63 C. capitata complex 50 Saccocirrus sp. 42 Inner (4) 13 C. capitata complex 93 S. gynobranchiata 71 S. gynobranchiata 90 14 L. acuta 75 S. gynobranchiata 89 S. gynobranchiata 90 15 C. capitata complex 75 S. gynobranchiata 76 S. gynobranchiata 40 16 S. gynobranchiata 16 S. gynobranchiata 80 Polydora spp. 59 17 C. capitata complex 53 S. gynobranchiata 71 Polydora sp. 32 18 Saccocirrus sp. 59 S. amica 52 Saccocirrus sp. 37 West (5) 19 C. capitata complex 34 S. cornuta 69 S.cornuta 52 20 Saccocirrus sp. 70 C. capitata complex 85 C. capitata complex 17

Table 6 Results of three-way permutational multivariate analysis of variance (Permanova). Data from dry season/2005, wet season/2006, and dry season/2006.

Source df Dry/05 Wet/06 Dry/06 FPFPFP Area 4 1.586 * 3.183 ** 1.481 * Beach (area) 5 4.828 *** 4.435 *** 2.872 *** Level 2 0.905 n.s. 1.362 n.s. 0.879 n.s. Area X level 8 0.891 n.s. 1.519 * 0.623 n.s. Beach (area) X level 10 0.782 n.s. 0.761 n.s. 1.674 *** Residual 60 Total 89

P > 0.05 (n.s.). * P < 0.01. ** P < 0.001. *** P < 0.0001.

Table 7 Results of three-way permutational multivariate analysis of variance (Permanova).

Source df FP Period 2 4.685 ** Area 4 2.121 ** Beach (area) 5 1.835 ** Period area 8 3.169 ** Period beach 10 1.968 ** Residual 60 Total 89

** P < 0.001.

ﬁrst axis (51.1%) (Table 9). Inner beaches were positively corre- lated with sorting and mud content of sediments, and were repre- sented by S. gynobranchiata. Mouth-of-the-bay and Paquetá beaches lies to the left of the main axis, where slope and water transparency were the main environmental factors. Grain size Fig. 3. Non-metric multidimension scaling plot of the samples (n-MDS) based on and chlorophyll a were also important variables and could explain species abundances of Guanabara Bay beaches on dry season/2005 (A) global R = 0.473; rainy season/2006; (B) global R = 0.546 and dry season/2006; (C) global the 24.4% of polychaeta spatial distribution (axis II). As Governador R = 0.498. Island and western-area beach samples lie near the origin, none of Author's personal copy

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Fig. 4. Diagram of axis 1 and 2 obtained from the CCA considering environmental variables, taxa and samples, data from dry/2005, rainy/2006 and dry/2005 seasons. INR = Inner bay rainy; IND1 = inner bay dry 2005; IND2 = inner bay dry 2006; PQR = Paquetá rainy; PQD1 = Paquetá dry 2005; PQD2 = Paquetá dry 2006; ENR = entrance rainy; END1 = entrance dry 2005; END2 = entrance dry 2006; GVR = Governador rainy; GD1 = Governador dry 2005; GVD2 = Governador dry 2006; WSR = West rainy; WD1 = West dry 2005; WSD2 = west dry/2006. (A) sampled areas; (B) biotic variables. the variables tested could discriminate these samples. Spatial column using their feeding palps in high energy conditions, such pattern was more important than temporal pattern on the distri- as found in exposed sandy beaches (Dauer, 1983; Pardo and bution of polychaete communities on these sandy beaches. Amaral, 2004). As well as Scolelepis, saccocirrid polychaetes are common in coarse sediments associated with high-energy beaches 4. Discussion (Brown, 1981). This species occurred at almost all areas of Guana- bara Bay and it was often a dominant species. At microtidal At Guanabara Bay the distribution of sublittoral macrofauna beaches along the Ligurian coast (NW Mediterranean, Italy) Sacco- seems to be primarily affected by hydrodynamic conditions and cirrus papillocercus was the dominant species at swash and surf secondarily by the anthropogenic impact (Santi and Tavares, zones, composed primarily by coarser sands, with an average 2009). A decrease gradient in density and species richness from 118.6 ind m2 (Harriague and Albertelly, 2007). The preference for the inlet to inner area of the bay was found in crustaceans, mollus- inhabiting coarse-sand sites was supported by experimental anal- can and polychaete fauna at Guanabara Bay (Mendes et al., 2007; yses that showed the exclusion of Saccocirrus from sites where the Santi and Tavares, 2009; Van Der Ven et al., 2006). High total or- contribution of fine sediments was above 25% (Lee and Correa, ganic matter and hypoxic conditions explained an azoic area pres- 2004). ent in the middle and inner region of the bay. The present study, Sandy beaches of the inner bay had a great contribution of silt– which evaluates intertidal sandy beach polychaeta, indicates the clay, organic matter and poorly-sorted, coarse grains. This habitat presence of many species at beaches along the central channel, favors tube-dwelling infaunal deposit feeding polychaetes, like C. western and inner areas, some of them with higher density values capitata complex and S. gynobranchiata. This is the first record of than at open beaches. Sheltered conditions of inner bay beaches, S. gynobranchiata on the Brazilian coast that was originally with a gentile profile and fine sands, were favorable to many sed- described in the Gulf of Mexico and on the Florida coast (Rice entary infauna capable to construct mucous galleries or permanent and Levin, 1998). It is regarded as an invader in Mediterranean burrows into the sediment. The macrofauna of sheltered beaches is Sea (Cinar et al., 2005) and Caspian Sea (Taheri et al., 2008), characterized by a higher density and diversity than that of ex- probably brought by ballast water. Streblospio benedicti, a closely- posed ones (Allen and Moore, 1987; Corbisier, 1991; Dexter, related species commonly found in temperate estuaries and wet- 1979, 1992). On the other hand, steep-slope and coarse-sand bea- lands, is able to actively select organic particles and detritus by ches cause an inhospitable swash climate and exclude sensitive sweeping its feeding palps across the sediment surface (Levin species, like many soft body macrofauna. Beach index of inner and Bridges, 1994; Mahon and Dauer, 2005). Significant correla- bay were higher than mouth bay beaches, corroborating the favor- tions between the density of S. gynobranchiata and the percentage able condition to soft bodied macrofauna colonization. A similar of total organic matter was also recorded (Taheri et al., 2008). A pattern was recorded on sandy beaches of a semi-enclosed bay different feeding mode is adopted by C. capitata complex, a typical where the degree of exposure, distance from the mouth of the deposit-feeding detrital consumer, which uses a papillose sac-like bay, beach index, as well as beach length and width significantly proboscis to gather detrital deposits (Levin et al., 1996). Both spe- affected the macrofauna distribution (Cardoso et al., 2012). cies are moderately euryhaline and they are able to survive in low- S. chilensis and Saccocirus sp. were the main species at mouth salinity waters. The salinity decrease along Guanabara Bay can also beaches. The occurrence S. chilensis at exposed sandy beaches be a favorable condition to recruiting this species at the inner along the Rio de Janeiro coastline was also recorded by Rocha beaches. et al. (2009). Observations of the feeding behavior of Scolelepis have Guanabara Bay, as an estuarine system, is subjected to natural shown its ability to catch suspended particles from the water stress associated with tidal variations that create spatial gradients Author's personal copy

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Fig. 5. Disturbance classiﬁcation based on AMBI values estimated by polychaeta fauna of 20 sandy beaches along Guanabara Bay, Rio de Janeiro. Slightly disturbed (1.2–3.3), moderately disturbed (3.3–4.3), heavily disturbed (5.0–5.5).

Table 8 Table 9 Results of canonical correspondence analysis relating granulometric and water Correlation matrix of environmental variables with axis 1, 2 and 3 from CCA. quality parameters with biological variables. Data from dry season/2005, wet season/ 2006 and dry season/2006 seasons. Axis 1 Axis 2 Axis 3

1 2 3 Total P Silt–clay 0.7990 0.1190 0.1446 inertia Grain size 0.1549 0.6791 0.1254 Sorting 0.7290 0.3568 0.1591 Eigen values 0.298 0.142 0.098 0.769 Organic matter 0.7609 0.0915 0.1843 Species–environment 0.965 0.929 0.866 0.589 Beach slope 0.7025 0.0557 0.1586 correlations Transparency (Secchi) 0.5661 0.5392 0.2938 Cumulative percentage variance Temperature 0.5561 0.2123 0.1967 of species data 38.8 57.3 70.0 74.1 Salinity 0.4863 0.3036 0.0938 of species-environment 51.1 75.5 92.3 97.7 Dissolved oxygen 0.2387 0.0059 0.5028 relation Total phosphorous 0.2498 0.0905 0.2661 Sum of all Eigen values 0.769 * Ammonia 0.0078 0.0389 0.4575 Sum of all canonical eigen 0.584 * Nitrates 0.5105 0.4596 0.1690 values Dissolved organic carbon 0.5484 0.0643 0.1564 * Montecarlo test of signiﬁcance of the ﬁrst canonical axes. Chlorophyll a 0.0582 0.4193 0.2289 Author's personal copy

E.P. Omena et al. / Marine Pollution Bulletin 64 (2012) 1861–1873 1871 in key parameters such as temperature, salinity, turbidity, and also of the very low density at this site (<7 individuals), low AMBI val- nutrient concentrations (Mayr et al., 1989). The effect of hypereu- ues were obtained. trophic conditions in the western area of the bay is shown by phy- Different from other studies that used the macrofauna commu- toplankton assemblages, where a larger contribution of the nity to apply marine biotic index, this study found consistent index autotrophic microplankton fraction and higher species numbers results in spite of dealing only with representative polychaeta fau- is found at the entry of the bay when compared to the west area na. As they generally follows community patterns in space and (Villac and Tenembaum, 2010). time, similar results of AMBI values could be possibly obtained if One of the effects of the eutrophication impact is the depletion we had considered the whole macrofauna (Wlodarska-Kowalczuk of oxygen levels, excluding aerobic organisms and the dominance and Kedra, 2007). of anaerobic bacteria populations that support the benthic micro- In the present study, sandy beaches located at Paquetá Island bial foodweb of the bay (Silva et al., 2008). According to Santi have a richer polychaeta fauna than inner and mouth sites. These and Tavares (2009) the hypoxic condition along the inner bay is poorly-sorted sandy beaches often receive clear water brought the main factor that explains the azoic area or impoverishes sublit- from tidal currents. The highest number of microhabitats provided toral polychaete community. Sewage discharge can lead to severe by poorly sorted sands explained the rich meiofaunal polychaeta at community degradation in marine environments, especially when some sandy beaches (Villora-Moreno 1997; Domenico et al., 2009). discharge occurs into relatively shallow and sheltered coastal areas Besides sediment properties, water renewal may have an impor- (López-Gappa et al., 1990; Hunter and Evans, 1995; Elias et al., tant effect on the colonization of many polychaete species rarely 2005). This condition seems not be true at intertidal zone as a high found at other sites of the bay. density was found at inner beaches, suggesting that oxygen deple- The present work makes clear that within estuarine habitats tion was not a limit factor on polychaete distribution. the spatial distribution of intertidal sandy beach macrofauna can- Organic enrichment, which is usually associated with sewage not be explained by a single major factor. The most important fac- discharge, characteristically leads to an increase in the abundance tors were the sorting coefficient, slope and the percentage of mud of certain species, particularly opportunistic polychaetes (Pearson and organic matter. Aspects related to water quality like transpar- and Rosenberg, 1978). Polychaete assemblages can change accord- ency, salinity and eutrophication also had an effect on faunal dis- ing to treatment level and flow rates of sewage discharge. Stations tribution. Western area and Governador Island sites were highly with effluent input had a significantly lower family richness and affected by anthropogenic disturbance, given that poor polychaeta diversity than those stations not affected by the discharge. fauna, dominated by opportunistic species, were found. The re- Otherwise an increase of opportunistic families like Capitellidae, sults of the present study showed that the current ecological clas- Spionidae and Dorvilleidae was recorded around impacted areas sification of Saccocirrus sp. needs a revision. The high density of (Del-Pilar-Ruso et al., 2009). Some of this opportunistic species this species in organic polluted areas suggested that it should be are able to continuously colonize the newly-available sediment, classified as an indicator species of Group III (Grall and Glemarec, adopting reproductive strategies with flexible life histories. The 1997).The concept of ecological quality status and the assessment highest density of polychaete fauna at Guanabara Bay was of biological quality of water masses in estuarine (transitional) recorded at heavily disturbed beaches, where C. capitata complex, waters have been focus of discussion (Dauvin, 2007). As estuaries Saccocirrus sp., S. gynobranchiata and S. amica dominate. C. capitata are physically disturbed, particularly in zones with variable salin- complex and S. benedicti are referred as true poecilogenous species, ity levels, it is difficult to discriminate natural and anthropogenic with both lecithotrophic and planktotrophic individuals (Levin effects. In the present work, where a set of parameters were used et al., 1991). The ability to change the reproductive pattern can with a multimetric approach, it was possible to evaluate the appli- be an advantage in stress and unstable environments (Levin cability of water quality indices, such as AMBI, in an estuarine et al., 1991; Mendez, 2002). condition. The effect of organic pollution in the distribution of annelid assemblages was detected in a Mexican coastal lagoon with differ- Acknowledgements ent sources of disturbances caused by anthropogenic activities (Ferrando and Mendez, 2011). An area located close to a fish pro- The authors are grateful to all participants of ‘‘Environmental cessing factory classified as a disturbed zone due to its high organic Assessment of Guanabara Bay’’ project for their assistance during content (12.9%) was dominated by Ophryotrocha puerilis, Nereis field work and laboratory processing samples. We also wish to procera, S. benedicti and Capitella sp., species well-known for their thank to Dr. Cinthya Simone Gomes Santos (Universidade Federal occurrence in eutrophic habitats (Ferrando and Mendez, 2011). Fluminense) and Dr. Vasily Radashesky (Institute of Marine Biol- The dominance of the pollution indicator polychaetes Boccardia ogy, Russian Academy of Science) for their help with taxonomy polybranchia and C. capitata at sandy beaches with high values of of polychaetes. We acknowledge an anonymous reviewer for valu- ammonium, phosphates and organic matter was recorded at Bahía able comments and suggestions on the first version of this paper. Nueva (Patagonia, Argentina) (Ferrando et al., 2010). Thanks are also given to Mike Kepp for revised the English text. The marine biotic index (AMBI) values were consistent with previous data about the water quality of Guanabara Bay (Mayr et References al., 1989), in spite of a great number of individuals without assign- ment to an ecological classification. However, if we use the ecolog- Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of ical classification assigned to Saccocirrus sp. (sensitive to pollution, variance. Austral Ecology 26, 32–46. Anderson, M.J., 2005. PERMANOVA: a FORTRAN Computer Program for EG I) we get some inconsistent results. So we excluded this species Permutational Multivariate Analysis of Variance. Department of Statistics, from our evaluation. 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