Impact of cage farming of cobia (Rachycentron canadum) on the benthic macrofauna in a tropical region

Aquaculture 512 (2019) 734314

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Impact of cage farming of cobia (Rachycentron canadum) on the benthic macrofauna in a tropical region

T

Larissa S. Limaa, Taciana K. Pintob, Bárbara de C.S. Brandãoa, Washington Santosb, Santiago Hamiltona, Ernesto C. Dominguesa,c, Ana P. Kleind, Carlos A. Schettinic, ⁎ Luis H. Poerschd, Ronaldo O. Cavallia,d, Laboratório de Piscicultura Marinha, Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco – UFRPE, Recife, PE, Brazil Laboratório de Ecologia Bentônica, Unidade de Ensino Penedo, Campus Arapiraca, Universidade Federal de Alagoas – UFAL, Penedo, AL, Brazil c Laboratório de Hidrodinâmica Costeira, Departamento de Oceanografia, Universidade Federal de Pernambuco – UFPE, Recife, PE, Brazil d Estação Marinha de Aquacultura, Instituto de Oceanografia, Universidade Federal do Rio Grande –FURG, Rio Grande, RS, Brazil a

b

A R T I C LE I N FO

A B S T R A C T

Keywords: Organic enrichment Marine fish farming Cage aquaculture Environmental impact Polychaeta Hydrodynamics

This study assessed the environmental impact of the cage culture of cobia (Rachycentron canadum) off the coast of Recife, northeastern Brazil. Fifteen thousand juveniles were reared in four 1200 m3 floating cages for 9 months and fed with a 42% protein commercial feed. Sampling campaigns were held at the beginning, during and after harvest (February, August and December of 2011, respectively). Seven sampling stations were established transverse to the coastline, and a control was placed 200 m to the southeast of the cages. Local hydrodynamics had an important role in dispersing the farming residues, which favored dispersion northeastwards. The area of direct impact of settling particles was estimated to be from 10 to 129 m from the cages. A significantly higher concentration of total nitrogen in the intermediate and final sampling campaigns and lower dissolved oxygen levels in the final sampling were observed. Significant changes in the structure of the macrobenthic community (decreased diversity and evenness parallel to an increase in density) reinforce that a process of organic enrichment took place in the area surrounding the fish farm. These changes, however, occurred only in a temporal, not spatial, fashion and were likely due to the organic enrichment of sediment by wastes from fish farming.

1. Introduction The rapid expansion of cage fish farming has amplified the need to consider the possible environmental impacts of this activity. One of the most commonly reported impacts is the release of organic matter and dissolved nutrients (Dean et al., 2007; Sanz-Lazaro and Marin, 2011). In intensive aquaculture systems, it is estimated that only 25% of the nutrients in feeds are incorporated by fish. The rest remains in the environment, with the largest amount ending up in the sediment (Holmer et al., 2013; Morata et al., 2015). The increased availability of nutrients usually boosts primary production, increases turbidity and may eventually cause the death and decomposition of the algal biomass, which in turn, may lead to decreased concentrations of dissolved oxygen (La Rosa et al., 2002). Given that most of the residues end up deposited around and below the cages, the impact of cage fish farming is frequently more noticeable in the sediment than in the water column (Vita and Marin, 2007; Yucel-Gier et al., 2007). For this reason, the

structure of the benthic community has been widely used as a tool to assess environmental impacts of aquaculture (Karakassis and Hatziyanni, 2000; Vita and Marin, 2007). To ensure the sustainability of cage fish farming, there is a need to assess possible environmental imbalances caused by this activity and, based on that, find ways to minimize impacts. Most of the currently available data on the environmental impacts of marine fish farming is derived from studies in temperate regions (Chen et al., 1999; La Rosa et al., 2002; Apostolaki et al., 2007; Dean et al., 2007; Sutherland et al., 2007; Yucel-Gier et al., 2007; Borja et al., 2009; Fernandez-Gonzalez and Sanchez-Jerez, 2011; Martinez-Garcia et al., 2013; Morata et al., 2015). This study, therefore, assessed the impact of the cage farming of cobia (Rachycentron canadum) on water quality variables and the structure of benthic macrobiota of a tropical area off the northeastern Brazilian coast.

⁎ Corresponding author at: Federal University of Rio Grande – FURG, Institute of Oceanography, Marine Aquaculture Station, Rua do Hotel, 2, Querência, Cassino, 96210-030 Rio Grande, RS, Brazil. E-mail addresses: [email protected], [email protected] (R.O. Cavalli).

https://doi.org/10.1016/j.aquaculture.2019.734314 Received 11 May 2018; Received in revised form 18 June 2019; Accepted 16 July 2019 Available online 17 July 2019 0044-8486/ © 2019 Elsevier B.V. All rights reserved.

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column and 1 h intervals. Currents were statistically treated as depth averaged, and the 50 and 90 percentiles were calculated for 15° sectors of directions. These values were crossed with settling velocity of feed pellets and feces to estimate the area of direct impact. Due to the lack of knowledge about the settling velocity of cobia feces, the values estimated by Magill et al. (2006) for gilthead bream (Sparus aurata) and sea bass (Dicentrarchus labrax) were used. Three sediment samples were collected at each station with the same corer type and sediment depth used for the determination of particle size and carbonate content. The samples were fixed in 4% buffered formaldehyde, stained with Rose Bengal and washed in a 300 μm geological sieve. The retained material was fixed in 70% alcohol for further screening and quantification. The animals were identified to the lowest possible taxonomic level, with Polychaeta identified to the family level (Brusca and Brusca, 2003; Ruppert et al., 2003). Univariate and multivariate analysis of the abundance and density of Polychaeta were applied to assess changes in community descriptors in relation to cobia farming. Margalef's richness index (d), Simpson's index of diversity (1-D) and Pielou's evenness index (J') were estimated. Unprocessed data were compared using Kruskal-Wallis' nonparametric analysis of variance (ANOVA) and Tukey's test for a posteriori comparison. The pattern of distribution of samples from different sampling times and places was described with multidimensional scaling (MDS) based on the abundance of all families of Polychaeta. The analysis of similarities (ANOSIM) was applied to compare the structure of the Polychaeta community in different sampling times and distances from the cages. BIO-ENV analysis was used to identify the group of abiotic parameters that were most closely related to the structure of the Polychaeta, whereas REPORT analysis was used to identify whether this correlation was significant. For multivariate analyses, a similarity matrix using the similarity index of Bray-Curtis was constructed for the unprocessed data. Principal component analysis (PCA) and KruskalWallis nonparametric ANOVA followed by Tukey's test were used to compare the environmental parameters and to assess possible trends in different sampling times. These analyzes were performed with the statistical software Primer v.6.1.6, SigmaPlot 11.0 and Statistica 7.0.

Fig. 1. Location of the eight sampling stations (red circles) in relation to a cobia (Rachycentron canadum) farm containing four round cages deployed off the coast of Recife, northeastern Brazil. Note the control station located 200 m southeast of the farm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

2. Material and methods Cobia (Rachycentron canadum) were reared in four 1200 m3 floating cages deployed at a 24 m deep area (08°09′07,14”S; 034°48′41,52”W) approximately 10 km from the coastline of Recife, state of Pernambuco, northeastern Brazil. The area is typically oligotrophic and covered with biogenic carbonate sediments (gravel) and sand. Fifteen thousand cobia juveniles (mean weight of around 150 g) were stocked at a density of 3.0 fish m−3 and reared for 9 months (from December 2010 to September 2011). Sampling campaigns were performed at the beginning (Initial sample; February 2011), during (Intermediary sample; August 2011) and after harvest (Final sample; December 2011). Fish were fed two daily meals of a commercial slow-sinking feed containing 42% crude protein and 8% total lipids. This was the first production cycle carried out on this site. Eight sampling stations were established (Fig. 1) according to Chen et al. (1999): one below the cages (0), three stations at 30, 80 and 100 m from the cages towards the open ocean (stations E), three stations with the same distance but towards the coast (stations W) and one station (control) 200 m southeast of the cages. A single sediment sample was collected at each station for the determination of particle size and carbonate content using a 10 cm internal diameter PVC corer, which was inserted 20 cm into the sediment. About 100 g of the sediment samples were previously dried to constant weight in an oven at 80 °C and sieved in 2000, 1000, 500, 250, 125 and 63 μm meshes. The fractions retained in each sieve were weighed and the sediment was classified according to Wentworth (1922). The content of calcium carbonate was obtained by the method of Gross (1971). The carbon content in the sediment was measured at all sampling times, with one sample per station. Water samples were taken at a depth of 20 m (4 m above seabed) for each sampling station. Temperature (°C), salinity and the concentration of dissolved oxygen (DO; mg L−1) were measured with a multi-parameter probe (Yellow Spring Instruments, USA). The concentrations of total nitrogen (TN; mg L−1) were determined with a WTW Photo Lab S6 multi-analyzer, while chlorophyll a (μg L−1) was estimated by fluorimetry (Welschmeyer, 1994). As the peak current intensity in this area is known to occur between August and October (Schettini et al., 2017), current speed and direction were measured with an acoustic Doppler current profiler – ADCP (Nortek, Norway) from June 2 to October 19, 2011. The currents were measured with 1.0 m of resolution of water

3. Results Sand was the predominant fraction (> 60% of the grains) in all sediment samples (Table 1). The sum of silt and clay represented only 0.1% to 0.7% of the sediment samples. The sediment was, therefore, classified as sandy-gravel. The content of calcium carbonate ranged from 50.7% to 71.4%. There was little spatial variation in water quality as most of the variables presented no significant differences among sampling stations (Table 2). The only exception was the concentration of TN, which was higher at the station 30 m east of the fish farm (Station E30). Fig. 2A and B present the results of water temperature, salinity, DO, TN and the content of carbon in the sediment as well as chlorophyll a at the initial, intermediate and final sampling campaigns, respectively. With the exception of the content of carbon in the sediment, all variables presented significant differences among sampling times. Throughout the study period, the mean salinity varied from 34.9 to 37.1, while water temperature ranged from 26.1 to 29.1 °C (Fig. 2A). The lowest temperature levels were recorded at the intermediate sampling campaign. The DO remained above 5.00 mg L−1 (from 5.18 to 7.77 mg L−1) at all sampling times, with the lowest DO levels being observed at the final sampling campaign. The carbon content in the sediment varied between 9.07 and 10.69% and was not significantly different either among sampling stations (Table 2) or among sampling times (Fig. 2A). The concentration of TN in the water was highly variable (from 1.54 to 14.00 mg L−1). The lowest concentrations of TN (1.54–3.08 mg L−1) were found at the initial sampling campaign, and were significantly lower than in the intermediate and final samplings 2

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Table 1 Sieve (%) and concentration of calcium carbonate (%) in the sediment of the stations sampled around the cages for cobia (Rachycentron canadum) farming off the coast of Recife, northeastern Brazil. Sampling stations

Gravel (2–8 mm) Very coarse sand (1–2 mm) Coarse sand (0.5–1.0 mm) Medium sand (0.25–0.5 mm) Fine sand (0.125–0.25 mm) Very fine sand (0.062–0.125 mm) Silt + Clay Calcium carbonate

200

E100

E80

E30

0

W30

W80

W100

38.8 22.1 17.6 14.3 5.6 0.8 0.7 62.7

26.2 26.5 19.1 18.5 9.0 0.6 0.2 50.7

19.1 37.3 21.9 14.3 6.6 0.6 0.2 71.4

15.3 30.3 24.0 21.2 8.7 0.5 0.1 65.7

25.1 28.1 23.9 16.0 6.2 0.6 0.1 51.5

29.4 28.2 24.7 13.6 3.6 0.2 0.1 58.0

26.8 34.7 16.7 12.9 8.0 0.6 0.3 63.0

27.3 24.9 18.8 16.7 10.8 1.2 0.3 60.4

(4–14 mg L−1 and 2–12 mg L−1, respectively). The concentration of chlorophyll a varied between 0.01 and 0.25 μg L−1, with the lowest values being recorded in the final sampling campaign (Fig. 2B). In general, significant differences in the environmental variables were detected between the initial sampling campaign and the intermediate and final samplings. PCA detected that the first two axes were responsible for 70.5% of the total variance of these parameters between samplings. Axis 1 explained 44.3%, while axis 2 explained 26.2% (Fig. 3). The concentrations of TN (0.442) and salinity (−0.418) were the variables with the highest weight in axis 1, indicating an inversely proportional relation, i.e. as salinity increased TN decreased and vice versa. The variables with the highest weight in axis 2 were temperature (0.577), DO (−0.517), chlorophyll a concentration (−0.503) and carbon content in the sediment (−0.189). Temperature was inversely proportional to the other variables. The plot factors in relation to axis 2 show a clear differentiation between the initial sampling campaign and the intermediate and final samplings (Fig. 3). The average current speed was estimated at 0.26 m s−1. During June and July, the maximum current speed of 0.78 m s−1 was recorded, but the average was 0.40 m s−1 (Fig. 4). The directions of the currents in June and July were predominantly north and northeast (Fig. 4). In August, current speed gradually decreased (maximum of 0.40 m s−1) and the direction changed to southeast. During September and October, current speeds remained at the same level as in the previous month, but the direction was predominantly southwest. An increase in current speed (up to 0.60 m s−1) was observed at the end of October. The horizontal particle displacement for feed pellets and feces estimated for the fish farm area is presented in Table 3. The area of direct impact of settling particles was estimated to be in the range 10–129 m below the cages. The dispersion of particles occurred mainly northeastwards. A total of 54 macrofauna taxa were identified. Polychaeta dominated all sampling campaigns, with > 45% of the total sampled animals. Thirty families of Polychaeta were identified. The most abundant was Syllidae (58.2%), followed by Dorvilleidae (6.5%), Phylodocidae (3.9%), Paraonidae (3.5%), Goniadidae (3.2%), Hesionidae (5.0%), Pisionidae (2.5%), Eunicidae (2.4%) and Nereididae (2.1%). In relation

to the sampling stations, the density of the families presented variability, but the two-way crossed ANOSIM (season and sampling campaigns as factors) indicated that the variability was not significant between the stations (Rglobal 0.004 eps = 0.46). The sampling stations were, thus, considered as replicates in time. The mean density of the main Polychaeta families at the initial sampling ranged from 127 to 28,025 individuals m−2 (ind m−2); and the highest density was found for the Syllidae, followed by Dorvilleidae (6369 ind m−2), Paraonidae (4968 ind m−2), Eunicidae and Phylodocidae (3949 ind m−2), Pisionidae (3567 ind m−2), Goniadidae (3057 ind m−2), and Hesionidae and Nereididae (2929 ind m−2). In the intermediate and final sampling campaigns, mean densities varied between 127 and 109,299 ind m−2, and 127 and 122,166 ind m−2, respectively. Again, Syllidae was dominant, presenting a four-fold increase in mean density at the intermediate sampling campaign in relation to the initial one. Density remained high in the final sampling campaign. Although richness was not significantly different between sampling campaigns (Fig. 5A), density increased over time (Fig. 5B) and was significantly higher in the intermediate and final sampling campaigns compared to the initial one. The indices of diversity (Fig. 5C) and evenness (Fig. 5D) decreased over time, being significantly lower in the intermediate and final sampling campaigns in relation to the initial one. A tendency of separation between the initial sampling and the intermediate and final sampling campaigns was detected by the multidimensional scaling analysis (MDS) (Fig. 6). The analysis of similarities (one-way ANOSIM) found significant differences between the initial and intermediate sampling and the initial and final sampling (R = 0.264 and p = .001, R = 0.433 and p = .001, respectively). The highest correlation between structure of the community of Polychaeta was 0.250 for the combination of temperature, DO, TN and carbon content in the sediment, and this correlation was significant (BIO-ENV analysis; R = 126; p = .002).

4. Discussion In the present study, significant changes in the descriptors of the structure of the macrobenthic community indicate the occurrence of

Table 2 Mean values ( ± SD) of water temperature (°C), salinity, dissolved oxygen (DO; mg L−1), total nitrogen (TN; mg L−1) and carbon content (C; %) in the sediment, and chlorophyll a (μg L−1) in the different sampling stations in the vicinity of cobia (Rachycentron canadum) rearing cages off the coast of Recife, northeastern Brazil. Sampling station

Temperature

Salinity

200 E100 E80 E30 0 W30 W80 W100

27.6 27.6 27.7 27.6 27.6 27.6 27.6 27.6

36.6 36.5 36.6 36.4 35.9 36.4 36.3 36.6

± ± ± ± ± ± ± ±

1.3 1.3 1.4 1.3 1.3 1.4 1.4 1.3

± ± ± ± ± ± ± ±

DO 0.4 0.2 0.5 0.7 0.9 0.6 0.5 0.4

6.63 6.60 6.59 5.59 6.40 6.43 6.58 6.56

TN ± ± ± ± ± ± ± ±

3

1.32 1.15 1.12 0.53 0.95 0.94 1.06 1.01

5.55 5.36 4.99 9.37 7.75 6.08 5.51 4.84

± ± ± ± ± ± ± ±

3.91 3.19 2.67 6.37 5.00 3.33 6.49 2.83

C

Chlorophyll α

10.2 ± 0.6 9.8 ± 0.2 9.8 ± 0.2 9.6 ± 0.4 9.6 ± 0.2 10.1 ± 0.5 10.1 ± 0.2 9.5 ± 0.7

0.11 0.11 0.14 0.07 0.08 0.13 0.16 0.11

± ± ± ± ± ± ± ±

0.10 0.12 0.10 0.05 0.06 0.03 0.10 0.08

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organic enrichment over time in the area surrounding the fish farm. The significantly higher concentration of TN in the intermediate and final sampling campaigns and the lower DO levels in the final sampling reinforce the notion that a process of organic enrichment did take place. The results of the principal components analysis (PCA) indicated that the pattern of separation of the sampling campaigns was related to the increase in the concentration of TN and the decrease of DO levels in the intermediate and final samplings. Organic enrichment in the water column and/or in the sediment is the most commonly reported environmental impact at fish farming sites (Sarà, 2007a; Borja et al., 2009; Fernandez-Gonzalez and SanchezJerez, 2011; Holmer et al., 2013; Morata et al., 2015). Fish farm effluents are predominantly made up of dissolved and particulate nutrients derived from fish excretion, defecation and uneaten feed (Holmer et al., 2013). The accumulation of organic matter in the sediment may increase microbial activity, and lead to an increased demand for oxygen and, eventually, to high levels of toxic compounds such as sulfides and methane (Sanz-Lázaro and Marín, 2011). However, the impact that nutrient and organic matter loadings may have on the environment depends on farm characteristics (number and size of cages, fish species, standing biomass, and feed quality and management), the type of ecosystem and environmental features (hydrodynamics – currents and waves, sediment type and depth) (García-Sanz et al., 2011). In the present study, the families of Polychaeta underwent significant changes in the different descriptors of the community structure over time. A significant decrease in the indices of diversity and evenness occurred parallel to an increase in density. These results are similar to those reviewed by Giangrande et al. (2005). These authors stated that stress effects on benthic organisms include increased production, especially linked to eutrophication; a decrease in the number of species accompanied by an increase in the number of individuals; reduction in diversity and increase in the dominance of opportunistic species, i.e. those capable of proliferating after an increase in organic matter (Pearson and Rosenberg, 1978). Changes in species composition at impacted sites were observed in a study on the effects of sewage discharges on the Polychaeta biodiversity in the Mediterranean Sea (Terlizzi et al., 2002). There was a decrease in the number of species with very few abundant and often exclusive species. This is a characteristic of Polychaeta located in unconstrained substrate sites under disturbance. The degree of tolerance to pollution varies among Polychaeta. Some species decrease in abundance (“sensitive”), while others benefit from

Fig. 2. Mean values ( ± SE) of water temperature (°C), salinity, dissolved oxygen (DO; mg L−1), total nitrogen (TN; mg L−1) and carbon content (C; %) in the sediment (A) and chlorophyll a (B; μg L−1) at the initial, intermediate and final samplings from a cobia (Rachycentron canadum) farm off the coast of Recife, northeastern Brazil. Different letters represent significant differences between sampling campaigns (p < .05).

Fig. 3. Principal component analysis (PCA) applied to the water quality variables (temperature, T; salinity; dissolved oxygen, DO; total nitrogen, TN; and Chlorophyll a, Chlo) and the carbon content in the sediment (C) at the initial, intermediate and final sampling campaigns from a cobia (Rachycentron canadum) farm off the coast of Recife, northeastern Brazil.

4

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Fig. 4. Time series of current speed (m s−1) and direction (degrees) in the area surrounding a cobia (Rachycentron canadum) farm off the coast of Recife, northeastern Brazil, from June to October 2011.

waste and uneaten feed over a broader area around the cages. The area immediately below the cages is subject to the settling of particles formed by fragments of feed pellets and feces. Both kinds of particles are formed basically by organic matter, and sink quickly with variable velocities (Rapp et al., 2007). The settling velocity of feces and feed pellets estimated by Magill et al. (2006) varied around 0.5 cm s−1 and up to 10 cm s−1, respectively. Considering a depth of 24 m, the travel time for feces and feed pellets to reach the bottom would be 8.3 and 4.2 min, respectively. During this period the particles will be under the action of the currents and be carried away from the farm site. To calculate the area of direct influence, the value of the median velocity and the 90% percentile velocity were determined for sectors of 15°, starting at the north. For each sector, the horizontal displacement was calculated by the product between the velocity and the vertical travel time. The flow is mostly orientated parallel to the shore, and the maximum displacement also presents this pattern. Also, the northwards currents are swifter than the southwards and, consequently, the displacement northwards is larger. These values seem quite small and would indicate a high accumulation rate under the cages. However, particles of high organic content have a short life as they are consumed by benthic fauna and disintegrated by wave action, which facilitates their removal (Schettini et al., 2006). The period monitored showed the predominance of northwards currents (> 75%), and this should be the predominant direction of the dispersal of the residues. However, during summertime the currents are mainly southwards (Schettini et al., 2017). This means that the dispersal may follow a seasonal pattern, following the current regime. Another possible explanation for the lack of significant differences between sampling stations may be the poor sensitivity of the macrofauna analyses as these were performed at the family level. The use of higher taxonomic levels in studies that use benthic organisms as indicators of impact in marine environments have been thoroughly investigated (Warwick, 1988; Olsgard et al., 1998; Olsgard and Somerfield, 2000). Even higher levels of species, such as family, order and even phylum, may reflect the effects of anthropogenic environmental disturbances (Bevilacqua et al., 2009). Thus, long and imprecise taxonomic identifications that cost time and money should be avoided (Olsgard and Somerfield, 2000). Sometimes, differences in the structure of the benthic community between impacted and control sites may be less evident when using a lower level of taxonomic resolution

Table 3 Horizontal particle displacement (L) for feed pellets and feces estimated for a cobia (Rachycentron canadum) farm located off the coast of Recife, northeastern Brazil. Values were calculated for median (50) and 90th percentile (90) of sea currents. Feed pellets

Northwards Southwards Towards the shore Away from shore

Feces

L50 (m)

L90 (m)

L50 (m)

L90 (m)

40 23 10 16

66 38 17 28

84 44 23 37

129 78 45 62

changes in environmental conditions and increase their abundance (“tolerant” or “opportunistic”) (Warwick, 1988). Giangrande et al. (2005) and Martinez-Garcia et al. (2013) classified the families of Polychaeta subjected to the effects of organic enrichment as tolerant, which are those that remain in the area exposed to the impact and often proliferate; while those families classified as sensitive are the ones that disappear or their abundance is drastically reduced. Many species have been identified as being associated with stress or pollution conditions, but, in general, these same species are also found in non-polluted environments (Rygg, 1985; Bellan, 2013). Although the literature has records for some families, impact responses are very specific for each situation and it is common to see differences or inconsistencies between results for some families. Moreover, since prior knowledge about the distribution and ecology of the Polychaeta in the area of the present study is limited, it is difficult to understand how the fauna will respond. The results of the present study may, therefore, serve as an initial reference for this geographical area. Although this was the first production cycle carried out on this site, alterations in some of the environmental variables and in the community structure of Polychaeta were detected throughout the study period, and were considered to be of moderate impact. These changes were significant in the scale of time, but not spatially, i.e. there was variability between different sampling campaigns, but not between sampling stations. One possible reason for the lack of differences between sampling stations may be the variation in the direction of the dominant currents and waves during the study period, which would disperse the 5

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Fig. 5. Mean ( ± SE) estimates of Margalef's richness index (A), density (B; individuals m−2), Simpson's index of diversity (C) and Pielou's evenness index (D) applied to the families of Polychaeta for the initial, intermediate and final sampling campaigns from a cobia (Rachycentron canadum) farm off the coast of Recife, northeastern Brazil. Different letters represent significant differences between sampling campaigns (p < .05).

considered sensitive enough to demonstrate changes between sampling campaigns, which leads to the conclusion that a taxonomic refinement would only emphasize the results found and perhaps identify some spatial gradient of organic enrichment moving away from the farm

(Somerfield and Clarke, 1995; Olsgard et al., 1998). The main issue is that the higher the species richness, the greater the loss of taxonomic information and the lower the ability to detect changes in the environment. In the present study, the resolution at the family level was

Fig. 6. Multidimensional scaling analysis (MDS) based on the abundance of Polychaeta in the initial, intermediate and final sampling campaigns at different sampling stations from a cobia (Rachycentron canadum) farm off the coast of Recife, northeastern Brazil (Unprocessed data. Bray Curtis Similarity). 6

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Acknowledgements

area. This issue is of particular importance for studies in the tropics given the much higher species diversity in relation to temperate areas. Environmental monitoring studies can be optimized using not only invertebrate data at large taxonomic levels, as proposed by the concept of taxonomic sufficiency, but also by choosing a group of representativeness in the samples and doing taxonomic refinement (Giangrande et al., 2005). In the present study, Syllidae was the most abundant family, which is appropriate for ecological studies not only because it is well-known taxonomically but also because it is sensitive to disturbances, decreasing in abundance or disappearing completely when exposed to different sources of impact (San Martín, 2005). In the present study, however, Syllidae was more abundant with the passage of time, which was also observed in a tropical bay subjected to the contribution of urban effluents (Omena et al., 2012). The possibility that nutrient-rich freshwater runoff may also have an effect in the area of the fish farm should also be considered. The relative proximity of the Barra de Jangada estuary to the fish farm (approximately 6 km) turns it into a probable source of nutrients. However, the reduced water flow throughout most of the year is known to cause little or no influence on the shallow continental shelf (between 20 and 40 m depth) (Coelho et al., 2004). Despite this, it is important not to discard the influence of freshwater runoff because events of heavy rainfalls within a short period of time are commonplace in northeastern Brazil during winter and may increase the discharge of freshwater into the ocean in such a way that the nutrient and organic matter supply may affect the area of the fish farm. In a parallel study, Klein (2012) concluded that the cage culture of cobia in this area had no significant impact on any of the several water quality variables measured. As mentioned earlier, the relatively fast currents (higher than 0.20 m s−1) would disperse the dissolved nutrients and organic material released from the fish cages. Molina Domínguez et al. (2001) suggested that currents with a mean speed of 0.06 m s−1 may be sufficient to disperse solid waste. Sarà (2007b) adds that significant impacts on water quality occur more commonly in environments with reduced hydrodynamics. Therefore, rather than water quality, the analysis of the structure of the benthic community appears to be a more potent indicator of the negative effects of cage fish farming, especially in environments characterized by high hydrodynamics. Using macrofauna to visualize stress effects on sediment would be more useful than using only physical-chemical analyses, as the classical monitoring programs do, because they reflect only conditions at the time of sampling, while macrofauna demonstrate the cumulative effects over time (Omena et al., 2012). Based on the present results, it is concluded that the changes in the structure of the benthic macrofauna community occurred only in a temporal, non-spatial way. The probable cause was the organic enrichment of the sediment due to the residues from the fish cages. Previous to the implantation of fish farming projects, the local biota, especially the benthic community, water quality variables and the marine currents should be characterized. The monitoring of these parameters should also be carried out during and after the installation of any cage aquaculture operation so that a more accurate analysis of its influence on the environment may be possible.

This study received national funds from the Ministry of Fisheries and Aquaculture – MPA and the National Council for Scientific and Technological Development – CNPq (Grants no. 559.759/2009-6 and 559.741/2009-0). L. S. Lima, B. C. S. Brandão, E. C. Domingues and A. P. Klein acknowledge study grants from CNPq and the Coordination for the Improvement of Higher Education Personnel- CAPES. R. O. Cavalli, L. H. Poersch and C. A. Schettini are research fellows of CNPq. References Apostolaki, E.T., Tsagaraki, T., Tsapakis, M., Karakassis, I., 2007. Fish farming impact on sediments and macrofauna associated with seagrass meadows in the Mediterranean. Estuar. Coast. Shelf Sci. 75, 408–416. https://doi.org/10.1016/j.ecss.2007.05.024. Bellan, G., 2013. Effects of pollution and man-made modifications on marine benthic communities in the Mediterranean: a review. In: Moraitou-Apostolopoulos, M., Kiortsis, V. (Eds.), Mediterranean Marine Ecosystems. Plenum Press, New York, pp. 163–188. 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Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Author contributions Conceived and designed the study: LSL, TKP, SH, CAS, LHP and ROC. Performed the experiment: LSL, SH, ECD, APK, LHP and ROC. Analyzed the data: LSL, TKP, BCSB, WS, APK, CAS, LHP and ROC. Wrote the paper: LSL, TKP, SH, APK, CAS, LHP and ROC. 7

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