Macrobenthic associations in a South Atlantic Brazilian enclosed bay: The historical influence of shrimp trawling

Marine Pollution Bulletin 62 (2011) 2190–2198

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Macrobenthic associations in a South Atlantic Brazilian enclosed bay: The historical influence of shrimp trawling Tito Cesar Marques de Almeida 1, Jorge Matheus Vivan ⇑ Laboratory of Aquatic Communities Ecology, UNIVALI – Universidade do Vale do Itajaí, Rua Uruguai, 458, Centro Bloco 20 Sala 144, Caixa Postal 360, CEP 88302-202 Itajaí, SC, Brazil

a r t i c l e

i n f o

Keywords: Macrobenthic associations Tijucas Bay Physical disturbance Trawling Diversity Restoration

a b s t r a c t This study characterized the macrobenthos of Tijucas Bay and related the distribution and dominance patterns with historical trawling activities. Fifteen sampling sites were established in the bay and were sampled in summer and winter for the characterization of the macrobenthos. To evaluate the trawling effects, three passages were established at each site with control and impacted areas analyzed before and after trawl-net action in impacted area. Seasonal differences occurred in macrobenthos, possibly influenced by rainfall where the relative water level of the Tijucas River was directly associated with the discharge of freshwater and particulate matter. The associations identified in the bay were distinct in comparison with the Zimbros Embayment. The trawling assessment showed no significant variation in the macrobenthos after the trawl, possibly due to decades of shrimp exploitation in the bay. Trawling and instable environmental conditions inside the bay make the establishment of a stable macrobenthic community difficult. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Benthic macroinvertebrates are present in all marine habitats, from abyssal trenches to mangrove roots, and are found even in very polluted or extremely disturbed environments (Brusca and Brusca, 1990; Lalli and Parsons, 1999), denoting the ecological importance of this group as an indicator of diversity (Boyd et al., 2003; Carvalho et al., 2001; Maia et al., 2001; Newell et al., 2004). The distribution, occurrence and abundance of benthic macrofauna are influenced by the predominant environmental characteristics, mainly in relationship to sediment, food availability and environment stability (Gray, 1974). Studies on the structure and composition of benthic communities are important in the processes of natural environment monitoring. The increase in the exploitation pressure on coastal ecosystems, such as shrimp fishing, was responsible for changes in the environment, affecting quality and maintenance of fish stocks (McConnaughey et al., 2000) and therefore compromising the quality of life of the human population that use these resources. Among the main effects caused by fishing are the resuspension of sediments, changes in the conformity of the physical environment, changes in biogeochemistry and changes in the structure and composition of the macrofauna (Kenchington et al., 2001;

⇑ Corresponding author. Tel.: +55 47 91341104. E-mail addresses: [email protected] (T.C.M. de Almeida), jm.vivan@ yahoo.com.br, [email protected] (J.M. Vivan). 1 Tel.: +55 21 71235099. 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.06.034

Thrush et al., 1998). There is an extensive scientific literature concerning the specific impacts of each of those effects (Collie et al., 2000; Duplisea et al., 2002; Gilkinson et al., 1998; Jones, 1992). Physical changes caused by fishing artifacts include scraping, the formation of cracks and grooves, the removal of natural features, such as outcrops and carbonate structures, and the destruction of aquatic vegetation (Black and Parry, 1994; Fonseca et al., 1984; Jones, 1992; Messieh et al., 1991; Schwinghamer et al., 1998). The trawl nets often penetrate from 5 to more than 30 cm into the sediment, resulting in the removal of epifauna and endofauna (Kaiser, 1998). Tijucas Bay allowed the establishment of a diversity of species of economical importance, such as shrimp in the Penaeidae family. These crustaceans were and are the principal fishery resource in the region, an important nursery area exclusively explored for decades by artisanal fishermen (Andrade, 1998; Perez et al., 2001). The objective of this study was to describe the benthic macrofauna associations in summer and winter in Tijucas Bay and the effects of trawling on the macrofauna. We believe that decades of trawling in Tijucas Bay may have changed the natural features related to the composition and structure of the benthic macrofauna. 2. Methods 2.1. Study site Tijucas Bay (lat. 27°150 S and long. 48°330 W, WGS84 Geographic Coordinate System) is on the coastal plain, with muddy shoals and

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chenier systems that extend 2.0 km inland, between the granitic rocks of Porto Belo and Ganchos Headland (FitzGerard et al., 2007), southern Brazil (Fig. 1). The mouth of the Tijucas River, with an average flow of 53 m3 s1 is located in the coastal plain. The area is protected from waves and currents by the Porto Belo Headland to the north and Santa Catarina Island and the Ganchos Headland to the south (Fig. 1). It is directly influenced only by a microtidal regime, allowing the deposition of fine sediment exported to the estuary, forming extensive muddy tidal flats (Schettini and Carvalho, 1998). Although it has a relatively small drainage basin, the Tijucas River has a high concentration of suspended sediment. These characteristics result in a complex balance between waves and tides dominating the hydrodynamic regime in the area (Asp et al., 2009). The bay is relatively shallow, with a maximum depth of approximately 12 m. Small fishing nuclei are found along the Tijucas River margins. The north margin nuclei are located in an urban area and are larger than the south margin nuclei (Wahrlich, 1999). The fishermen who live in these nuclei focus their activities mainly in Tijucas Bay and the adjacent areas near the coast. 2.2. Macrofauna characterization and composition To characterize the mollusk and polychaete associations, two surveys were completed, the first in the summer (March 15, 2005) and second in the winter (August 2, 2005). Fifteen sample sites were distributed in Tijucas Bay (Fig. 1). In each season, six samples were collected at each site, with a 0.025 m2 Van-Veen grab: five samples for macrofauna analysis and one for granulometric analysis. The samples collected for macrofauna were fixed

in a formaldehyde saline solution at 4%. In the laboratory, each sample was washed through a 500 lm mesh size sieve. The macrofauna was sorted under a stereomicroscope, identified to the lowest possible taxonomic level, quantified and transferred to a 70% alcohol solution in properly labeled plastic containers. A specific abundance table of the sampled taxa was created. The sediment samples collected for granulometric assessments were analyzed according to the methodology proposed by Suguio (1973). Rainfall and temperature data for summer and winter were obtained at Empresa de Pesquisa Agropoecuária e Extensão Rural (EPAGRI) (www.epagri.sc.gov.br). 2.3. Assessment of trawling effects on the macrofauna Three experiments were performed in May 2006 on board a small (8 m long) shrimp trawl boat. Three passages were established in the north side of Tijucas Bay, near the Zimbros Embayment (Fig. 1). Intensive fishing activities occur in passages 1 and 2. Less intensive fishing activities occur in passage 3 because of the proximity of headlands and outcrops. Two parallel areas were defined in each passage, 10 m wide and 100 m long. One area of each passage was trawled (impacted) while the other area was considered to be a control. Sampling was completed in each area before and after the trawling of the impacted area. The impacted area was trawled five times. Five samples were collected with a 0.042 m2 Van-Veen grab for macrofauna analysis. The collected samples of macrofauna were fixed in a formaldehyde saline solution at 4%. In the laboratory, each sample was washed through a 500 lm mesh size sieve. The macrofauna was sorted under a stereomicroscope, identified to the lowest possible taxonomic level, quantified and transferred

48º30’33’’ 1

1

N

Zimbros Embayment

3

2

27º11’57’’

Brazil

2

4 3

5

6

Porto Belo Peninsula

7 10 m

Tijucas River 8

10

9

Tijucas Bay 5m

Tijucas Bay

Santa Catarina Island

27º18’27’’

11

13

12

Ganchos Peninsula 14

48º34’24’’

15

4000 m

Fig. 1. Map of the study site, with the locations of the 15 sample sites for the characterization of the macrofauna and the three passages used in the trawling experiment located within the Zimbros Embayment. The black areas of the passages = impacted and the white areas of the passages = control.

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design used for the analysis of variance for the characterization and assessment of the trawling effects was applied in the PERMANOVA analysis. This analysis used the Bray–Curtis similarity coefficient transformed using log(X + 1). Subsequently, a pairwise comparison was performed. Using the same Bray–Curtis similarity matrix, a non-metric multidimensional scaling analysis (MDS) was applied to interpret the temporal and spatial variations (Clarke and Warwick, 2001) evidenced by the PERMANOVA analysis. For the characterization study, a similarity percentage analysis (SIMPER) was performed on the groups formed by the pairwise PERMANOVA. For the trawling experiment, a similarity percentage analysis (SIMPER) was performed to identify composition changes for each time (before and after trawling in the control and impacted areas) (Clarke and Warwick, 2001).

to plastic containers with 70% alcohol solution, properly labeled. A specific abundance table of the taxa sampled was created. 2.4. Data analysis Principal component analysis (PCA) was used to test for temporal and spatial variation in granulometric characteristics. The dependent variables were the percentage of fine sediment, coarse sediment, carbonate and organic matter, all of which meet the requirements of non-colinearity and univariate normality (Clarke and Warwick, 2001). For macrofauna characterization, the community structure of each site was evaluated based on abundance (N, number of individuals/0.025 m2) and Shannon–Weaver diversity (H0 , calculated using natural logarithms). To assess trawling effects on the macrofauna, the community structure of each site was evaluated based on richness (S), abundance (N, number of individuals/ 0.042 m2), Shannon–Weaver diversity (H0 , calculated using natural logarithms) and evenness (Pielou, J0 ). A crossed analysis of variance was used to test the null hypothesis that the interaction of sites and season was not significant in the analyzed ecological descriptors. To test the null hypothesis that trawling did not modify faunal structure, a nested analysis of variance was applied, considering spatial variability. The sampling design of the characterization used the factors time (summer and winter, two levels, random) and sites (1–15, 15 levels, random and crossed with the factor time). The sampling design of the trawling experiments used the factors area (impacted and control, two levels and random), time (before and after, two levels, random and orthogonal) and passage (1, 2 and 3, three levels, random and hierarchic to the factors area and time). The normality and homogeneity of the variances were verified using Kolmogorov–Smirnov and Bartlett tests, respectively, both were accepted if p > 0.05. When the homogeneity of variances was not found, the data were transformed using log(X + 1). A non-parametric permutational multivariate analysis of variance (PERMANOVA) was used to test for significant differences in the community composition (Anderson, 2001, 2005). The same

3. Results The depths at the sample sites in the bay ranged from 3 to 12 m. The shallower sites were located in the Zimbros Embayment (3 m depth at sites 1 and 2, 6 m at sites 3 and 4). The sites near the Tijucas River (7, 10 and 11) were 5 m deep. The central sites of Tijucas Bay (sites 5, 6, 8, 12 and 13) had depths of approximately 8–10 m. Site 9 was the deepest, at approximately 12 m. Higher rainfall occurred in the summer. During the 15 days prior to the summer survey, the average rainfall was 6 mm per day, whereas during the 15 days prior to the winter survey, the average rainfall was 2.7 mm per day. The average atmospheric temperature during the summer was approximately 20.8 °C, whereas in the winter it was approximately 10.9 °C. The first two principal components of the PCA explained 92.09% of the total variation (Fig. 2). The first axis, which explained 72.63% of the overall variance, described the highest percentage of fine sediment and organic matter, principally at the sites located in the Zimbros Embayment and near the Ganchos Peninsula (sites 3, 4, 5, 6, 11, 12, 13 and 15), and the coarse sand with carbonate in the sites mainly in the center of the bay (2, 7, 8, 9 and 10). Axis 2, which explained 19.46% of the total variation, separated the

1.2

Summer Winter

Carbonate

Fine Sediment (Silt and Clay)

Axis 2 (19,46%)

9

15 12 13 4 1 11 6 3 3

5

-0.7

6

7 7 10

1 9

8

1.2

5

2 15

11

2

Organic Matter

12

4

13 10

Coarse Sediment

-0.7

Axis 1 (72,63%) Fig. 2. Principal component analysis (PCA). The representation of the factorial axes 1 and 2, which explained 72.63% and 19.46%, respectively, of the variation. The vectors represent the percentage of fine sediment (silt and clay), coarse sediment (sand), carbonate and organic matter. The numbers represent the sites, and the colors represent the season: Black = Summer, Gray = Winter. There were no sediment data from sites 14 (summer and winter) and 8 (summer).

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Table 1 Specific abundance composition in the summer and winter characterization sampling and the trawling change assessment. For the summer and winter characterization sampling a 0.025 m2 Van-Veen grab was used (n = 150). For the trawling change assessment a 0.042 m2 Van-Veen grab was used (n = 60). Characterization

Trawling changes assessment Impact

Total

%

Control

Before

After

Before

After

Summer

Winter

1

2

3

1

2

3

1

2

3

1

2

3

Polychaeta Aricidea sp. Armandia spp. Cirratulidae sp. Cirrophorus branchiatus Ehlers, 1908 Cossura sp. Eusyllinae sp. Exogone sp. Glycera sp. Goniada maculata Örsted, 1843 Gyptis sp. Kinbergonuphis orensanzi (Fauchald, 1982) Laonice cirrata (Sars, 1850) Linopherus ambigua Monro, 1933 Lumbrineris sp. Magelona crenulata Bolívar and Lana, 1986 Magelona papillicornis Müller, 1858 Magelona posterelongata Bolívar, 1986 Magelona variolamellata Bolivar & Lana, 1986 Maldanidae sp. Mediomastus californiensis Hartman, 1944 Neanthes bruaca Lana and Sovierzoski, 1987 Ninoe brasiliensis Kinberg, 1865 Notomastus lobatus Hartman, 1947 Owenia sp. Paradoneis sp. Loandalia spp. Paraonis sp. Paraprionospio pinnata (Ehlers, 1901) Pholoididae sp. Phylo sp. Piromis sp. Poecilochaetus sp. Polinoidae sp. Prionospio dayi (Foster, 1969) Prionospio steenstrupi Malmgren, 1867 Protoaricia sp. Sabellidae sp. Schistomeringos rudolphi (Delle Chiaje, 1828) Scoloplos sp. Sigalionidae sp. Sigambra spp. Sthenelais sp. Syllidae sp. 1 Syllidae sp. 2 Syllidae sp. 3 Syllidae sp. 4 Terebellides sp.

370 6 3 3 14 0 0 0 3 10 48 3 1 2 0 17 30 22 2 309 11 67 497 8 1 30 10 62 0 0 0 1 6 5 0 1 0 4 4 0 36 2 1 1 9 0 0

127 9 4 0 5 0 25 0 10 2 175 6 1 0 1 10 16 14 0 71 14 42 64 7 0 23 0 156 0 0 2 1 1 6 92 0 2 0 1 0 22 10 0 9 2 1 1

24 0 0 0 0 0 0 0 1 0 0 3 0 1 0 14 7 5 0 1 13 9 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0

102 0 0 0 0 0 0 0 4 0 0 0 0 1 0 15 2 8 0 13 5 20 0 0 0 4 0 6 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0

2 0 1 3 0 0 0 0 0 0 0 7 0 0 0 1 0 0 0 0 1 0 17 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 1

7 0 0 0 0 0 0 0 5 0 0 1 0 0 0 13 2 9 0 1 14 4 1 1 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

69 0 0 0 0 0 0 0 1 0 0 0 0 0 0 8 2 3 0 7 6 13 0 2 0 4 0 10 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0

1 0 0 0 0 0 0 0 0 0 0 9 0 0 0 0 0 0 0 4 0 1 21 0 0 0 0 3 0 1 0 0 0 0 0 0 0 0 0 0 10 0 0 0 0 0 0

39 0 0 0 0 0 0 0 1 0 0 0 0 0 0 27 6 6 0 2 2 12 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0

87 0 0 0 0 0 0 0 3 0 0 0 0 0 0 11 0 11 0 6 4 22 1 0 0 4 0 6 0 0 0 0 0 0 0 0 0 0 0 0 7 0 0 0 0 0 0

1 0 0 1 0 0 0 0 0 0 0 8 0 0 0 1 0 1 0 2 0 1 21 0 0 0 1 1 1 1 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0

14 0 0 0 0 0 0 0 2 0 0 0 0 0 0 12 5 5 0 1 5 12 0 0 0 2 0 7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

71 0 0 0 0 0 0 0 2 0 0 0 0 1 0 7 5 17 0 7 4 28 3 0 0 4 0 4 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0

0 0 4 6 0 1 0 1 0 0 0 12 0 0 0 0 0 0 0 7 3 0 42 0 0 0 0 3 1 0 0 1 0 0 0 0 0 0 0 0 7 0 0 0 0 0 0

914 15 12 13 19 1 25 1 32 12 223 49 2 5 1 136 75 101 2 431 82 231 667 18 1 71 11 266 4 2 2 3 7 11 92 1 2 4 5 1 93 12 1 10 11 1 2

14.5 0.2 0.2 0.2 0.3 0.0 0.4 0.0 0.5 0.2 3.5 0.8 0.0 0.1 0.0 2.2 1.2 1.6 0.0 6.8 1.3 3.7 10.6 0.3 0.0 1.1 0.2 4.2 0.1 0.0 0.0 0.0 0.1 0.2 1.5 0.0 0.0 0.1 0.1 0.0 1.5 0.2 0.0 0.2 0.2 0.0 0.0

Gastropoda Acteocina bullata (Kiener, 1834) Anachis obesa Adams, 1845 Cylichna discus Watson, 1886 Eulima sp. Natica sp. Olivella sp. Volvulella persimilis (Morch, 1875)

4 2 3 0 2 0 0

6 0 3 1 14 1 2

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

0 0 0 0 0 0 0

10 2 6 1 16 1 2

0.2 0.0 0.1 0.0 0.3 0.0 0.0

Pelecypoda Abra lioica (Dall, 1881) Chione subrostrata (Lamarck, 1818) Corbula caribaea Orbigny, 1842 Diplodonta sp. Felaniella vilardeboana (d´Orbigny, 1846) Mactra fragilis Gmelin, 1791 Mactra iheringi Dall, 1897 Mactra marplatensis Doello-Jurado, 1918 Mactra spp. Nucula puelcha Orbigny, 1846 Nucula semiornata d´Orbigny, 1846

6 1 33 0 0 6 197 7 31 2 0

14 0 0 1 1 0 0 0 208 2 1

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0

20 1 33 1 1 6 197 7 239 4 1

0.3 0.0 0.5 0.0 0.0 0.1 3.1 0.1 3.8 0.1 0.0

(continued on next page)

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Table 1 (continued) Characterization

Trawling changes assessment Impact

Total

%

Control

Before

After

Before

After

Summer

Winter

1

2

3

1

2

3

1

2

3

1

2

3

Pitar fulminatus (Menke, 1828) Pitar sp. Tellina sp. Trachycardium muricatum (Linnaeus, 1758) Transenella stimpsoni Dall, 1902 Transenella sp.

0 0 21 0 0 0

1 2 21 1 1 1

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

1 2 42 1 1 1

0.0 0.0 0.7 0.0 0.0 0.0

Crustacea Amphipoda Brachyura Cumacea Decapoda Kalliapseudes sp.

6 65 45 74 439

174 2 218 28 316

0 0 0 0 0

0 0 0 0 0

10 0 0 9 50

0 0 0 0 0

0 0 0 0 0

8 0 0 6 83

0 0 0 0 0

0 0 0 0 0

17 0 0 9 81

0 0 0 1 0

0 0 0 0 0

17 0 0 11 96

232 67 263 138 1065

3.7 1.1 4.2 2.2 16.9

Anthozoa Anfioxo Echinoidea Echiura Holothuroidea Nemertea Ophiuroidea Opisthobranchia Sipuncula

0 5 0 0 0 2 8 21 47

7 9 1 1 7 2 1 114 35

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

7 14 1 1 7 4 9 135 82

0.1 0.2 0.0 0.0 0.1 0.1 0.1 2.1 1.3

Total

2626

2128

840

6301

100

summer and winter samples; the summer was characterized by fine sediments and the winter by organic matter. A total of 6.301 organisms were collected, and 4.252 were polychaetes or mollusks. Polychaetes were the most abundant taxonomic group, with 86% of the total abundance, and mollusks composed 14% of the total abundance. The most abundant taxa were Aricidea sp., Owenia sp., Neanthes bruaca Lana and Sovierzoski, 1987, Mediomastus californiensis Hartman, 1944, Mactra spp. and Kinbergonuphis orensanzi (Fauchald, 1982); together, they accounted for 60.6% of the total (Table 1).

707

3.1. Macrofauna characterization and composition The abundance (ind./0.025 m2) and Shannon–Weaver diversity showed significant differences for the site  season-crossed interaction and among the sites. There were no significant differences between seasons (Table 2). The sites that showed the highest variability in abundance were the sites inside the Zimbros Embayment (1, 2, 3, 4 and 5), sites near the Ganchos Peninsula (11, 12, 14 and 15) and sites near the mouth of the Tijucas River (7 and 10). Generally, the higher abundances were found at the sites inside

Table 2 Fisher’s test (F) and significance (p) for abundance (ind./0.042 m2) and Shannon–Weaver diversity (H0 ) to the season, sites and the crossed interaction site(season). DF = degree of freedom. DF

Season Site Season  site

1 14 14

Abundance (ind./0.042 m2)

Shannon–Weaver diversity (H0 )

F

p

F

p

2044 10,616 3572

0.155376 0.000000 0.000064

0543 2519 1807

0.462748 0.003500 0.044965

Abundance (ind./0,025m²)

. . . . . .

Fig. 3. Abundance (ind./0.025 m2) for the summer sites (a) and winter sites (c), and Shannon–Weaver diversity (H0 ) for summer sites (b) and winter sites (d). Bars indicate standard error.

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T.C.M. de Almeida, J.M. Vivan / Marine Pollution Bulletin 62 (2011) 2190–2198 Table 3 Permutational multivariate analysis of variance (PERMANOVA). P of permutation values, between summer and winter. DF = degree of freedom, SS = sum of squares, MS = mean of squares. Source

DF

SS

MS

F

P(perm)

Season Site Season  site Residual

1 14 14 120

19602.2688 151175.0849 73315.7562 242204.5220

19602.2688 10798.2204 5236.8397 2018.3710

3.7431 2.0620 2.5946

0.0019 0.0004 0.0001

Total

149

486297.6319

2 4 5

10

1 11

3.2. Assessment of trawling changes on the macrofauna Abundance (ind./0.042 m2), evenness (J0 ) and Shannon–Weaver diversity (H0 ) varied significantly between passage(area  time)

11

6

2

13

3 7 9 8

5

the Zimbros Embayment. The diversity was higher at the sites located in the center of the bay, and the seasonal variations occurred mainly in the sites located inside the Zimbros Embayment (2, 3 and 5), near the Ganchos Peninsula (13, 14 and 15) and near the mouth of the Tijucas River (7, 9 and 10) (Fig. 3). PERMANOVA showed significant differences for site  season (Table 3). The macrofauna associations varied in space. The pairwise comparisons between sites for each season (summer and winter) demonstrated distinct associations for the central sites of Tijucas Bay. The sites located inside the Zimbros Embayment and in front of the mouth of the Tijucas River showed distinct faunal associations (Fig. 4). The species primarily responsible for the similarity between the associations, analyzed by the percentage of similarities (SIMPER), are also presented in Fig. 4. Multidimensional scaling analysis (MDS), applied to identify space–time variations between the macrobenthic associations, showed that across space, composition differences were seen between the sites located in the Zimbros Embayment and the sites located in central Tijucas Bay. For time, differences in abundance were seen between summer and winter (Fig. 5).

2D Stress: 0,16

7

8 9

1

3

14 12

15

6 4

14

12

13

10

15

Summer Winter

Fig. 5. Diagram from the multidimensional scaling (MDS) analysis indicating the clear differences among the sites located in the Zimbros Embayment and the outer areas and the differences between summer and winter.

(Fig. 6). Significant differences between area and between times were not verified for diversity. The F and p values for each ecological parameter are described in Table 4. The nested PERMANOVA showed no significant differences between area and time. Significant differences were found only for the passage(area  time) interaction (Table 5). This result indicates that trawling did not alter the composition of the associations present in the passages. Similarity percentage analysis (SIMPER) showed no alterations of the faunal composition between the control and impacted areas and times, except for the impacted area of passage 1, where Aricidea sp. contributed to the similarity before the trawl and Magelona papillicornis after the trawl (Table 6).

Fig. 4. Diagram of Tijucas Bay indicating the associations found by post hoc non-metrical permutational analysis (PERMANOVA), with the calculations based on the Bray– Curtis similarity matrix and transformed using log(X + 1), demonstrating the central association (line) during summer (a) and winter (b). The main taxa responsible for the formation of these associations are also shown, based on similarity percentage analysis (SIMPER). Av. Ab. = Average Abundance, Cont. (%) = Contribution Percentage.

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Before

1,0

After

40

0,8 Eveness (J’)

Abundance (ind./0,042m²)

50

30 20 10

0,0 Impacted

Impacted

Control

Corridor 1

Control

Impacted

Corridor 2

Control

Impacted

Corridor 3

Control

Impacted

Corridor 1

Control

Impacted

Corridor 2

Control

Corridor 3

2,0 Shannon-Weaver Diversity (H’)

12 Species richness (ind./0,042m²)

0,4 0,2

0

10 8 6 4 2 0

0,6

Impacted

Control

Impacted

Corridor 1

Control

Impacted

Corridor 2

1,6 1,2 0,8 0,4 0,0

Control

Impacted

Corridor 3

Control

Impacted

Corridor 1

Control

Impacted

Corridor 2

Control

Corridor 3

Fig. 6. Species richness, abundance (ind./0.042 m2), evenness (J0 ) and Shannon–Weaver diversity (H0 ). Bars indicate standard error.

Table 4 Nested analysis of variance (ANOVA). F and p values for ecological parameters of species richness, abundance (ind./0.042 m2), evenness (J0 ) and Shannon–Weaver diversity (H0 ). Source

DF

Abundance (ind./0.025 m2)

Richness (S)

F

p

F

p

F

p

F

p

Area Time Passage(area  time)

1 2 1

7.892 0.0422 3.5929

0.0208 0.8438 0.0048

5.3987 0.7739 1.0114

0.0455 0.4128 0.4286

9.5738 0.1177 3.1847

0.0135 0.7432 0.0100

1.054 0.319 2.431

0.4052 0.5925 0.0385

Table 5 Permutational multivariate analysis of variance. P of permutation values, evidencing that there is significant differences among all investigated interactions. Source

DF

SS

MS

F

P(perm)

Area Time Corridor(area  time) Residual Total

1 1 8 48 59

9181.113 7646.225 974547.126 360469.244 1357178.641

9181.113 7646.225 121818.391 7509.776

0.0754 0.0628 162.213

0.9368 0.9523 0.0001

A non-metric multidimensional scaling analysis (MDS) applied to identify the variations before and after trawling among the passages in the impacted and control areas only indicated that there were alterations caused by trawling in passage 3. The MDS indicated that passages 1, 2 and 3 were different (Fig. 7).

4. Discussion A clear distinction of faunal composition between summer and winter could be seen, emphasizing the importance of seasonality effects on the behavior of organisms. In the winter, the predominance of organic matter at sites 4, 11, 12, 13 and 15 was seen, possibly caused by low local water input because of a decrease in rainfall during this season. The summer was characterized by a higher concentration of fine sediment (mud), possibly due to the increase in rainfall during this period, which altered the flow of the Tijucas River, increasing the supply of terrigenous sediment. In the summer, the mollusk Mactra iheringi was the principal

Eveness (J0 )

Shannon–Weaver diversity (H0 )

species responsible for the similarity of sites 7 and 10, the sites nearest to the river mouth; this species may have benefited from the increased suspended particulate matter during this period. Climatic perturbations during the winter, such as cold fronts, are often observed in the region. The elevation in wind speed can modify local hydrodynamics and can promote resuspension in the shallow areas of Tijucas Bay, homogenizing sediment distribution and consequently the macrofauna distribution, which is closely related to sediment features. The most abundant species, Aricidea sp., Notomastus lobatus Hartman, 1947, Mediomastus californiensis Hartman, 1944 and Paraprionospio pinnata, are considered to be non-selective deposit feeders (Fauchald and Jumars, 1979). The high dominance of this feeding group in the area suggests a region of unstable characteristics, possibly influenced by human activities. Trawling, which has occurred for a long time (Wahrlich, 1999), combined with the unique environmental conditions of the bay, such the low water renewal, the freshwater contribution of the Tijucas River and environmental problems such sewage, may be contributing to this dominance pattern in the area. Many authors cite sewage as one of main problems in coastal waters (Cannicci et al., 2009; Guerra-García and García-Gómez, 2004; Whomersley et al., 2007). The intensity and extent of human disturbances in marine ecosystems represent a danger to functional and structural environmental biodiversity (Claudet and Fraschetti, 2010). Anthropogenic disturbance can often eliminate natural systems that could be used as baseline for assessment of this kind of impact (Thrush and Dayton, 2002), increasing the difficulty of related studies of disturbances caused by human activities.

2197

T.C.M. de Almeida, J.M. Vivan / Marine Pollution Bulletin 62 (2011) 2190–2198 Table 6 Similarity percentage (SIMPER) for each time, at two areas and in the three corridors. Corridor

Area

Time

Average similarity (%)

Species

Contribution (%)

Cumulative contribution (%)

1

Impact

Before

58.32

After

44.82

Before

61.4

After

53.86

Aricidea sp. Neanthes bruaca Magelona papillicornis Magelona papillicornis Neanthes bruaca Magelona variolamellata Aricidea sp. Aricidea sp. Magelona papillicornis Aricidea sp. Ninoe brasiliensis Magelona papillicornis

34.21 21.1 20.31 26.14 20.46 15.22 14.52 48.57 31.12 26.56 25.36 24.07

34.21 55.32 75.63 26.14 46.6 61.82 76.34 48.57 79.7 26.56 51.92 76

Before

67.13

After

67.09

Before

62.42

After

56.46

Aricidea sp. Ninoe brasiliensis Aricidea sp. Ninoe brasiliensis Pelecypoda Aricidea sp. Ninoe brasiliensis Aricidea sp. Ninoe brasiliensis

69.97 7.88 55.51 11.41 9.17 62.31 12.15 62.27 11.19

69.97 77.85 55.51 66.92 76.09 62.31 74.46 62.27 73.46

Before

63.64

After

59.89

Before

63.75

After

62.9

Kalliapseudes sp. Notomastus lobatus Kalliapseudes sp. Notomastus lobatus Kalliapseudes sp. Amphipoda Kalliapseudes sp. Notomastus lobatus

60.21 14.03 65.34 11.65 57.14 15.14 60.6 16.98

60.21 74.24 65.34 76.99 57.14 72.28 60.6 77.58

Control

2

Impact

Control

3

Impact

Control

i

c

2D Stress: 0,08

i i

i i

i

i i i c c

c c i c i c c c i c c

i

i

i i

i c c

i i

c

c c

i

c

c

c i c i c i c i c ci c c i i i c c c i c i

Fig. 7. Diagram of non-metric multidimensional scaling (MDS), indicating the alterations in time in passage 3. Circle: passage 1. Square: passage 2. Triangle: passage 3. Black: before trawling. White: after trawling. i: impacted. c: control. The dotted line represents the before and after separation in passage 3.

The impacts of trawling on benthic associations may negatively affect environmental quality, and intensive trawling in a region can cause drastic changes in all marine ecosystems (Thrush and Dayton, 2002). Some previous studies (Bergman and Santbrink, 2000; Currie and Parry, 1999) have shown that the structure and composition of macrobenthic associations were not damaged by trawling. The results found in Tijucas Bay corroborated these studies, where macrobenthic communities were only slightly affected or were unaffected by the activities. Environmentally and human imposed conditions allowed the development of resilient communities (McConnaughey et al., 2000; Pagliosa and Barbosa, 2006). In addition, the strong dominance of Aricidea sp., Ninoe brasiliensis, Magelona papillicornis, Notomastus lobatus found in Tijucas Bay was the result of larger time scale changes, possibly caused by frequent

trawling in the bay. The low diversity in the passages reinforced this evidence. These four Polychaeta species have similar feeding behavior; they are preferential deposit feeders. The genera Ninoe and Magelona show some selectivity, while the genera Aricidea and Notomastus are not selective (Fauchald and Jumars, 1979). These species are small, with a short life cycle, and reproduction occurs throughout most of the year (Linton and Taghon, 2000; Qian and Chia, 1994), denoting stress conditions. Carnivorous species with a long life cycle have low frequency and abundance in Tijucas Bay, and human disturbances are the main cause of their reduction. Tuck et al. (1998) showed that trawling causes significant changes in associations in places where this activity does not often occur. Resilient species remain in the area, while sensitive species disappear, due to the remobilization of the seabed. The establishment of benthic populations in Tijucas Bay is naturally difficult because of the instability of the sediments and the influence of freshwater from the Tijucas River. Some species populations have high temporal variation in abundance in these environments, but in relationship to community structure, they present stability to physical disturbances, having high resistance and resilience (Turner et al., 1995). Few or no alterations occurred in the structure and composition of the Tijucas Bay associations, and only in passage 3 were the changes related to species composition. Trawling has occurred in Tijucas Bay for approximately 80 years (Wahrlich, 1999), which may be influencing the results. The composition of the benthic macrofauna may have changed considerably, with only tolerant organisms remaining.

5. Conclusions Trawling is a very important activity for the development of the populations that inhabit coastal regions. Despite the irreversible environmental changes it causes, many families rely on this activity as their main source of revenue.

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Although there are no previous data on structure and community composition of the benthic macrofauna in Tijucas Bay, we believe that decades of intensive trawling have changed this community, which is different now than it was before trawling. The results did not show that trawling did not cause damage to the benthic macrofauna, but that the environmental conditions in the bay may have changed because of human activities, influencing the benthic macrofauna. The trawling effects were not similar between the passages, showing that these effects can vary according to sediment characteristics, the location of the study site, currents, tidal patterns and the degree of exploitation of the area. We are unable to affirm that the changes in the composition and structure of the macrofauna are harmful to the fishery because the shrimp feed on detritus from the ocean floor. However, human impacts on ecosystems can cause problems for the local biota, reducing biodiversity and the natural balance. The objective of this study was to highlight the importance and consequences of human activities on the marine environment. Irresponsible cultural actions need to be reconsidered, even if they are important for human population survival, if the activities are to be sustainable. The management of these areas by the responsible authorities is essential for the maintenance of biodiversity and the possibility of less damage from trawling in the region.

Acknowledgments The authors thank Thiago Emílio Rohr and Cleiton Luiz Foster Jardeweski for assistance in polychaetofauna identification and Juliana Martins de Freitas for assistance in the field. Thanks to UNIVALI for the scientific initiation fellowship PROBic awarded to J.M. Vivan. To Fundação Nacional do Meio Ambiente (FNMA) and the Ministério do Meio Ambiente (MMA) Project ‘‘Pesca Responsável na Baía de Tijucas’’ that made the development of this work possible.

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