Does dredging activity exert an influence on benthic macrofauna in tropical estuaries? Case study on the northern coast of Brazil

ABSTRACT The aim of the present study was to investigate the effect of dredging activities on the structure of the macrobenthic community of a port complex in São Luís do Maranhão (2°S, Brazil). Sampling was performed on four occasions: pre-dredging, dredging 1 (25% of the material dredged), dredging 2 (75% of the material dredged) and post-dredging. Total mean density was 430.8 ± 55.0 ind/m², with 147.76 ± 280.82 ind/m² at pre-dredging, 161.90 ± 285.67 ind/m² at dredging 1, 53.83 ± 72.15 ind/m² at dredging 2 and 67.29 ± 72.58 ind/m² after dredging, revealing a reduction during dredging 2. The most representative groups were Polychaeta, Oligochaeta, Crustacea and Mollusca. Lumbrineris sp. (Polychaeta) was present in all sampling periods and was the dominant species. Richness and Shannon diversity of the species were higher in the pre-dredging and post-dredging periods, with reductions during the dredging activities (dredging 1 and 2). Principal component analysis revealed a correlation with granulometry and heavy metals in the sediment. The dredging activities led to a reduction in the macrobenthic community. Moreover, post-dredging recovery was insufficient for the recovery of the community.

Coastal ecosystems have high ecological, social and economic value, but have been undergoing changes due mainly to the excessive exploitation of natural resources as well as disorderly land use and occupation (Gruber et al., 2003).Among the different impacts to which coastal environments are subjected, the expansion of port activities is considered one of the factors posing the greatest environmental risk (Bolam, 2012).The operational and expansion activities of a port complex exert a considerable impact on the ecosystem (Castro & Almeida, 2012).Moreover, periodic dredging for the maintenance of navigation channels (Cruz-Motta & Collins, 2004) causes impacts in the form of changes to the water and sediment, such as an increase in the turbidity of the water column, pollution by toxic substances as well as changes in the structure and dynamics of macrobenthic communities (Lewis et al., 2001;Bolam, 2012).
Benthic communities are important to the secondary production of aquatic ecosystems, playing key roles in the stability of the sediment, the cycling of organic matter and as an important food source for larger organisms, many of which have economic value (Thrush & Dayton, 2002;Bolam, 2014).The occurrence, abundance and structure of the benthic macrofauna are influenced by the predominant environmental characteristics, especially those related to the sediment, availability of food sources and environmental stability (Almeida & Vivan, 2011;Zalmon et al., 2013).Environmental factors, such as the homogeneity of the sediment and organic enrichment, are also determinants in the reduction of the benthic macrofauna, making environments with a high degree of disturbance azoic (Pires-Vanin et al., 2011).Dredging activities cause short-and long-term effects on benthic communities, such as reducing the number of species and abundances, altering the properties of sediments, nutrients and organic matter (Newell et al., 1998;Wilber et al., 2007;Ponti et al., 2009).
Due to their errant or sedentary lifestyle and relatively long lifecycles, benthic organisms offer a precise reflection of environmental conditions prior to the time of sampling (Sola & Paiva, 2001;Khedhri, 2016), making them excellent indicators for evaluation of environmental changes (Netto & Lana, 1994;Sandrini-Neto et al., 2016).The rapid deterioration of estuarine ecosystems due to urbanization and industrialization throughout the world has been widely discussed.One such issue is the recovery of dredged environments, where the loss of taxonomic and functional characteristics has hindered evaluations in tropical regions (Mulik et al., 2017), which are generally studied less.This is particularly true for the channels that connect estuaries to the ocean in port areas.Recurrent dredging activities affect the depth, re-suspension and composition of the sediment, resulting in changes in local communities, which are often unable to attach themselves in these environments, leading to their sporadic occurrence (Cruz-Motta & Collins, 2004).
The impact of dredging on macrobenthic communities has been worrying, because this group plays an important role in nutrient recycling, secondary production and is efficient as an indicator of environmental disturbances (McLusky & Elliot, 2004;Gray & Elliott, 2009;Rehitha et al., 2017).Studies have shown that macrofaunal communities of stressed habitats are typically more resilient in comparison to those in more stable environments; moreover, the recovery of the original community may take nine months in less stressed environments, but up to four or five years in more disturbed environments (Bolam & Rees, 2003;Froján et al., 2011).Thus, regions under the influence of port and industrial activities are extremely susceptible to pollution and contamination.
The São Luís Port Complex in the state of Maranhão is one of the main ports of Brazil (Amaral & Alfredini, 2010) and has considerable economic importance due to intensive exportation activities, particularly grains, iron and aluminum.Dredging activities have been performed when needed for the circulation of ship traffic in the region since 1856 (Viveiros, 1954).The frequent dredging for the maintenance of navigation channels underscores the need to evaluate the impact on biological communities in this tropical estuarine ecosystem.It has potentially high diversity, but has been sparsely studied, especially in terms of benthic macrofauna, which are drastically exposed to disturbances of the sediment.The few studies on the benthic macrofauna of the Maranhão coast have mainly been conducted around São Marcos, which is near the port complex, as well as in mangroves and on beaches (Oliveira & Mochel, 1999;Fernandes, 2003;Barros, 2008;Feres et al., 2008;Neves & Valentin, 2011;Ribeiro & Almeida, 2014;Cutrim et al., 2018).
Considering the results of previously conducted studies, one may expect significant reductions in the abundance, diversity and richness of the benthic macrofauna during dredging activities as well as the subsequent recovery of these organisms in the dredged area.Therefore, the objective of the present study was to evaluate the impact of dredging, environmental variables and the recovery time of organisms in the studied area.

MATERIALS AND METHODS
Study area.The São Luís Port Complex is located in São Marcos Bay (02º 30'0"S 44º37'0"W) to the southeast of São Luís Island (Fig. 1).It is considered one of the largest ports on the Brazilian coast and the second largest port in Latin America in terms of cargo movement (Amaral & Alfredini, 2010).The tidal pattern of the port areas is semidiurnal macrotides (~7 m in range; Diniz et al., 2014).Mean currents range from 0.6 to 6.3 knots during the low and high tide, respectively (Garcia & Alfredini, 2005).The region is dominated by mangroves and characterized by a warm, semi-humid climate with two well-defined seasons (a rainy season from January to June and a dry season from July to December), with total annual precipitation around 2000 mm (Azevedo & Cutrim, 2007).
Sampling and analysis.Sampling was performed on four occasions: prior to dredging (January 27, 2014), dredging 1 with 25% of the material dredged (February 2, 2015), dredging 2 with the remaining 75% of the material dredged (March 9, 2015) and 120 days after the conclusion of the dredging activities (June 16, 2015).Eight points (P1-8) were sampled in each period.P3 and P5 were areas of the discarding of the dredged material; P4 and P6 were located near the mangrove; P1 and P2 were in the mooring area; and P7 and P8 were in the navigation canal.
The area was dredged by Cutter and Suction Dredge, which has equipment for the fragmentation of hard material and a self-transporting dredge as secondary dredging equipment, totaling 580,343 m³ of dredged material in the two campaigns.
Samples were collected from each sampling point with the aid of a 20-l stainless steel van Veen sampler for the analysis of the macrofauna, granulometric characterization and the determination of heavy metals.Immediately after collection, one of the samples at each point was placed in a plastic bag and fixed with 4% formalin.The material was transported to the laboratory for sorting with a sieve (0.5mm mesh) and the organisms were identified with the aid of specialized literature (Rios, 1994;Amaral & Nonato, 1996).The other sediment samples were stored in plastic bags and transported to the laboratory for the determination of the textural characteristics of the sediment through sifting (ABNT NBR norm 7181/84) and the determination of heavy metal concentrations following recommendations by American Public Health Association -APHA (2012).Additionally, subsurface water (-50 cm) was collected from each point with a Nansen bottle for the determination of temperature, pH, dissolved oxygen and salinity, which were measured using a multi-parameter probe (Hanna HI 9828).The water was then stored and sent to the laboratory for the determination of total heavy metals (dissolved Mn, Fe, Zn and Fe) according to APHA (2012).Heavy metal concentrations in both the water and sediment were compared to the limits established by Brazilian environmental legislation (CONAMA Resolutions 357/2005 and454/2012, respectively).
Margalef richness, Shannon-Weaver diversity and Pielou evenness were calculated using the PRIMER 6.0 software program.Two-way analysis of variance (ANOVA) Iheringia, Série Zoologia, 113: e2023009 was used to test significant differences (p < 0.05) of ecological indexes, total and main species density between periods and sampling points.Kolmogorov-Smirnov test was run in order to test the normality of the data (Zar, 2010), with the aid of the Statistic 6 program.Agglomerative hierarchical clustering analysis was performed to identify spatial distribution patterns in the structure of the associations (Bray-Curtis similarity index) based on abundance data from the sampling points calculated using the PRIMER 6.0 program.Principal component analysis (PCA) was performed using the software PAST -Palaeontological Statistics, version 1.81 (Hammer et al., 2008) to analyze the influence of environmental variables on the distribution of the benthic fauna.Pearson's correlation matrix was used for the selection of the most significant environmental variables for these analyses.

RESULTS
Physicochemical characteristics of water.All abiotic water variables differed among the sampling campaigns, but differed relatively little among the sampling points (Figs 2A -D).Salinity was lowest in the post-dredging (25 to 29.5) and pre-dredging (28 to 29) periods, with values > 29 during dredging 1 and 2, reaching as high as > 33 in the latter period (Fig. 2A).Temperature varied little (27.5 to 29.7°C), generally with values < 28°C during dredging 1 and > 28.5°C during the other sampling campaigns (Fig. 2B).Dissolved oxygen ranged from 3.3 to 6.6 mg L -1 (Fig. 2C), with large spatial variations in the pre-dredging period, but not during the other campaigns; the highest dissolved oxygen values were found during dredging 1. PH remained around 8 for all campaigns, except during dredging 1, when pH was ~8.5 (Fig. 2D).
Granulometric composition.The sediment was generally dominated by sand in all periods, except at points 2, 4 and 6, which had a large silt content.Dredging 2 was the period that most stood out from the rest, with a reduction in the sand content at all points, except points 2 and 4, at which the sand content increased and the silt content decreased, and point 6, at which the clay content increased (Fig. 3).
Heavy metals in water and sediment.The largest concentrations of total iron in the water (~6 to 10 mg kg -1 ) occurred in the pre-dredging period at points 3, 4, 6 and 7, always remaining less than 4 mg kg -1 in the other samples (Fig. 4A).The concentration of dissolved iron was always < 0.07 mg kg -1 , except at point 4 in the pre-dredging period Iheringia, Série Zoologia, 113: e2023009 (Fig. 4B).Manganese concentrations were generally < 0.1 mg kg -1 during dredging 1 and 2 and generally > 0.15 mg kg -1 in the pre-dredging and post-dredging periods (Fig. 4C).Zinc concentrations were always < 0.1 mg kg -1 , except at point 4 in the post-dredging period (~0.5 mg kg -1 ) and a peak of 5.0 mg kg -1 at point 6 in during dredging 1 (Fig. 4D).
In the soil, highest concentrations of lead (Fig. 5A), nickel (Fig. 5D) and zinc (Fig. 5E) were found in the predredging period, especially at points 2, 4 and 6.The highest concentrations of copper (Fig. 5B) were found during dredging 1 at points 2 and 4. The highest concentrations of chromium (Fig. 5C) were found at point 2 during dredging 1 as well as at point 4 in the pre-dredging and dredging 1 periods.No large differences in arsenic concentrations (Fig. 5F) were found among the different periods.
Macrofauna.Macrofauna was present in 75% of the samples, always with a small number of species as well as low density and diversity (Figs 6AD).Nine taxonomic Phylum were found, among which we identified 21 species of polychaetes, five mollusks, four crustaceans and one ophiuroid.The other groups were rare and not identified on lower taxonomic levels (Tab.I).The vast majority of individuals did not show high density and this was not commom to all sampling campaigns.A total of 46 different taxa belonging to nine major taxonomic Phylum were collected, these 40 taxa occurred in only one or two samples (Tab.I).The dominant organisms were Lumbrineris sp. and Oligochaeta, accounting for 28.5 and 16.2% of the total macrofauna, respectively, but even these organisms were found in only 15.5% of the samples (Tab.I).
The number of species in each sample never surpassed seven, with higher values in the pre-dredging period and the lowest during dredging 2, when the number of species never surpassed three.Spatially, the number of species was consistently lower at points 3 and 5 in all periods (Fig. 6A).Density of organisms was generally low -typically < 100 individuals in all periods, with peaks of 35 to 55 individuals at points 2 and 4 in the pre-dredging and dredging 1 periods (Fig. 6B).Shannon's diversity index was always < 2, with particularly low values during dredging 1 and 2 (typically lower than 1 and 0.7, respectively) (Fig. 6C).
Despite a certain tendency toward reductions in density, the number of species and the Shannon diversity during the dredging periods, with a subsequent increase in the number of species and Shannon index in the post-dredging period, no significant differences were found due to the considerable variability among sampling points (Tab.II).The highest density of organisms was found at point 4 during all periods except the post-dredging period, when point 8 had the highest abundance.Point 2 stood out in the pre-dredging and dredging 1 periods, whereas point 6 stood out in the dredging 2 and post-dredging periods.At points 3 and 5, which were used for the discarding of the dredged material, density was low, especially during the dredging activities, when no organisms were found at these sites (Fig. 6B).No significant differences in density were found among the sampling periods (df= 3; F = 1.0; p = 0.392) (Tab.II).Point 4, which was located near the mangroves of the estuary, was dominated by Polychaeta, Oligochaeta and Nematoda, with the polychaete Lumbrineris sp. the dominant species in the area sampled.In contrast, Bryozoa, Cnidaria and Echinodermata had few representatives and occurred at points 3, 5 and 7, which were the most disturbed.Point 3 and 5 were the discarding sites and point 7 was located in the navigation channel, which has high hydrodynamics.
The dendogram shows that points 6 and 8 were the most similar (73.9%), followed by points 3 and 7 (73.4%)and points 2 and 4 (70%).Above 40%, we may consider the formation of two large groups (Fig. 7) The PCA explained 64.24% of the variation among the samples (Factor1 = 39.24% and Factor 2 = 25.00%).Silt and heavy metals in the sediment (copper, chromium, nickel and zinc) were positively correlated with the dredging 2 period.Sand was negatively correlated with these metals in the sediment during the pre-dredging period.Manganese in the water was positively correlated with iron and pH was negatively correlated with temperature (Tab.III; Fig. 8).Iheringia, Série Zoologia, 113: e2023009

DISCUSSION
Significant differences in environmental variables among the dredging periods do not correspond to the causal agents of changes in microbenthic communities.However, the removal of sediment generally leads to a reduction in the abundance and diversity of organisms, exerting an influence on the structure of the communities (Ceia et al., 2013).
An increase in silt occurred during the dredging periods at nearly all sampling points.A reduction in the size of the sediment particles can alter the composition of the community, exerting a direct effect on species with requirements that are specific to the sediment type (Ceia et al., 2013).This is a general pattern in several regions throughout the world (Schettini et al., 2002;Xu, 2014;Rehitha et al., 2017).
After dredging, the characteristics of the sediment were similar to those found in the pre-dredging period, demonstrating that depositional environments achieve a balance with the governing environmental conditions of these locations before 120 days after the last dredging period.This factor plays an important role in the dynamics of the sediment (Bellotto et al., 2009), despite the high hydrodynamics of the region.
Among the heavy metals found in the water, manganese in the pre-dredging and post-dredging periods and zinc at point 4 in the post-dredging period were above the limits permitted by Brazilian legislation (CONAMA Resolution 357/05).The high concentrations of manganese at the sampling points may be related to the port cargo, as this mineral is the main product that circulates in the loading activities of the São Luís Port Complex (Amaral & Alfredini, 2010).
The higher concentrations of heavy metals at points 2, 4 and 6 are related to the granulometric composition.These sites are near mangroves and consequently have larger amounts of silts, suggesting the greater adsorption of these metals (Faraco & Lana, 2003) and the consequent reduction in the benthic fauna, as metals are determinant factors to the reproductive success and mortality of invertebrates (Ellis et al., 2017).The force of the tides and velocity of the currents are low in these locations.This probably favors the deposition of fine sediments and organic matter, which have greater capacity for the adsorption of heavy metals (Siqueira & Aprile, 2012).Despite the presence of these metals in the study area, the concentrations were within the limits permitted by CONAMA Resolution 454/2012.
A significant reduction in organisms was found in the dredging 2 period.Dredging activities are generally accompanied by reductions in the number of species, population density and the biomass of benthic organisms (Froján et al., 2011;Ceia et al., 2013;Katsiaras, 2015).However, there are records of increases in Polychaeta and Crustacea (Bemvenuti et al., 2005;Vivan, 2009).
The highest densities of organisms were also recorded at points 2 and 4. Environments with fine particles are favorable to the establishment of benthic populations (McLachlan & Brown, 2006).This type of substrate offers larger proportions of organic matter and facilitates the locomotion of organisms (Knox, 2001;Levinton, 2001).
The reduction or absence of organisms at points 3 and 5 during the dredging activities is probably due to the fact that these points are discard sites, leading to the burying of organisms and subsequent death by asphyxiation (Schratzberger et al., 2000).Previous studies have reported the immediate effect of the dumping of dredged material on benthic assemblages, with a reduction in the total abundance of individuals (Cruz- Motta & Collins, 2004;Powilleit et al., 2005;Witt et al., 2004).
However, the recovery time of affected areas depends on the magnitude and frequency of disturbance events (Lundquist et al., 2010).As the communities inhabit fine sediments, they generally recover faster than reef communities of sand, gravel or coral, which are more prone to the migration of opportunistic species (Newell et al., 1998).
The largest number of species was found in the pre-dredging and post-dredging periods, which explains the higher Margalef and Shannon-Weaver indices in these periods.The recovery of the benthic macrofauna in the post-dredging period has previously been recorded in terms of density and diversity.Nonetheless, dredging leads to the decline of more sensitive species and their replacement by more tolerant species (Cruz-Mota & Collins, 2004;Ceia et al., 2013).
The study area has extremely high hydrodynamics that can form dunes up to four meters in height that are subsequently displaced to other locations (Amaral et al., 2003).The disturbance caused by dredging and the high hydrodynamics hinder the migration and settlement of microbenthic juveniles in this location.The recovery of benthic communities in disturbed environments is associated with the migration of opportunistic species, juveniles and larval recruitment (Faraco & Lana, 2003;Egres et al., 2012;Gern & Lana, 2013;Sandrini-Neto & Lana, 2014).
The cluster analysis showed that points 6 and 8 had the greatest similarity.This finding apparently is directly related to the equal abundance and distribution of individuals in the sampling periods.These points are located closer to land and are consequently more protected, with low hydrodynamics and composed of finer sediments, which favors the establishment of benthic populations (Paiva et al., 2005).In contrast, points 3 and 7 had the smallest number of individuals and greater heterogeneity among the species.These points are in the central area of the channel and are consequently more prone to local disturbances.A similar situation has been reported near the navigation channel and mooring of the ships, with the occurrence of greater sedimentation suppressing the local fauna (Lana et al., 2001).
The PCA suggested/indicated a positive correlation between silt and heavy metals in the sediment.A similar situation has been described along the coast of the state of Rio de Janeiro, where positive correlations were found between a reduction in grain size and the occurrence of Pb, Cr, Ni, Cu and Co (Cabrini et al., 2016).It is likely that this correlation is related to fine sediment, in which Lumbrineris sp., I. pulchella and Micronephtys sp. are generally more abundant; this type of substrate also favors the fixation of metals (Faraco & Lana, 2003).Lumbrineris sp. and I. pulchella are surface deposit-eating species, whereas Micronephtys spp.are carnivorous and highly mobile (Fauchald & Jumars, 1979;Jumars et al., 2015).
Dredging activities altered the structure of the benthic assemblages, leading to reductions in the density and diversity of the organisms, followed by their recovery after the cessation of the dredging activities.Despite this recovery, the species were not all found throughout the pre-dredging to the post-dredging period, occurring sporadically in all campaigns, with the exception of Lumbrineris sp.This study could serve as the basis for future studies on the dredging area, considering the importance of the location as the second largest port with a natural depth in the world, where the maintenance of large cargo ships and navigation through the port area cause considerable changes to the composition and functioning of the local benthic communities.

Fig. 1 .
Fig. 1.Map of the location of Port Complex of São Luís, Maranhão, Brazil, indicating the eight sampling points.

Fig. 3 .
Fig. 3. Temporal and spatial variation of different granulometric size fractions contribution (%) to the sediment total weight at São Luís Harbor, Maranhão, Brazil.The number below the x-axis indicate the sampling stations.

Fig. 4 .
Fig. 4. Temporal and spatial variation of total iron (A), dissolved iron (B), manganese (C) and zinc (D) concentrations (mg kg-1) in the sub superficial water at São Luís Harbor, Maranhão, Brazil.The thick black bar indicates the maximum allowed by resolution 357/05.

Fig. 6 .
Fig. 6.Number of species, density and diversity of Shannon of the benthic macrofauna found in the Port Complex of São Luís, Maranhão, Brazil: (A) Number of species, (B) Density, (C) Shannon diversity and (D) Lumbrineris sp.
Does dredging activity exert an influence on benthic macrofauna ... Does dredging activity exert an influence on benthic macrofauna ... Summary of the ANOVA testing for differences in the number of species, Shannon diversity, total density and the dominant species abundance (ind/m²) considering the temporal (4 levels) and spatial (8 levels) factors in the São Luís Port Complex, Brazil.Differences are considered significant if p<0.05.DF = degree of freedom; SS = sum of squares; MS = mean squares; F = parameter of the ANOVA; p = probability associated to the test.