Marine Pollution Bulletin 104 (2016) 70–82 Contents lists available at ScienceDirect Marine Pollution Bulletin j ourna l homepage: www.e lsev ie r .com/ locate /marpo lbu l Using an integrated approach to assess the sediment quality of an estuary from the semi-arid coast of Brazil Ivanildo Surini Souza a,b,⁎, Giuliana Seraphim Araujo c, Ana Carolina Feitosa Cruz c, Tainá Garcia Fonseca c,d, Julia Beatriz Duarte Alves Camargo c, Guilherme Fulgêncio Medeiros e, Denis M.S. Abessa a,c a Ceará Federal University— UFC, Institute of Marine Sciences, Av. Abolição, 3207, Fortaleza, CE 60165-081, Brazil b Rio Grande do Norte Federal Institute for Science and Technology Education — IFRN, Av. Senador Salgado Filho, 1559, Natal, RN 59015-000, Brazil c São Paulo State University— UNESP, Praça Infante Dom Henrique, s/n., São Vicente, SP 11330-900, Brazil d Centre for Marine and Environmental Research — CIMA, Faculty of Sciences and Technology (FCT), University of Algarve, Campus de Gambelas, Faro 8005-139, Portugal e Federal University of Rio Grande do Norte — UFRN, Campus Universitário Lagoa Nova, 1524, Natal, RN 59078-970, Brazil ⁎ Corresponding author at: Ceará Federal University—U Av. Abolição, 3207, Fortaleza, CE 60165-081, Brazil. E-mail address: ivanildo.surini@ifrn.edu.br (I.S. Souza) http://dx.doi.org/10.1016/j.marpolbul.2016.02.009 0025-326X/© 2016 Elsevier Ltd. All rights reserved. a b s t r a c t a r t i c l e i n f o Article history: Received 29 August 2015 Received in revised form 8 January 2016 Accepted 1 February 2016 Available online 15 February 2016 The Jundiaí–Potengi Estuary (JPE) on the semi-arid coast of Brazil is influenced by multiple sources of pollution. Sediment quality at 10 JPE sites was evaluated through an integrated approach. Rainy and dry seasons were considered. Collected sediments were analyzed for texture, metal, nitrogen, phosphorus concentrations, and toxicity to invertebrates. Geochemical and ecotoxicological data were integrated using qualitative approaches and multivariate techniques. We observed decreased sediment quality in both seasons, particularly in the mid- estuary. In the dry season, the contamination–toxicity relationship was clearer, as hydrological conditions favor contaminant retention within the estuary. Rainy season conditions were found to be worse, since stormwater drainage from agricultural and urban areas carries the contamination into the estuary. Because of the contamination sources and dissolved and particle-bound metal transport, contamination and toxicity did not correlate as clearly in the rainy season. The results suggest that unmeasured contaminants are contributing to JPE sediment degradation. © 2016 Elsevier Ltd. All rights reserved. Keywords: Geochemistry Contamination Toxicity Semi-arid coast Sediments 1. Introduction Themajority ofworld's population inhabits coastal areas. As a conse- quence, the natural environments of these areas have been continuous- ly altered and replaced with industrial facilities, ports, aquaculture ponds, agricultural fields, and urban expansion (Diegues, 2001; Chen et al., 2004; Marshall et al., 2010; Souza and Silva, 2011). Rapid popula- tion growth, the disordered occupation of coastal areas, and an econom- ic model based on the consumption of natural resources have all caused the deterioration of these areas. The discharge of chemicals into the environment is one of the main threats to coastal and marine ecosys- tems. These pollutants include nutrients, pesticides, metals, detergents, oil, plastics, pharmaceuticals and personal care products, among others (Petrovic et al., 2003; Marins et al., 2004). Despite the advances in environmental legislation to regulate emis- sions and reduce pollution, and in spite of the frequent insistence among scientists for the need to protect coastal zones, the release of contaminants into the sea and coastal water bodies continues, and FC, Institute ofMarine Sciences, . many people and governments still believe that the world's coastal water bodies are capable of diluting contaminants to safe levels for both humans and biota (Zagatto and Bertoletti, 2008). This scenario has become a very problematic situation, especially in developing coun- tries, where the establishment of new economic activities is often combined with ineffectiveness and inefficiency of their respective resi- due treatment systems and thus represents an emerging challenge to sustainable development (Choueri et al., 2009a; Torres et al., 2009). Within the coastal zone, estuaries have been widely recognized as some of the most important and productive environments on the plan- et, as they provide different ecosystem products and services (Costanza et al., 1997; Savage et al., 2012). However, estuaries receive both the natural influences of continental terrains and that of human activity. Although estuarine degradation is a matter of global concern, the evalu- ation of the impacts on these environmental has not been an easy task (Chapman and Wang, 2001; Zonta et al., 1994, 2007; Elliott and Quintino, 2007), largely because estuaries may be susceptible to chemicals of different natures, and also because of estuaries high envi- ronmental instability. Chemicals introduced into estuarine environments are influenced by a set of physical, chemical, and biological processes thatmay affect their fate and behavior (Chapman et al., 1999). Metals represent substances http://crossmark.crossref.org/dialog/?doi=10.1016/j.marpolbul.2016.02.009&domain=pdf mailto:ivanildo.surini@ifrn.edu.br http://dx.doi.org/10.1016/j.marpolbul.2016.02.009 www.elsevier.com/locate/marpolbul 71I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 of special interest because they cannot be destroyed and may persist in the environment (TamandWong, 2000; Nicolau et al., 2006; Yang et al., 2014). After settling in sediments andwaters, metals can be incorporat- ed by the biota and easily spread along the food chain; during this process, these contaminants may have toxic effects on a wide range of organisms. Most contaminants that are released into estuaries accumulate in the sediments (Bartoli et al., 2012); thus, sediments become not only a repository but also a source of contaminants for the water column and the biota (Adams et al., 1992; Nipper, 1997; Delvalls et al., 2004; Burton and Johnston, 2010). The retention of contaminants in the sedi- ments, their bioavailability, and their potential toxicity are all strongly influenced by environmental factors, such as grain size distribution, salinity, pH, redox potential, and levels of organic matter. In addition, these environmental factors are influenced by winds, tides, freshwater input, bioturbation, and other aspects that characterize natural estua- rine dynamics (Chapman and Wang, 2001; Pekey, 2006; Idris, 2008). Because sediments tend to integrate environmental variations over time, they can be used as an appropriate environmental compartment in environmental assessments. Many studies on sediment quality have been conducted and have provided information on the effects of sedi- ment contaminants on aquatic organisms and ecosystems (Araújo et al., 2009; Cesar et al., 2009; Ré et al., 2009; Langston et al., 2010; Du et al., 2012; Gonçalves et al., 2013; Roig et al., 2015). In Brazil, investiga- tions into sediment quality have been concentrated in some industrial and port zones of the southern and southeastern regions (Carvalho et al., 2002; Machado et al., 2002; Abessa et al., 2005; Pusceddu et al., 2007; Torres et al., 2009; Choueri et al., 2009a; Buruaem et al., 2013a; Fonseca et al., 2013; Rodrigues et al., 2013; Zalmon et al., 2013). On the other hand, studies conducted on the northeastern region of the country are still scarce (Buruaem et al., 2013b; Nilin et al., 2013; Krull et al., 2014), despite the ecological importance of this region to the bio- diversity of the South Atlantic. The semi-arid coast is located in the northeastern region of Brazil, between the states of Piauí (PI) and Rio Grande do Norte (RN). It includes the Jundiaí–Potengi Estuary (JPE), which is the largest andmost important in RN state. In spite of its socio- economic and ecological importance, this estuary has been exposed to a variety of anthropic pressures, which include the discharge of untreated industrial and domestic effluents (Souza and Silva, 2011), runoff from agricultural areas, and discharges from shrimp farm effluents. Little is known about the sediment quality of this estuary (Buruaem et al., 2013b). The objective of this investigation was to consider both the dry and rainy seasons in order to assess the sediment quality of an estuary from the semi-arid coast of northeastern Brazil (JPE), which is influenced by multiple sources of contamination. To achieve this objec- tive, different lines of evidence (LOEs), including geochemical and eco- toxicological analyses, were employed. 2. Materials and methods 2.1. Study area The JPE is located on the eastern sector of the RN coast in northeast- ern Brazil, between the 5°53′S and 5°43′S latitudes and 35°21′W and 35°09′W longitudes (Fig. 1) (Souza and Silva, 2011). The estuary pre- sents a maximum depth of 15 m and typical marine influence, in which the tidal fluxes range from 5000 to 20,000 m3·s−1 (Silva et al., 2001; Boski et al., 2015). Freshwater input comes from the Potengi, Jundiaí and Doce Rivers; the Potengi River is the main contributor to the estuary, draining a basin with 3180 km2 and flow of 5 m3·s−1 dur- ing the rainy period. The Jundiaí River has an intermediate flow but is more heavily influenced by tides. The Doce River presents the smallest freshwater contribution; its mean flow remains at about 2m3·s−1 for most of the year (Silva et al., 2006). The climate in the region is characterized as tropical and semi-arid, with a dry season (September to February) that has a mean rainfall rate of 220 mm, and with a rainy period (March to August) during which themean rainfall rate is 1390mm. The annualmeanprecipitation rates range from 1300 to 2000mm (Silva et al., 2007; Boski et al., 2015). The JPE is approximately 30 km long, and its basin includes the cities of Macaíba, São Gonçalo do Amarante, and Natal, which have a com- bined population ofmore than 1.4million people (IBGE, 2014). Approx- imately 60% of the raw sewage fromNatal is discharged directly into the JPE; in addition, the estuary receives effluents from several industrial sources, such as textile factories, food and beverage producers, pulp mills, and leather and tannery manufacturers (Silva et al., 2006; SEPLAN, 2013). The estuary also receives effluents from shrimp farms and from the dumping sites where residues from urban septic tanks are stored and treated (IDEMA, 2008). 2.2. Sediment sampling Two sampling surveys were conducted from which 10 sampling sites distributed along the JPE were considered (Fig. 1). The first survey occurred in May 2013 (the rainy season); the accumulated rainfall in that month was 399.1 mm. The second survey was performed in December 2013 (the dry season). The rate of precipitation for that month was 9.8 mm, and the accumulated precipitation for 2013 was 1846.7mm, according to EMPARN (2013). Sediments from theGalinhos Estuary (150 km northwest of the JPE) were collected to be used as reference sediments; this estuary is not impacted. The sediment collection followed the recommendations described by Burton (1992). Composite sediment samples were collected from each site (with at least 3 subsamples) through the use of a stainless steel Van Veen grab sampler. From thematerial retained in the sampler, only the first 5 cm of the surface layer was separated. The sediments were transferred to plastic trays, thoroughly homogenized, and split into aliquots. The aliquots to be used for toxicity tests were conditioned in polyethylene flasks and stored at 4 °C in the dark until the assays were performed. The aliquots for the metal, organic carbon, and grain size distribution analyses were kept in polyethylene flasks and stored at−20 °C. 2.3. Geochemical analyses The sediment samples were dried at 45 °C for 5 days, and aliquots were then separated for the following analyses: grain size distribution, organic matter (OM) contents, concentrations of total nitrogen (N) and phosphorus (P) and metal concentrations (Fe, Mn, Cd, Cr, Cu, Pb, Ni, and Zn). 100 g sediments were used to assess grain size distribu- tion, in which quantities of mud (b0.063 mm) and sand (N0.063 mm) were determined (ABNT, 1988). OM levels were measured using the volumetric method described by EMBRAPA (1998), which is an adapta- tion of the Walkley-Black (1965) method. Concentrations of N and P were measured using the colorimetric method (Grasshoff et al., 1999). For the chemical analysis, 5 g of the fine fractions (b0.063mm) from the sediments were dried and digested using a mixture of HCl 0.05 M and H2SO4 0.0125 M (EMBRAPA, 1998). The extracts were analyzed via atomic absorption spectrophotometry (model: Varian Spectr-AAS- 220-FS). The spectrophotometer was calibrated based on the reading the absorbance of six standards prepared for each element. The analyt- ical precisions were established by analyzing a certified sediment (NIST 1646-A); the recoveries ranged from 80.7 to 114% (see supplementary material), values which are considered acceptable, and their uncer- tainties were below the acceptable limits (between 7% and 18%). Metal concentrations in the JPE sediments were compared to those ob- tained at the reference site, and a risk quotient (RQ) was established based on the ratios between these concentrations (Roig et al., 2015). This quotient aims to evaluate both the pollution load and the potential risk to the biota as a result of the contribution of the eight elements measured, by defining four risk categories: low risk (RQ b 1), moderate Fig. 1.Map of the study area and position of the sampling sites. 72 I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 risk (1 ≤ RQ b 3), considerable risk (3 ≤ RQ b 6), and very high risk (RQ ≥ 6) (Loska et al., 1997; Islam et al., 2015). Due to the considerable anthropic interferences in the study area, the evaluation of sediment contamination wasmade using the percent- age enrichment factor (%EF) defined by Zonta et al. (1994) and further used by Loska andWiechuła (2003). The percentage enrichment factors (EFs) were calculated according to the following equation: EF %ð Þ ¼ C−Cminð Þ= Cmax−Cminð Þ½ � � 100 ð1Þ where C indicates the mean concentration of the concerned element, Cmin and Cmax indicate the respective minimum and maximum con- centrations determined during the period of investigation. To evaluate themetal load at each site, the EFs of all of the elements were added to- gether, as suggested by Adamo et al. (2005). 2.4. Sediment toxicity Sediments were tested for acute toxicity (AT) and chronic toxicity (CT), in which organism exposure to whole-sediment (WS) and sediment–water interface (SWI) was considered. For all toxicity tests, physical and chemical parameters — which included pH, salinity, dissolved oxygen (DO), and temperature—were determined at the be- ginning and end of each experiment. The original tables containing this information can be seen in the supplementary material. 73I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 2.4.1. Whole-sediment acute toxicity The whole-sediment acute toxicity tests were conducted using the amphipods Leptocheirus plumulosus and Tiburonella viscana and follow- ing the protocols described by ABNT (2008) and Melo and Abessa (2002), respectively. T. viscana specimens were collected from the Engenho D'água Beach (Ilhabela, São Paulo, Brazil) and were then accli- mated to laboratory conditions over 3 days. Sediment from this beach was collected to be used as internal control. L. plumulosus specimens were obtained from a culture maintained in laboratory. The tests consisted of exposing the amphipods (20 juvenile L. plumulosus specimens and10 adult T. viscana specimensper replicate) to the sediments for a 10–day period. Test chambers consisted of polyethylene flasks containing approximately 200 ml of homogenized sediment and filtered sweater (salinities of 20‰ for L. plumulosus and 34‰ for T. viscana). The system was kept under constant lighting and aeration and at a temperature of 25 ± 2 °C. At the end of the test, the contents of each test chamberwere sieved, and the surviving organisms were counted. Missing organisms were considered dead. Three repli- cates were used for each sample. 2.4.2. Whole-sediment chronic toxicity The copepodNitocra sp.was used as the test organism for thewhole- sediment chronic toxicity tests, based on the protocol developed by Lotufo and Abessa (2002). The copepods were obtained from a culture kept in the laboratory. Four replicates were set up for each sample, and 15 ml of high density polyethylene test chambers filled with 2 ml of sediment and 8 ml of filtered sea water (salinity 17‰) were used. Ten healthy ovigerous females were introduced into each replicate. The entire test system was incubated at 25 ± 2 °C with a 12 h:12 h (light:dark) photoperiod for 10 days. Next, the content of each replicate wasfixedwith formaldehyde (10%) and Rose-Bengal dye (0.1%). Finally, the adult females and their offspring (nauplii and copepodits) were counted using a stereomicroscope. 2.4.3. Chronic toxicity of the sediment–water interface The sediment–water interface chronic toxicity test was conducted following the method described by Anderson et al. (2001) and adapted by Cesar et al. (2004) for small volumes. This treatment assesses the effects of contamination that arises from sediment andwhichmay affect organisms in the adjacent water column. In this procedure, the test system was set up in test tubes containing sediment and water 1:4 (v:v).The samples were then tested for toxicity by analyzing the embryo-larval development of the sea urchin Lytechinus variegatus ac- cording to ABNT NBR protocol No. 15350 (ABNT, 2012). Sea urchin spawning was induced and subsequent in vitro fertilization was imple- mented. The test was conducted by introducing approximately 400 em- bryos in each of the four replicates, as well as in a negative control (filtered seawater). After the test (24 h), embryoswere analyzedmicro- scopically for morphological abnormalities and delayed development. 2.5. Interpretation and integration of the ecotoxicological data The results of all toxicity data were checked for normal distribution using the Chi-Square test. Variance homogeneity was assessed using Table 1 Criterion for classifying the sediment quality in the Jundiaí–Potengi Estuary based on the toxic Test type Endpoint Species Acute % mortality L. plumulosu T. viscana Chronic fecundity ((nauplii + copepodits)/female) Nitocra sp. % abnormal development L. variegatus NT: not significantly toxic in relation to the controls. a Mortality below 50%, but significantly different from the reference sediment. b Significantly toxic (in comparison with the controls) but the difference from the control g Fisher's exact test. Student's t-test was then used to compare each sam- ple to its respective control. Sediments were considered significantly toxic when the value for the respective endpoint (mortality, fecundity, embryo development)was lower than the value observed in the control (e.g. when p ≤ 0.05). The analyseswere run using the STATISTICA 7 soft- ware tool. The results of all of the testswere then combined, and the qualitative conclusions of each test were considered. The criteria for classifying the sediments based on their toxicities are shown in Table 1. For the amphi- pod tests, non-toxic sediments were considered good, and the signifi- cantly toxic sediments were classified as poor (b50% difference from the control) or very poor (≥50% in commonwith the control). A similar criterion was used in the copepod test. Meanwhile, for the sea-urchin embryo test, there were four classes (good: not toxic; moderate: devel- opment inhibition rates ranging from 30 to 49%; poor: development in- hibition rates between 50% and 74%; very poor: development inhibition equal or greater than 75%). Finally, to determine the sediment quality at each site based on the combination of toxicity tests, the results regard- ing acute and chronic toxicity were combined in order to produce five possible sediment quality classes (Fig. 2). Because acute toxicity gener- ally indicates severe responses, our approachwas conservative and gave more weight to the results of acute toxicity. 2.6. Integration of geochemical and ecotoxicological data Geochemical and toxicity data were integrated using cluster analy- ses (CAs), with the Euclidean distance and the Ward's method, and also using factor analysis with data extracted with the principal compo- nent analysis (FA–PCA). The data matrix used for these analyses was comprised of the results on OM, muds, Nitrogen, Phosphorus, and metals (Fe, Mn, Cd, Cr, Cu, Pb, Ni, Zn) concentrations, amphipodmortal- ity, reduction in copepod fecundity, and the abnormal development rate of sea-urchin embryos. In the FA–PCA, we used 0.4 as the cut-off value (Comrey and Lee, 1992), which is equal to or higher that the criteria used by Choueri et al. (2009a, 2009b, 2010) and Rodrigues et al. (2013). The selection of the number of principal components was based on the Scree plot method, and the analysis considered the nor- malized Varimax rotation. Prior to both the CAs and the FA–PCA, the data was auto-scaled in order to reduce the magnitude differences between variables. 2.7. Quality assurance/quality control (QA/QC) The QA/QC procedures included the use of replicates and repeatabil- ity tests in the analyses of total N and P, as well as the use of analytical blanks and standard reagents. In the case of metals, the calibration curve was adjusted using linear regression, and the curves obtained for each element showed the relationships between the absorbances and the concentrations of the known solutions. Method validation included the analysis of a standard sediment (NIST 1646-A). The analyt- ical precisions were within the acceptable limits for uncertainty and ranged from 7% to 18%. In the ecotoxicological tests, the experimental variables (pH, DO, temperature, salinity, and luminosity) were moni- tored. Tests with reference substances were run for each species or ity to marine/estuarine invertebrates. Sediment classification for toxicity Good Moderate Poor Very poor s NT – b50%a ≥50% NT – b50%b ≥50% NT 30–49% 50–74% N75% roup is less than 50%. Fig. 2. Classification of sediment samples from the Jundiaí-Potengi Estuary in the rainy and dry seasons based on the combination of the conclusions obtained for each individual toxicity test (amphipod mortalities, inhibition of copepod reproduction, and reduction in normal sea urchin embryo development). 74 I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 survey in order to evaluate the sensitivity of the test organisms. Tests were used to determine L. plumulosus and T. viscana sensitivities to zinc sulfate and potassium dichromate, respectively. The LC50-48 h for T. viscana was estimated to be 8.2 mg·L−1 (6.25–9.37 mg·L−1 K2Cr2O7), while the LC50-96 h for L. plumulosus was estimated to be 0.89 mg·L−1 (0.67–17 mg·L−1). Both values were within the accept- able ranges defined by the respective control charts.Nitocra sp. sensitiv- ity toK2Cr2O7was determined aswell, and the LC50-96 hwas estimated to be 26.92 mg·L−1 (16.25–33.33 mg·L−1, which is within the accept- able range. Finally, L. variegatus sensitivity to zinc sulfatewas estimated, and EC50-24 h values ranged from 0.20 to 0.43 mg·L−1, values which were within the range established in the control chart. 3. Results and discussion 3.1. Sediment properties The results of the geochemical characterization of the sediment sam- ples are summarized in Table 2. The sediment textures along the estuary were heterogeneous overall, particularly in the second survey (dry sea- son). Fine sedimentswere predominant in themid-estuary (P4–P7) and in the lower estuary (P8–P10). This high percentage ofmud is an indica- tion of the low hydrodynamic energy in these portions of the JPE, as is the presence of a dense mangrove forest, which increases fine particle retention. In addition, the narrow mouth of the JPE may contribute to the siltation process within the estuary. The quantities of OM in the sediments ranged from 0.05 to 12.67%. The highest values were observed during the dry season, possibly find- ing which may be due to the lower turbulence and higher deposition rate during this period. In both sampling campaigns, the highest levels of OM occurred in the mid-estuary (P4–P7). However, all along the JPE, OM levels were within the range expected for tropical estuaries from northeastern Brazil (0.76–38.9%) (Freire et al., 2004; Lacerda and Marins, 2005; Marques et al., 2008; Nascimento et al., 2010). The distri- bution of OM in the sediments presented a pattern similar to that exhib- ited by thefine sediments, a findingwhich reinforces the possibility that the lower and mid-estuarine zones are depositional areas. Moreover, in these portions of the JPE, both human activity and natural sources may be contributing to the increase in OM levels. OM input to the JPE is influ- enced by the seasonal population increase resulting from tourism, espe- cially during the dry season. In addition, effluents and residues from the shrimp farms are continuously released into the JPE. There are 61 shrimp farms in the vicinity of the JPE basin; they cover approximately 1440 ha (Medeiros, 2009), and aremost frequent along the banks of the mid- and lower-estuary. 3.2. Nutrients (total nitrogen and phosphorus) Phosphorus concentrations were highest in the internal portion of the estuary, and they decreased progressively as the sites became closer to the mouth of the JPE. The P2 and P6 sites presented the highest con- centrations in both seasons. In general, the concentrations were higher during the rainy season.When nitrogen levels were assessed, there was no clear pattern for the element's distribution in the sediments in either season, but the concentrations tended to be higher during the rainy sea- son. In the dry season, sediments from themid-estuary (P4 and P6) and from the lower estuary (P8–P10) presented the highest concentrations, particularly those from P8 (2580 mg·kg−1). P8 is close to the mouth of the Baldo Channel, which carries a large amount of untreated sewage and other domestic residues into the JPE (Silva et al., 2001). The relatively high levels of nitrogen and phosphorus in the sedi- ments from P2 and P7, particularly in the first campaign,may be a result of leakage from agricultural areas or urban drainage during rainstorms. According to Singh et al. (1997) and Walker et al. (1999), urban drainage contributes to pollution loads in estuaries that cross urban areas. Nitrogen and phosphorus are important nutrients for organisms, but they can be introduced into coastal environments through sewage and urban effluents (Mackenzie and Chou, 1993), and high values can cause eutrophication. Tavares et al. (2014) observed the phenomenon of eutrophication in the JPE, which was dependent on tidal conditions and rainfall precipitation levels. Shrimp farms also represent important sources of nitrogen and phosphorus for the JPE; large amounts of fertil- izer and shrimp food are employed to accelerate shrimp growth (Lacerda et al., 2006a; Silva et al., 2010; Marins et al., 2011). Thus, we can infer that there are multiple sources of N and P contributing to the JPE. Table 2 Geochemical variables (percentage of organic matter, mud, nitrogen, phosphorus and metals) of the sediment samples collected in the Jundiaí–Potengi Estuary and in the reference site (Galinhos Estuary) during the rainy and dry seasons. Sampling Sites Geochemical analyses N P Mn Cr Cu Cd Ni Pb Zn Fe OM Mud (mg·kg−1) (%) Rainy season P1 340 17 21.74 b0.01 0.90 0.02 0.86 1.29 2.47 0.569 0.59 12.7 P2 1340 175 9.26 b0.01 7.46 0.15 3.58 6.51 30.17 0.598 3.15 23.6 P3 1120 85 9.65 b0.01 3.81 0.12 2.31 3.05 6.30 0.443 4.43 32.2 P4 280 136 23.39 0.27 3.08 0.19 2.21 3.30 11.36 0.611 5.53 36.7 P5 1680 113 15.00 0.74 2.42 0.25 2.82 2.87 10.41 0.392 6.22 39.5 P6 900 117 52.62 0.37 2.72 0.22 1.83 2.44 8.68 0.494 4.57 34.7 P7 1230 29 22.57 0.51 1.82 0.37 2.18 3.12 13.23 0.281 5.04 34.6 P8 950 2 8.16 0.64 6.63 0.26 1.29 4.74 26.22 0.471 3.12 17.9 P9 1060 1 22.96 b0.01 0.41 0.36 1.22 2.24 1.82 0.011 4.55 31.7 P10 780 1 18.36 b0.01 0.40 0.33 0.98 2.17 1.27 0.005 1.78 39.8 GAL 220 2 11.23 b0.01 0.48 0.25 1.11 1.24 1.45 0.007 3.72 30.4 Dry season P1 340 9 78.50 b0.01 1.63 b0.01 1.76 1.05 2.53 0.579 0.35 17.6 P2 220 17 21.11 b0.01 0.29 b0.01 0.38 0.25 2.13 0.437 0.05 3.5 P3 170 47 10.35 0.26 17.90 0.08 1.56 1.85 4.96 0.253 2.18 18.9 P4 1960 141 98.60 0.93 2.46 0.38 4.14 3.92 14.46 0.655 11.38 67.8 P5 170 94 46.62 0.94 0.64 0.47 3.10 2.70 10.61 0.336 12.67 61.0 P6 1570 34 34.03 0.70 1.64 0.29 1.92 2.18 8.84 0.456 8.58 45.6 P7 390 1 21.32 0.39 0.40 0.35 1.24 1.96 3.67 0.054 4.04 40.5 P8 2580 1 29.33 0.53 0.65 0.49 1.51 2.45 2.21 0.005 6.39 69.9 P9 1010 2 15.48 0.42 0.42 0.36 1.06 2.02 1.61 0.010 4.98 58.4 P10 1120 1 20.90 0.41 0.43 0.35 1.07 1.79 1.25 0.005 3.04 46.3 GAL 140 2 12.55 0.42 0.46 0.25 1.11 1.06 1.19 0.008 3.46 31.1 GAL: Reference site — Galinhos Estuary northeastern Brazil. 75I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 Previous studies (Souza and Silva, 2011) showed that the region be- tween the cities of Natal and São Gonçalo do Amarante (close to P8, P9 and P10) corresponds to a portion of the estuary that has been increas- ingly degraded over the last few decades. According to theses authors, the main causes of degradation include urban expansion, the release of raw sewage, and the replacement of mangrove forests with shrimp farms and with anaerobic ponds from sewage effluent plants; these sources explain the high levels of nitrogen that were found in the lower JPE in the current study. 3.3. Metals Most of the metal concentrations found in the sediments were higher in the rainy season, with the exception of Mn, Cd, and Cr (see Table 2). During the rainy season, the higher concentrations tended to occur in sediments from P2–P8 (sites which represent almost the entire length of the estuary). Meanwhile, in the dry season, the highest levels of metals were observed in the sediments from P4–P6. The difference in levels between dry and rainy seasons suggests an influence of the drain- age from urban and agricultural areas on the distribution of metals along the JPE. Rainstorms in tropical areas are considered important for sustaining river flows and contribute to contaminant runoff from the surrounding areas (Nilin et al., 2013). Ambrozevicius and Abessa (2008) observed that storm water runoff and urban drainage have contributed to the degradation of water quality in some urban channels located in the Santos Bay (southeast Brazil). However, the long dry season on the semi-arid coast causes the riv- ers to be perennial only in their estuarine portions, since the freshwater input drops to minimum levels. Thus, the reduced river flow is not strong enough to reach the sea and remains blocked within the estua- rine zone by the marine waters (Lacerda et al., 2012), thus increasing the water's residence time in this region. Under these conditions, con- taminants tend to be retained within the estuary during the dry season, and only a small fraction is carried to the sea as dissolved metals. This phenomenon can explain the higher concentrations of metals in the intermediate portions of the JPE, especially in the sediments collected between P4 and P6 (Table 4). On the other hand, the exportation of contaminants toward the sea tends to occur predominantly during the rainy season, when the flow becomes strong enough to break the resis- tance imposed by marine waters (Lacerda et al., 2007, 2012). This explains, at least partially, the larger number of sampling sites affected by metal contamination. For this reason, it can be inferred that the presence of multiple contamination sources along the entire JPE do not support the idea of metal retention in the sediments from the sites located upstream. Many studies have reported that the physical and chemical proper- ties of surfacewaters also can regulate metal precipitation or solubiliza- tion and thus influence the mechanisms involved in the temporal geochemical variability of coastal sediments (Cooper and Morse, 1998; Warnken et al., 2001). Lau (2000) concluded that salinity and tempera- ture variations influenced the dynamics of metals through the sedi- ment–water interface in a subtropical estuary, thus increasing metal availability to the biota. There is a consensus that other factors, such as the redox potential and pH, may influence metal precipitation and mobilization in coastal sediments, since they alter the stability of some compounds involved in the contaminant retention process in sediments (Chapman andWang, 2001), as is the case of sulfides (Otero andMacias, 2002). However, these factors cannot be considered the only factors responsible for the changing behavior of metal concentrations in sedi- ments. Human activity must also be considered, since multiple point and diffuse sources are present along the JPE, and their contributions of metals vary over time, as observed by Guedes (2012). Marins et al. (2004) found a similar situation in other estuaries from northeastern Brazil. Metal concentrations in sediments from the JPE were lower than global geological reference levels (Turekian and Wedepohl, 1961) and were also lower than those adopted by the Brazilian government as standards for sediment dredging and disposal (CONAMA, 2012); these 76 I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 results are consistent with those obtained by Dantas (2009). The con- centrations were comparable to levels found in other estuaries of Brazil and lower than those observed around theworld (Table 3). Possi- ble reasons for relatively lower levels of nutrients and metals in JPE in comparison to other sites worldwide may include the fact that our study themetalswere extracted byweak acid digestion; and the region- al concentrations of these elements are low, as suggested by the results for the reference site and by previous studies in JPE (Sindern et al., 2007; Buruaem et al., 2013b). International sediment quality guidelines must be used with caution, since they may not represent the best basis for comparison (Marins et al., 2004). Abessa et al. (2008) observed that more than 75% of the sediments from the Santos Estuarine System that exhibited concentrations above the Canadian threshold effect levels (TELs) were toxic tomarine invertebrates, and these authors stated that the sediment quality guidelines (SQGs) for tropical regionsmay need to be lower than those of temperate zones. Choueri et al. (2009b) and Buruaem et al. (2012) showed that site-specific SQGs could be much more reliable for predicting toxicity than those adopted by the Brazilian legislation. Thus, we adopted risk quotients (Loska et al., 1997; Islam et al., 2015) and enrichment factors (Zonta et al., 1994) to evaluate the geochemical conditions of the JPE. Risk quotient (RQ) and enrichment factor (EF) values are shown in Table 4. Total EF values ranged from 16.9 to 67.2% during the rainy sea- son and were between 10.6 and 97.1% during the dry season. The most enriched sediments (%EF N 50) during the rainy season were P2 N P8 N P5 N P6, while in the dry season, the most enriched samples were those from P4 N P5 N P6. The RQ values indicated that the sedi- ments from sites P2–P8 were of considerable or very high risk during the rainy season, and that those from P4–P6 were of considerable risk (RQ ≥ 3) during the dry season. Results obtained for %EF and RQ were in agreement and presented similar metal accumulation patterns. The enrichment of metals in the sediments was clearly demonstrated, a re- sult which indicates the influence of human activity, particularly in the mid-estuary, where sediments were found to be of considerable or very high risk. The mid-estuary also coincides with the regions where deposition and accumulation of organicmatter, fine particles, and nutri- ents would be expected due to the hydrological regime. Many sources of pollution are established along the JPE, particularly near the mid-estuary. These include 26 factories representing different sectors (textile, food and beverages, pulp, and leather and tannery), and most of them discharge their effluents along the intermediate estuarine zone (IDEMA, 2008; Souza and Silva, 2011). The contribution of effluents from the textile factories is the most relevant source of pol- lution. Alencar et al. (2005) and Vandevivere et al. (1998) reported that their composition includes organic compounds (such as detergents), carbonates, sulfates and chlorides, and also metals (Zn, Ni, Cr, Cd, Pb, and Fe), among other substances. These effluents may be associated Table 3 Concentrations of metals (mg·kg−1) in sediments from different estuarine zones of the world Region Fe Mn Cr Jundiaí–Potengi Estuary (Brazil)1a 0.005–0.61 8.1–52.2 b0.01–0.74 Jundiaí–Potengi Estuary (Brazil)1b 0.005–0.65 10.3–98.6 b0.01–0.94 Potengi River (Brazil)2 0.47–0.6 – 7.2–20.8 Guaratuba Bay (Brazil)3 – – – Paranaguá Estuarine System (Brazil)4 – – 14,5–58 Parnaíba River Delta (Brazil)5 0.3–2.5 145–1356 1.5–38 Tapacurá River (Brazil)6 0.7 53.8 1.7 Port of Rotterdam (Netherlands)7 – – – Port of Cádiz (Spain)8 – – 0.1–14.9 Daya Bay (China)9 – – – River Ganges (India)10 – – 1.8–6.4 Toxicity reference value11 – – 26 World average12 4.7 850 90 References: 1a this study (rainy season), 1b this study (dry season), 2 Sindern et al. (2007), 3 Rod (2008), 7 Van Den Hurk et al. (1997), 8 Casado-Martínez et al. (2009), 9 Gao and Chen (2012), with enrichment of metals in the JPE sediments, particularly in the re- gion between P4 and P6. Metal contamination may be linked to the surrounding shrimp farms as well. This activity occurs close to the mid-estuary and the low estuary (Silva et al., 2007; Souza and Silva, 2011), and it is associat- edwith a series of contaminants, including copper-based fungicides and algaecides (Boyd and Massaut, 1999), as well as with shrimp feed, which presents high levels of Cu, Zn, and Mn (Lacerda et al., 2006b; Cunha, 2010). Therefore, the enrichment of metals in sediments from the JPE may be a result of a combination of human activity and natural factors. 3.4. Sediment toxicity Sediment toxicity tests have been widely used as a line of evidence (LOE) to evaluate the quality of sediments and the bioavailability of chemicals (Cesar et al., 2009). The combined use of different toxicity tests has been recommended by Abessa et al. (2008) in order to provide more reliable information on sediment quality. For this reason, we used 4 different species and considered both acute and chronic toxicities. As shown in Table 5, sediments from P1, P2, P6, P8, and P10 presented chronic and acute toxicities for at least one of the tested organisms. The sediments from P3, P4 and P9were chronically toxic. In the dry sea- son, sediments from P2, P3, and P6 presented only chronic toxicity. In both campaigns, there was not any sediment that showed only acute toxicity — as expected, more samples presented chronic toxicity than acute toxicity. This fact highlights that more weight should be placed upon acute toxicities when sediment quality is assessed. The combination of the results from the chronic and acute toxicity tests showed that sediments from P6 and P8 (during the rainy season) and from P5 and P8 (during the dry season) were toxic to the point of negatively affecting amphipod survival, copepod reproduction, and the development of sea urchin embryos (Fig. 2). On the other hand, sed- iments from P5 and P7 (during the rainy season) and from P4 (during the dry season) were not toxic. These results showed that toxicities of sediments from the mid-estuary change over time, despite the higher levels of metals and nutrients in this portion of the JPE. Sediments from the lower and upper portions of the JPE were toxic in both seasons. These findings corroborate the study conduct- ed by Buruaem et al. (2013b), in which chronic toxicity was found along the length of the estuary, while acute effects were associated only with sediments from the inner portion of the estuary. Previous studies found metal bioaccumulation in bivalves, barnacles and crabs collected along the JPE (Silva et al., 2001, 2006; Lopes, 2012), and foraminiferal assemblages from the estuary exhibited signs of environmental stress. (iron concentrations are expressed in %). Cu Cd Ni Pb Zn 0.4–7.4 0.02–0.37 0.8–3.5 1.2–6.5 1.2–30.1 0.29–2.4 b0.01–0.49 0.3–4.14 0.2–3.9 1.1–14.4 1.6–3.7 b0.01–0.013 3.8–11.8 1.67–4.67 6.7–12 0.58–8.49 0.07–0.40 – 1.38–2.51 0.39–2.14 b0.04–16.2 b0.01 6.6–21.9 b0.3–29.7 26.9–80 1.5–48 – – 1.5–28 2.6–31 12.5 0.3 1.1 0.2 18.9 b5–40 0.5–1.8 b5–20 b10–60 15–190 7–202 0.92–1.3 0.06–21.3 2.3–86.9 21.27–378 20.8 0.05 31.2 45.7 113 0.98–4.4 0.14–1.4 – 4.3–8.4 – 16 0.6 16 31 – 45 – – 20 95 rigues et al. (2013), 4 Choueri et al. (2009b), 5 Paula Filho et al. (2015), 6 Aprile and Bouvy 10 Gupta et al. (2009), 11 USEPA (1999), 12 Turekian and Wedepohl (1961). Table 4 Enrichment factors for metals (%EF) and risk quotients of toxicity (RQ) obtained for the sediments collected from the Jundiaí–Potengi Estuary in the rainy and dry seasons. Seasons Enrichment Factor (%EF) EF-total Risk Quotient (RQ) RQ-total Classification Fe Mn Cr Cu Cd Ni Pb Zn Fe Mn Cr Cu Cd Ni Pb Zn RQ Rainy season P1 93 31 0 7 0 0 0 4 16.9 8.1 1.0 0 1.9 0.1 0.8 1.0 1.7 1.9 Moderate P2 98 3 0 100 37 100 100 100 67.2 8.5 0.8 0 15.5 0.6 3.2 5.3 20.8 6.8 Very high P3 72 3 0 48 29 53 34 17 32.1 6.3 0.9 0 7.9 0.5 2.1 2.5 4.3 3.1 Considerable P4 100 34 36 38 49 50 39 35 47.5 8.7 2.1 0.3 6.4 0.8 2.0 2.7 7.8 3.8 Considerable P5 64 15 100 29 66 72 30 32 50.9 5.6 1.3 0.7 5.0 1.0 2.5 2.3 7.2 3.2 Considerable P6 81 100 50 33 57 36 22 26 50.5 7.1 4.7 0.4 5.7 0.9 1.6 2.0 6.0 3.5 Considerable P7 46 32 69 20 100 49 35 41 49.0 4.0 2.0 0.5 3.8 1.5 2.0 2.5 9.1 3.2 Considerable P8 77 0 86 88 69 16 66 86 61.1 6.7 0.7 0.6 13.8 1.0 1.2 3.8 18.1 5.8 Considerable P9 1 33 0 0 97 13 18 2 20.6 0.2 2.0 0 0.9 1.4 1.1 1.8 1.3 1.1 Moderate P10 0 23 0 0 89 4 17 0 16.6 0.1 1.6 0 0.8 1.3 0.9 1.8 0.9 0.9 Low Dry season P1 88 77 0 62 2 37 22 10 37.2 7.2 6.3 0 3.5 0 1.6 1.0 2.1 2.7 Moderate P2 66 12 0 0 0 0 0 7 10.6 5.5 1.7 0 0.6 0 0.3 0.2 1.8 1.3 Moderate P3 38 0 28 63 16 31 44 28 31.0 3.2 0.8 0.6 3.6 0.3 1.4 1.7 4.2 2.0 Moderate P4 100 100 99 100 78 100 100 100 97.1 8.2 7.9 2.2 5.3 1.5 3.7 1.7 12.2 5.6 Considerable P5 51 43 100 16 96 72 67 71 64.5 4.2 3.9 2.2 1.4 1.9 2.8 2.5 8.9 3.5 Considerable P6 69 27 74 62 59 41 53 57 55.4 5.7 2.7 1.7 3.6 1.2 1.7 2.1 7.4 3.3 Considerable P7 8 12 41 5 71 23 47 18 28.2 0.7 1.7 0.9 0.9 1.4 1.1 1.8 3.1 1.5 Moderate P8 0 21 56 17 100 30 60 7 36.5 0.1 2.3 1.3 1.4 2.0 1.4 2.3 1.9 1.6 Moderate P9 1 6 45 6 73 18 48 3 25.0 0.1 1.2 1.0 0.9 1.4 1.0 1.9 1.4 1.1 Moderate P10 0 12 44 7 71 18 42 0 24.2 0.1 1.7 1.0 0.9 1.4 1.0 1.7 1.1 1.1 Moderate 77I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 3.5. Integration of geochemical and ecotoxicological data The cluster analyses showed 4 groups for the rainy season and 3 groups for the dry season (Fig. 3). In the rainy season, CA separated P1 from the resting sites, probably due to the low levels of metals and nutrients found. Sites P9 and P10 formed a second group that presented intermediate quantities of OM, a high percentage ofmuds, high nitrogen content, low phosphorus levels, and low metal concentrations (except in the case of Cd). The third group included P2 and P8, with intermedi- ate quantities of OM andmuds, high nitrogen levels, highmetal concen- trations, and poor quality according to the toxicity tests. The fourth group included sites P3, P4, P5, P6, and P7 (mid-estuary) the sediment of which presented highmetal concentrations and OM levels, moderate to high quantities of nitrogen and phosphorus, and variable toxicities. This CA suggests that other contaminants (not analyzed herein) may be contributing to the sediment toxicities, especially in the lower and upper portions of the JPE. In the dry season, the first group included P4, P5 and P6, with high levels of metals, nutrients, and OM, as well as variable toxicities. The second group included P7 and P10, where the sediments presented low phosphorus concentrations, moderate concentrations of OM, Cr, Cd and Pb, high amounts of muds, high total nitrogen content, and high toxicity. The third cluster included sites P1, P2 and P3, where Table 5 Results of the tests on sediments from the Jundiaí–Potengi Estuary and the experimental contr Rainy season C P1 AT % mortality L. plumulosus 3.3 0 T. viscana 10 73.3 CT fecundity ((nauplii + copepodits)/female) Nitocra sp. 33.1 46.8 % abnormal development L. variegatus 15 95.2 Dry season AT % mortality L. plumulosus 1.7 5 T. viscana 16.7 96.7 CT fecundity ((nauplii + copepodits)/female) Nitocra sp. 43.7 35.6 % abnormal development L. variegatus 19.2 64.2 AT: acute toxicity. CT: chronic toxicity. C: control. metals, nutrients and OMwere low but where the toxicities were mod- erate to high. As well as in the rainy season, non-measured contami- nants may be contributing to the toxicity levels. As sewage is discharged into the JPE, some pollutants would be ex- pected to occur, as pharmaceuticals and personal care products (PPCPs), detergents, chloramines and other chemicals (Bound and Voulvoulis, 2005; Wise et al., 2011). A previous study found high con- centrations of HPAs in sediments collected along the JPE (Queiroz, 2011), and since this group of substances is widely known as toxic and carcinogenic, they may have contributed to the observed toxicity. In addition, we measured the concentrations of ionized ammonia in the sediments and the concentrations reached levels capable of induc- ing negative biological effects; however three of test-organisms used in this study are relatively insensitive to ammonia. Campos et al. (2016) showed that in estuarine sediments rich in ammonia, inputs of low amounts of metals may induce sediment toxicity. Therefore, many chemicals may be present in JPE sediments, interacting with metals and contributing to the observed toxicity. Further studies should be con- ducted with the purpose of identify and quantify such substances. The results of the FA–PCA for both campaigns are shown in Figs. 4 and 5. For the results of the rainy season, the first three factors ex- plained 74.82% of the variances. Each axis explained a relatively low percentage of variances (Table 6), which is expected in heterogeneous ol (C) during the rainy and dry seasons. The values shown are the means. P2 P3 P4 P5 P6 P7 P8 P9 P10 5 3.3 13.3 16.7 1.7 11.7 30 1.7 1.7 83.3 30 33.3 33.3 46.7 40 76.7 36.7 56.7 35.4 29.7 27.9 34.7 19.3 25.1 24.2 17.1 20.6 100 100 91.5 33.2 54.7 26.2 100 79.2 83.7 3.3 1.7 16.7 21.7 20 15 13.3 10 45 46.7 60 55 40 53.3 73.3 73.3 83.3 40 37.5 17 33.4 22.7 18.6 34.7 20.7 36.5 22.1 94.7 92.5 36.7 92 81 88.7 100 74.7 41.7 Fig. 3. Results of the cluster analysis with geochemistry and toxicity data of sediments from 10 collection sites along the Jundiaí–Potengi Estuary (a) = rainy season; (b) = dry season. 78 I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 environments where interactions between variables are intense and complex. The first factor (F1) explained 34.19% of the variances and showed associations between nitrogen, Cr, Cu, Pb, Zn, and amphipod mortality (Table 6); sites P2 and P8 made the highest contribution to this factor (Fig. 5). Mn correlated negatively with F1, a finding which suggests that the positive correlationsmentioned above indicate an an- thropic component, since Mn naturally occurs in high concentrations and is not typically associated with human activity (Niencheski et al., 1994). These findings are consistent with the EF results, which showed enrichment of metals in sediments from P2 and P8 (Table 4). The second factor explained 26.38% of the variances and showed positive correlationswith nitrogen, Cr, Cd, Ni, OM, andmuds (Table 6). Negative correlations with this factor were obtained in the case of T. viscana mortality and abnormal sea urchin embryo development. Site P1 was the most important to F2 (Fig. 5). This result corroborates those from the CA and suggests that, during the rainy season, P1 is not directly influenced by the deposition of OM and muds or, consequently, by the Fig. 4. Three-dimensional projection of geochemical and ecotoxicological variables from elements associated with suspended particles, such as nitrogen, Cr, Cd, and Ni; under these conditions, toxicity may have been caused by unmeasured contaminants (Table 6 and Fig. 2). The third factor (F3) ex- plained only 14.3% of the variances and showed an association between Fe, Cu, Ni, Pb, and phosphorus. This finding may indicate a common source for these elements, such as sewage or urban drainage. Copepod fecundity was found to be negatively correlatedwith this factor, a result which indicates that the elements above may be linked to chronic tox- icity; on the other hand, the negative correlation observed in the case of Cd may be a mathematical artifact, since the concentrations of this ele- ment were low. When the dry season was considered, the first three factors ex- plained 78.95% of the variances (Fig. 5). The first factor explained 46.33% of the variances and showed positive correlation for Fe, Mn, Cr, Cu, Ni, Pb, Zn, phosphorus, and OM (Table 6). Abnormal L. variegatus de- velopment was found to be negatively correlated with F1; thus, these results suggest that the main causes of toxicity for this species were the Jundiaí–Potengi Estuary for the rainy and dry seasons after the factor analyses. Fig. 5. Scores of the two first factors obtained in the factor analyses using geochemical and ecotoxicological variables of the Jundiaí–Potengi Estuary for the rainy season and the dry season. 79I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 unmeasured contaminants. Sites P4, P5, and P6 were the most impor- tant to this factor (Fig. 5). The results also suggest, at least partially, that the metals and phosphorus may have a natural source. Since sedi- ments from P4, P5, and P6 presented the highest EF values, this portion of the JPE is likely being influenced by both natural and human inputs during the dry season. Moreover, sediments from P4 were not toxic in this campaign, which indicates that metals were not bioavailable. Chapman and Wang (2001) reported that the increased metal concen- trations in relation to the background levels do not necessarily indicate toxicity. The second factor explained 22.01% of the variances and showed an association between nitrogen, OM, muds, Cr, Cd, Pb, Ni, and L. plumulosus mortality (Table 6); thus, F2 essentially provides evidence of the human causes of environmental degradation and its ef- fects. These correlations also showed that OM and muds are important geochemical carriers during the dry season, as suggested by Lacerda et al. (2012) in a study on other estuaries from the semi-arid coast of Table 6 Eigenvalues and correlations obtained in the factor analysis–principal component analysis (FA–PCA) using geochemical and ecotoxicological data on sediments from the Jundiaí– Potengi Estuary from the rainy and dry seasons. Bold fonts indicate significant correlations (for a cut-off value of 0.40). Variable Rainy season Dry season Factor 1 Factor 2 Factor 3 Factor 1 Factor 2 Factor 3 Fe 0.20 −0.22 0.84 0.87 −0.40 −0.06 Mn −0.56 0.28 −0.03 0.85 0.12 −0.39 Cr 0.51 0.54 −0.10 0.48 0.79 0.35 Cu 0.79 −0.15 0.51 0.85 −0.05 −0.13 Cd 0.20 0.57 −0.73 −0.06 0.97 0.13 Ni 0.38 0.46 0.73 0.88 0.43 0.07 Pb 0.82 −0.02 0.41 0.54 0.79 0.06 Zn 0.89 −0.06 0.38 0.88 0.31 0.30 N 0.47 0.58 0.02 0.08 0.70 −0.25 P 0.08 0.34 0.89 0.89 0.22 0.27 MO 0.11 0.91 0.17 0.53 0.72 0.32 Fines −0.28 0.83 −0.12 0.13 0.97 −0.04 Mort_L. plumulosus 0.80 0.16 −0.13 −0.14 0.61 0.23 Mort_T. viscana 0.45 −0.75 0.08 −0.13 −0.16 −0.81 Fec_Nitocra −0.14 0.31 −0.66 −0.04 0.07 0.63 Abnormal_L. variegatus 0.07 −0.79 0.19 −0.42 −0.27 0.38 Eigenvalues 5.47 4.22 2.27 7.41 3.52 1.69 % Total variance 34.19 26.39 14.23 46.33 22.01 10.6 % Cumulative var. 34.19 60.59 74.82 46.33 68.34 78.95 Brazil. Iron was found to be negatively correlated with to F2, a finding which corroborates that the source of metals was human activity. The third factor explained 10.60% of the variances. T. viscana mortality was found to be negatively correlated with this factor, while the abnormal sea-urchin embryo development was found to be positively correlated. This result suggests that, during the dry season, other variables (unmea- sured contaminants, confounding factors) contributed to sediment toxicity. The analyses showed that sediments from the JPE are especially enriched by the mid-estuarine portion. We were not able to not detect clear gradients along the estuary, because the JPE presents multiple contamination sources that create a complex and heterogeneous geo- chemical and ecotoxicological dynamic. A similar situation was ob- served by Rodrigues et al. (2013) in Guaratuba Bay (southern Brazil), as well as in other sites around the world (Du et al., 2012; Araujo et al., 2013; Roig et al., 2015). We also observed that, in both seasons, the sediment quality of the JPE was altered, and that nutrients and metals have both natural and anthropic sources, similar to other estuar- ies from the semi-arid coast of Brazil (Marins et al., 2002; Lacerda et al., 2007, 2012). Metal concentrations tended to occur in sediments from sites located close to sources of human activity, a finding which corrob- orates previous data on the JPE (Silva et al., 2001, 2003, 2006). These other studies reported that themain sources of pollution for this estuary are untreated sewage, industrial effluents, and agricultural residues, which include fertilizers and pesticides. Further studies are recom- mended to determine which chemical groups are responsible for the sediment toxicity in the JPE, as well as to determine if the microbenthic community is being affected by the contaminants. 4. Conclusions Our results indicate that the sediments from the JPE present some degree of degradation. These sediments are toxic and enriched by metals and nutrients, and this situation is produced by a combination of natural sources and human activity. The mid-estuary is considered to be the most altered portion of the JPE, regardless of the season. Con- ditions are worse during the rainy period, when urban and agricultural runoffs are more intense and carry other contaminants to the estuary. The dry season shows amore clear relationship between contamination and toxicity, because the conditions favor the retention of contaminants within the estuary. In this study, toxicities did not correlate highly with 80 I.S. Souza et al. / Marine Pollution Bulletin 104 (2016) 70–82 metal concentrations, a resultwhich suggests that unmeasured contam- inants are contributing to the environmental degradation. Acknowledgments The authors would like to thankMr. Espedito Carvalho for providing the map in a GIS environment; both the NEPEA Laboratory of São Paulo State University (UNESP) and the Federal University of Rio Grande do Norte (UFRN) Ecotoxicology Lab staff for the technical assistance; to the Rio Grande do Norte Federal Institute for Science and Technology Education (IFRN), and the Secretary of Professional and Technological Education from theMinistry of Education (SETEC-MEC) for the technical and financial support (grant No. 07/2013-2 andNo. 001/2012-1, respec- tively). Dr. D. Abessa thanks the Brazilian National Council for Scientific and Technological Development (CNPq) for their financial support (grant No. 479899/2013-4). Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.marpolbul.2016.02.009. References Abessa, D.M.S., Carr, R.S., Rachid, B.R.F., Sousa, E.C.P.M., Hortelani, M.A., Sarkis, J.E., 2005. 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Introduction 2. Materials and methods 2.1. Study area 2.2. Sediment sampling 2.3. Geochemical analyses 2.4. Sediment toxicity 2.4.1. Whole-sediment acute toxi