Marine Pollution Bulletin 115 (2017) 266–272

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Marine Pollution Bulletin

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Mercury concentrations in dusky marginatus in littoral and neritic habitats along the Southern Brazilian coast

Mario V. Condini a,⁎, David J. Hoeinghaus b, Aaron P. Roberts b, Brianne K. Soulen b, Alexandre M. Garcia a a Laboratory of , Institute of Oceanography, Federal University of Rio Grande, Av. Itália Km 8, Carreiros, 96, 201-900, Rio Grande, RS, b Department of Biological Sciences and the Advanced Environmental Research Institute, University of North Texas, 1155 Union Circle #310559, Denton, TX 76203-5017, USA article info abstract

Article history: Our study incorporated a comprehensive suite of parameters (i.e., body size, age, diet and trophic position) to in- Received 4 July 2016 vestigate mercury concentration in dusky Epinephelus marginatus. This study was carried out in rocky Received in revised form 28 November 2016 bottoms in littoral and neritic habitats along the Southern Brazilian coast. We also determined spatial variation Accepted 5 December 2016 in mercury concentrations in individuals inhabiting both zones, which may provide insights into how dietary dif- Available online 13 December 2016 ferences or potential pollution sources affect bioaccumulation. A total of 244 dusky groupers was analyzed to de-

Keywords: termine total mercury concentrations. Our study revealed that when considering similar body sizes, individuals Total mercury inhabiting littoral rocky habitats had higher concentrations of mercury probably due to proximity to pollution Trophic position sources associated with human activities in the estuary and its drainage basin. Furthermore, large individuals Epinephelidae (N650 mm and N8 years old) showed mercury contamination levels that are potentially harmful for this endan- Human health risk gered fish species and above the acceptable limits for human consumption. © 2017 Elsevier Ltd. All rights reserved.

1. Introduction 2012). Dusky grouper are exploited by fishermen in rocky bottoms along the coasts of South America (Figueiredo and Menezes, 1980; Mercury is a non-essential toxic element commonly found in aquatic Condini et al., 2007), Europe (Heemstra and Randall, 1993) and Africa ecosystems. It is released through a variety of natural and anthropogen- (Fennessy, 2006), and are widely consumed by human populations ic processes including geologic weathering, gold mining, and burning of (Heemstra and Randall, 1993). Mercury bioaccumulation in other coal (Pacyna et al., 2010). In aquatic systems, inorganic mercury can be epinephelids has been investigated mainly in the northern hemisphere transformed by microbial activity into organic methylmercury (MeHg) (Hassan et al., 2007; Evers et al., 2009; Tremain and Adams, 2012; Harris which biomagnifies in the food web and results in high concentrations et al., 2012, but see Lacerda et al., 2007 and Kutter et al., 2009), and prior of methylmercury in piscivorous species (including humans). Previous studies on mercury contamination of large-bodied fishes in the south- studies have shown deleterious effects of mercury on fish health at con- western Atlantic are restricted to other fish families such as scianids, centrations N0.3 mg kg−1 wet weight (Sandheinrich et al., 2011; Depew trichiurids, and scombrids (Viana et al., 2005; Medeiros et al., 2008; Di et al., 2012). These concentrations are not uncommon to aquatic food Beneditto et al., 2013). These studies focused mainly on levels of mercu- webs suggesting that health and reproduction of wild fish populations ry in fish tissues, typically muscle, and usually related contamination may be impacted at environmentally relevant concentrations of MeHg levels with body size (Adams and Onorato, 2005; Lacerda et al., 2007) (Beckvar et al., 2005; Webb et al., 2006; Sandheinrich and Wiener, and/or trophic position of the individual estimated by stable isotopes 2011). A literature review by Depew et al. (2012) of mostly freshwater (Bank et al., 2007; Hassan et al., 2007; Tremain and Adams, 2012; Di fishes found that concentrations of mercury within this range results in Beneditto et al., 2013; Sluis et al., 2013). In several cases, these studies decreases in gonadosomatic index (GSI), sex steroid production, report that mercury concentrations in large-bodied fishes are above spawning success, fertilization, fecundity, and increases in ovary the proposed threshold (0.3 mg kg−1 wet weight) required to safeguard apoptosis. these wild populations (Adams and Onorato, 2005; Lacerda et al., 2007; Large-bodied and long-lived fish species such as the dusky grouper Evers et al., 2009). In some instances, they are also above the safety (Epinephelus marginatus) are well recognized for their ability to levels (0.5 mg kg−1 wet weight, World Health Organization - WHO) bioaccumulate mercury (Evers et al., 2009; Tremain and Adams, for human consumption (Cai et al., 2007; Hassan et al., 2007; Harris et al., 2012; Sluis et al., 2013). Taken together, these studies provide evi- dence that mercury concentrations in dusky grouper are likely to fi ⁎ Corresponding author. occur at levels that may negatively affect sh health and pose a risk E-mail address: [email protected] (M.V. Condini). for human consumption.

http://dx.doi.org/10.1016/j.marpolbul.2016.12.006 0025-326X/© 2017 Elsevier Ltd. All rights reserved. M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272 267

Dusky grouper is an important fisheries species of conservation con- pair of rocky jetties is approximately 4.5 km long and extends from cern (classified by IUCN as “endangered”; Cornish and Harmelin-Vivien, the littoral zone to the sea. They were built in the beginning of the 2004), thus, additional information is needed on factors (e.g. body size, 20th century to maintain a navigation channel to allow regular mari- age, trophic position, habitat use) that affect mercury concentrations in time access to the harbor of Rio Grande. Over time, the area was colo- order to support conservation and socio-ecological aspects of fisheries nized by diverse marine benthic fauna (Capítoli, 1996) and by dusky management (e.g. size limits, consumption advisories). Dusky grouper grouper, mainly juveniles and immature females (Condini et al., also provide a unique ecological model for the study of effects of mercu- 2007). The second study area (Carpinteiro Bank) is located in the neritic ry on fish populations due to a complex life-history strategy that in- zone approximately 16 nautical miles offshore and between 20 and cludes slow growth rates, late maturation, aggregate spawning, and 30 m isobaths (Fig. 1; 32°16′S, 51°47′W) and was composed of beach sexual reversal (Heemstra and Randall, 1993; Craig et al., 2011). The rocks with a high level of cementation by recrystallized calcium carbon- first step in the study of potential mercury effects on population dynam- ate (Buchmann et al., 2001; Abreu and Calliari, 2005). Both study loca- ics is an understanding of ecological factors that mediate mercury con- tions represent rocky habitats within a coastal landscape that is centrations in the individuals. otherwise dominated by homogeneous sandy substrates. Individuals Our study provides the first account of total mercury bioaccumula- were collected in the littoral and neritic zones between January 2008 tion for an Epinephelus species in the Southwestern Atlantic, and has di- and April 2009 and between January 2010 and May 2011, respectively. rect relevance for conservation of this threatened species and human Collected specimens were stored directly on ice and taken to the lab- health of coastal communities that rely on this fishery. In contrast oratory for processing. Each individual was measured for total length with most prior studies on mercury contamination in groupers, our (TL, mm) and weighed (g). The new Hg contamination dataset present- study incorporated a more comprehensive suite of parameters (i.e., ed in this study builds on previously published research conducted by body size, age, stage of reproductive maturation, sex, diet and trophic the authors on maturity stages, age and trophic ecology of E. marginatus position) that may be expected to affect variation in mercury concentra- in the same study area (i.e. Condini et al., 2014a, 2014b, 2015). Maturity tion. We also determined spatial variation in mercury concentrations in stage and sexes of the dusky grouper were determined by histological individuals inhabiting littoral and neritic zones which may provide in- analysis of gonads (Condini et al., 2014a) and age estimates were deter- sights into how dietary differences or potential pollution sources affect mined by readings of saggital otoliths (Condini et al., 2014b). Condini et bioaccumulation. Our previous research at these sites (Condini et al., al. (2015) previously described the trophic ecology of dusky grouper at 2015) found that even though there was no relationship between these sites based on stomach contents and stable isotope data (δ13Cand body size and trophic position, dusky grouper at the littoral site had a δ15N). The same anterior-dorsal muscle tissue samples from each indi- diet dominated by fishes. Individuals at the neritic site consumed simi- vidual that were used to determine stable isotopes composition are an- lar amounts of shrimp and fishes except for the largest size class which alyzed in this study for mercury concentration. The current study builds consumed a greater proportion of fishes. Based on this, we expected a on the aforementioned previous findings for sex stage, age and trophic strong positive relationship between mercury concentration and body ecology by testing for relationships between each of these factors and size (length, weight) and age due to bioaccumulation, but not with tro- muscle mercury concentration. Importantly, muscle tissue collected phic position (i.e. biomagnification). Furthermore, the greater propor- for these analyses is representative of the fish fillet usually consumed tion of fish in the diets of dusky grouper from the littoral zone and the by humans (Adams and Onorato, 2005). largest size class from the neritic zone should correspond with higher Hg accumulation rates due to longer lifespans and greater proportion 2.2. Mercury analysis of Hg associated with assimilated biomass of prey fishes versus crabs and shrimp. Subsamples of dried and homogenized muscle tissue (n = 68 litto- ral, n = 176 neritic) were weighed to the nearest 0.3 mg using an ana- 2. Materials and methods lytical balance. Total mercury concentration was determined on a direct mercury analyzer (DMA-80; Milestone Inc., Monroe, Connecticut) using 2.1. Study area and sample collection thermal decomposition, gold amalgamation, and atomic absorption spectrometry (USEPA, 1998). Calibration curves were generated using This study was carried out in rocky habitats located adjacent to Patos three reference materials from the National Research Council of Canada: Lagoon Estuary. Patos Lagoon Estuary constitutes one of the largest and MESS-3 (marine sediment: certified value = 91 ± 9 ng of total Hg g−1 most well-studied estuarine regions in South America (see Seeliger et of dry weight), TORT-2 (lobster hepatopancreas: certified value al., 1997 and Odebrecht et al., 2010) and has been exploited by fisher- =270 ± 60 ng g−1), and DOLT-4 (dogfish liver tissue: certified men since the nineteenth century (Von Ihering, 1896). This estuary value = 2580 ± 220 ng g−1). Quality assurance included blanks, dupli- also contains the third most important Brazilian harbor that engages cate samples, and reference samples. Blank (empty boats) were ana- mainly in transport of chemical products, grains, and agricultural ma- lyzed every 20 samples with a mean Hg content of 0.0004 ± chines, among other potential pollutant sources (Odebrecht et al., 0.0005 mg kg−1 (range = 0–0.0015, n = 22). Duplicate samples were 2010; SPRG, 2016). Mirlean et al. (2003) report mercury concentrations analyzed every 20 samples with a mean relative percent difference of up to 21 mg kg−1 in suspended particulate matter of the shallow waters 3.69 ± 2.85% (range = 0.41–9.36%, n = 15). Reference samples of Patos Lagoon Estuary. The authors link this contamination to domes- (MESS-3, TORT-2 and DOLT-4) were analyzed every 10 samples with a tic sewage and stormwater runoff sources. Niencheski et al. (2001) and mean percent recovery for each of: MESS-3101.35 ± 3.54% (n =8), Kutter et al. (2009) quantified mercury contamination in fishes in Patos TORT-2110.01 ± 13.63% (n = 8), and DOLT-4 98.90 ± 2.44% (n = 8). Lagoon Estuary and adjacent marine area and found mercury concen- Results are presented as wet weight mercury concentrations, assuming trations b0.3 mg kg−1 for nearly all of species. These studies sampled a standard 80% moisture content of muscle. This conversion was done in primarily smaller-bodied species that feed at lower trophic positions, order to compare our dusky grouper muscle mercury concentrations to but also included some larger predatory species (e.g. Cysnoscion other reported literature values as well as toxicity benchmarks which guatacupa, Pomatomus saltatrix, Macrodon ancylodon) and one specimen are generally determined as wet weights. of E. marginatus. Dusky grouper were sampled from two marine sites adjacent to 2.3. Data analyses Patos Lagoon Estuary. The first is in the littoral zone along a pair of rocky jetties (locally known as ‘Molhes da Barra de Rio Grande’)located Individuals were pooled into four size classes (b351 mm TL, 351– at the mouth of Patos Lagoon Estuary (Fig. 1; 32°09′S, 52°05′W). The 500 mm TL, 501–650 mm TL, and N650 mm TL) in order to evaluate 268 M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272

Fig. 1. Patos Lagoon (~10,000 km2) and its estuarine zone in the state of Rio Grande do Sul, southern Brazil (A). Rocky jetties at the mouth of the lagoon (littoral zone, arrow) and Carpinteiro Bank in the adjacent marine area (neritic zone, box highlight) (B). The lines along the coast denote 10, 15, and 20 m isobaths, respectively. mercury contamination along the size increment of the species. These were conducted using continuous data and ecological factors of interest, size classes were chosen based on prior studies of dusky grouper repro- with and without the inclusion of individuals N650 mm TL from the ne- duction, age structure and feeding habits for the study region (Condini ritic zone (no individuals of this size were present in the littoral zone). et al., 2014a, 2014b, 2015, respectively). However, all statistical analyses Conducting complementary analyses with and without the largest size M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272 269 class is relevant for a couple reasons. First, excluding individuals and mature individuals. Importantly, the lack of large males from the N650 mm TL allows for a more direct comparison between sites with littoral site is not due to sampling bias, but rather is a natural aspect of completely overlapping size distributions. Second, sexual reversal this system. Large males only occur at the neritic site, likely due to the occurs at approximately the 650 mm TL threshold (Condini et al., absence of suitable habitat (i.e. large crevices) in the rocky jetties of 2014a), and this important physiological and ecological change may af- the littoral zone and occurrence of spawning aggregations in the neritic fect mercury accumulation differently in this largest size class compared zone (Condini et al., 2014a, 2014b). with smaller size classes. Total mercury concentrations across both study sites ranged from Relationships between factors expected to affect mercury concentra- 0.01 to 0.90 mg kg−1 wet weight, with higher concentrations in larger, tion ([Hg]) (i.e. total length, weight, age and δ15N) were tested at the older fishes (TL, weight and age, respectively: R2 = 0.77 and R =0.88, ‘global’ scale, i.e. all individuals from both sites, using linear regression, both P b 0.001; R2 = 0.84 and R = 0.92, both P b 0.001; and R2 =0.81 and relationships were compared between sites using analysis of co- and R = 0.90, both P b 0.001; Fig. 3a–c). These positive relationships be- variance (ANCOVA). Relationships between independent variables are tween mercury contamination and fish size and age reflect a well- depicted in Fig. 2, and ANCOVAs with site as the factor and the indepen- established pattern, which occurs due to the greater assimilation rate dent variables from the global regressions as the covariate are depicted of mercury versus the slow rate at which mercury is eliminated, i.e. bio- in Fig. 3. As noted above, all of the aforementioned analyses were con- accumulation (McKim et al., 1976; Adams and Onorato, 2005; Evers et ducted with and without individuals N650 mm TL. An additional series al., 2009; Tremain and Adams, 2012). In contrast, δ15N was not correlat- of ANCOVAs tested for differences in the relationship between each ed with [Hg] (R2 = 0.02 and R = 0.14, both P N 0.05). Mercury concen- factor and [Hg] for individuals b650 mm TL vs. N650 mm TL from the trations typically correlate with δ15N within and among species (Wang, neritic site (Hoeinghaus et al., 2006). All analyses were conducted 2002; Hussey et al., 2014) because nitrogen isotope ratios are useful using R version 3.1.2. tracers of trophic position which is also frequently correlated with body size and age in fishes (i.e. reflecting both bioaccumulation and 3. Results and discussion biomagnification). Dusky grouper in this study, although representing a broad range in body sizes and ages (Fig. 2), have similar trophic levels All individuals captured from the littoral zone were females, and few throughout their ontogeny (Condini et al., 2015), as evidenced by the males were caught from the neritic zone (94% females, 6% males). Total limited difference in δ15N among individuals (Table 1, Figs. 2dand lengths (TL) of individuals from the littoral zone ranged from 260 to 3d). That being said, dusky grouper exhibit differences in prey ingested 640 mm and total weights (TW) ranged from 0.34 to 5.23 kg and assimilated among sites and size classes (Condini et al., 2015). (Table 1). In the neritic zone, TL ranged from 290 to 1160 mm and TW Bayesian mixing models based on carbon and nitrogen stable isotope ranged from 0.31 to 25.00 kg. Approximately 53% of all individuals data of dusky grouper and potential prey taxa (Condini et al., 2015) were below the TL of first maturation (496 mm TL), thus our sample indicate greater assimilation of fishes by grouper in the littoral zone population is approximately equally split between sexually immature (approximately 80% contribution across size classes) compared with

Fig. 2. Relationship between total length (mm) and weight (g), age (years) and δ15N(‰) (A, C and D) and between log total length and log weight (B) of dusky grouper from littoral and neritic habitats along the Southern Brazilian coast. 270 M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272

Fig. 3. Relationships between total mercury concentration (mg kg−1 wet weight) and total length (mm), weight (g), age (years) and δ15N(‰) (A through D, respectively) of dusky grouper from littoral and neritic habitats along the Southern Brazilian coast. Significant regressions are plotted for both sites for each factor. Shading indicates toxicity thresholds at 0.3 mg kg−1 and 0.5 mg kg−1.

Table 1 Comparison of mercury concentration (mg kg−1 wet weight), total length (mm), total weight (kg), age (years) and δ15N(‰) of the dusky grouper (Epinephelus marginatus) from littoral and neritic habitats along the Southern Brazilian coast.

Parameters Mean ± SD Range Mean ± SD Range

b351 mm Littoral zone (n = 10) Neritic zone (n = 26) Hg (mg kg−1) 0.09 ± 0.03 0.06–0.12 0.08 ± 0.02 0.05–0.14 Total length (mm) 318.4 ± 24.2 260–349 318.7 ± 17.8 290–350 Total weight (Kg) 0.63 ± 0.12 0.34–0.79 0.56 ± 0.13 0.31–0.87 ⁎ Age (years) 3.9 ± 0.8 3–5 2.1 ± 0.4 2–3 δ15N(‰) 17.55 ± 0.45 16.82–18.29 17.66 ± 0.39 17.09–18.32 351–500 mm Littoral zone (n = 40) Neritic zone (n = 57) Hg (mg kg−1) 0.14 ± 0.03 0.07–0.24 0.12 ± 0.03 0.01–0.20 Total length (mm) 433.9 ± 37.1 368–500 419.5 ± 39.5 353–499 Total weight (Kg) 1.54 ± 0.41 0.86–2.54 1.38 ± 0.41 0.70–2.27 ⁎⁎ Age (years) 4.7 ± 0.8 3–6 3.6 ± 1.0 2–7 δ15N(‰) 17.89 ± 0.35 16.78–18.58 17.74 ± 0.48 16.34–18.47 501–650 mm Littoral zone (n = 18) Neritic zone (n = 57) Hg (mg kg−1) 0.21 ± 0.03 0.15–0.28 0.18 ± 0.03 0.13–0.26 Total length (mm) 555.8 ± 42.7 501–640 567.9 ± 43.2 501–650 Total weight (Kg) 3.31 ± 0.92 2.04–5.23 3.51 ± 0.93 2.11–5.90 ⁎⁎⁎ Age (years) 6.7 ± 1.4 5–11 6.2 ± 1.3 4–10 δ15N(‰) 17.90 ± 0.31 17.44–18.77 17.94 ± 0.37 17.09–18.82 N650 mm Littoral zone (n = 0) Neritic zone (n = 36) Hg (mg kg−1) 0.38 ± 0.17 0.14–0.90 Total length (mm) 792.8 ± 114.8 660–1160 Total weight (Kg) 9.67 ± 4.15 4.73–25.00 Age (years) 18.4 ± 8.5 7–40 δ15N(‰) 17.98 ± 0.61 16.47–19.14

* Age in the littoral zone n = 8 and neritic zone n = 26; ** Age in the littoral zone n = 33 and neritic zone n = 51; *** Age in the littoral zone n = 16 and neritic zone n = 55. M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272 271 the neritic zone (approximately 40% for all size classes b650 mm TL, but Total mercury concentrations in individuals from the littoral zone approaching 60% for individuals N650 mm TL; shrimp were the other were below suggested threshold values (0.3 mg kg−1) to prevent fish primary prey , contributing 30–50% and decreasing with body size). health impacts (Beckvar et al., 2005; Sandheinrich et al., 2011; Depew The aforementioned differences in diet between sites likely contrib- et al., 2012). A similar pattern was observed for dusky groupers with ute to the significant differences in mercury accumulation rate between total length b650 mm TL caught at the neritic zone. However, two- individuals from the littoral and neritic zones (Fig. 3a–c). Regression thirds of the individuals N650 mm TL at the neritic zone (n = 36) had slopes in ANCOVA analyses for total length, weight and age were signif- mercury concentrations above the 0.3 mg kg−1 toxicity threshold (Fig. icantly steeper for the littoral site (F = 7.746, d.f. =1,P b 0.01; F = 3a). Although most individuals of dusky grouper showed mercury con- 10.045, d.f. =1,P b 0.01; F =5.993,d.f. =1,P b 0.05, respectively), in- centration below safety levels, the majority of larger, reproductively dicating greater rate of mercury accumulation compared to the neritic mature individuals (N650 mm TL) had higher concentrations site (for individuals b650 mm TL). This may be due to the greater pro- (N0.3 mg kg−1) indicating potential harmful consequences for fish portion of fish in the assimilated diet of littoral zone grouper (see health and human consumption. Thus, consumption of dusky grouper Condini et al., 2015), even though trophic position did not differ be- larger than 650 mm TL by humans should be avoided or limited in tween sites or size classes, because the fish species primarily consumed this region of the Southwestern Atlantic to prevent exposure to (mainly sciaenids, e.g. whitemouth croaker Micropogonias furnieri, ar- mercury. gentine croaker Umbrina canosai, southern kingcroaker Menticirrhus Mercury contamination values found in the present work were con- americanus, barbel drum Ctenosciaena gracilicirrhus, and stripped weak- siderably higher than prior results reported for this lagoon by fish Cynoscion guatucupa) are longer lived than alternate prey (e.g. blue Niencheski et al. (2001) and Kutter et al. (2009). Niencheski et al. crabs, shrimp) and thus are expected to carry greater total mercury in (2001) investigated only two estuarine species (Odonthestes bonariensis their tissues due to bioaccumulation. Similarly, Tremain and Adams and Micropogonias furnieri) and all analyzed individuals had mercury (2012) investigated relationships between total mercury contamina- concentrations below 0.3 mg kg−1. In contrast, Kutter et al. (2009) an- tion and feeding ecology in some epinephelids and found that species alyzed several freshwater, estuarine and marine species, but only two feeding mainly on fish exhibited higher mean mercury concentrations freshwater species (Oligosarcus jenynsii and O. robustus) showed mercu- than those species preying upon invertebrates. ry contamination values above 0.3 mg kg−1. Kutter et al. (2009) ana- Dusky grouper N650 mm TL from the neritic zone had a significantly lyzed a single large (900 mm TL) dusky grouper specimen, which higher slope in our ANCOVA analysis than smaller size classes (individ- showed a lower value (215.8 ng g−1 wet weight, equivalent uals b650 mm) (F = 111.066, DF =1,P b 0.001), representing an Hg ac- 0.22 mg kg−1) than the average value observed in this study for individ- cumulation rate N3× faster than the smaller size classes (Fig. 3a). The uals of similar body size (e.g. 0.53 mg kg−1 wet weight). Unfortunately, slopes between smaller size classes (b650 mm) from the littoral and ne- they did not report the site location where this specimen was caught, ritic zones were not significantly different (Fig. 3a), suggesting that part but considering its large body size and expected size distribution of of the observed increase in accumulation rate with length is due simply this species in this region (Condini et al., 2014a), it most likely came to bioaccumulation. This largest size class in the neritic zone exhibits a from offshore waters and not from the rocky jetties in the littoral significant increase in the proportion of fish in the assimilated diet zone. In contrast, Tremain and Adams (2012) determined mercury and larger prey in general (Condini et al., 2015), but fish still contribute levels in several Epinephelus grouper species (E. adscensionis, E. less to the assimilated diet than for individuals of all size classes from drummondhayi, E. flavolimbatus, E. itajara, E. morio and E. nigritus)in the littoral zone. Site specific differences in the species composition of the Gulf of Mexico and found mean concentrations similar to those we prey may play a role (e.g. cephalopods such as spp. consumed observed in the present study. only in the neritic zone; Condini et al., 2015), though our data are insuf- Many of the fish species consumed by dusky grouper (e.g., ficient to assess the importance of specificpreytaxa. whitemouth croaker) use the estuarine regions as a feeding and grow- Another key ecological factor that occurs only in the largest size class ing site during their early stages of life and then migrate to the ocean is sexual reversal. Several Epinephelidae species, including dusky grou- to spawn. It seems plausible that the mercury concentrations observed per, are protogynous hermaphrodites, undergoing sex change from fe- in this dusky grouper population occur mainly due to the consumption male to male at larger sizes (Heemstra and Randall, 1993). We are of fish prey that spends the majority of their life in the estuarine region unaware of any physiological studies that have examined potential in- of Patos Lagoon. That is, fish moving from the estuary to the coastal zone fluences of hermaphroditism (e.g. due to hormone changes) on mercury are serving as a vector for mercury transport and accumulation in coast- bioaccumulation. Although our sample size for comparing sexes in the al fisheries. This is potentially significant due to the expected greater po- largest size class is admittedly small (i.e. females 764–933 mm TL, tential for mercury methylation in shallow wetland habitats of the n = 11; males 765–1160 mm TL, n = 10), we found no significant dif- estuary and concentrated point sources in that region. Further investi- ferences in total mercury concentration between genders (ANOVA: gation on mercury contamination of marine estuarine-dependent fishes F = 0.1096, P N 0.05). integrated with natural markers (e.g., otolith chemistry, stable isotopes) Higher mercury contamination at the littoral zone was expected to reveal fish movement patterns between estuary and adjacent sea since it is located in the mouth of the largest costal lagoon (~ would be necessary to evaluate this hypothesis. 10,000 km2) in Southern Brazil. This lagoon and its drainage basin (~ 200,000 km) is surrounded by several cities and possesses a large port 4. Conclusions with extensive traffic and industrial center located approximately 10 km from our study site (Asmus, 1998). Industrial and agricultural ac- Our study revealed that large individuals of dusky grouper occurring tivities and high density urban settlements occurring in this area are as- in the southernmost limit of its distribution in the Southwestern Atlan- sociated with several contamination sources such as domestic sewage, tic have mercury contamination levels that are potentially harmful for stormwater runoff and atmospheric emissions (Seeliger and Costa, this endangered fish species and also above the acceptable limits for 1998; Asmus and Tagliani, 1998; Niencheski et al., 2001; Mirlean et al., human consumption. Mercury contamination in this species was corre- 2003). All runoff and continental discharge from this lagoon reach the lated both with site locations and body sizes. Mature larger-body indi- ocean through the estuary mouth where our study site at the rocky viduals (N650 mm and N8 years old) exhibited the highest mercury jetties is located (Marques et al., 2010). In contrast, the neritic popula- concentrations. When considering similar body sizes, individuals tion is located approximately 16 nautical miles from the mouth of the inhabiting littoral rocky habitats adjacent to a large coastal lagoon had lagoon and, consequently, probably experiences far lower exposure higher concentrations of mercury probably due to proximity to pollu- from pollutants due to massive dilution in the marine system. tion sources associated with human activities in the estuary and its 272 M.V. Condini et al. / Marine Pollution Bulletin 115 (2017) 266–272 drainage basin. Based on prior diet studies with this population, we hy- Figueiredo, J.L., Menezes, N.A., 1980. Manual de peixes marinhos do sudeste do Brasil. III. fi fi Teleostei (2). Museu de Zoologia, Universidade de São Paulo, São Paulo. pothesized that sh consumption (mainly of estuarine-dependent sh- Harris, R., Pollman, C., Landing, W., Evans, D., Axelrad, D., Hutchinson, D., Morey, S.L., es) was the most likely trophic link leading to mercury contamination, Rumbold, D., Dukhovskoy, D., Adams, D.H., Vijayaraghavan, K., Holmes, C., Atknson, especially in the littoral zone. Further studies are needed to identify R.D., Myers, T., Sunderland, E., 2012. Mercury in the Gulf of Mexico: sources to recep- tors. Environ. Res. 119, 42–52. which human activities are the primary sources of mercury contamina- Hassan, A.A., Ababneh, F.A., Lean, D.R., 2007. Evaluating mercury biomagnification in fish tion and also to test our proposed hypothesis on the prevalence of estu- from a tropical marine environment using stable isotopes (δ15Nandδ13C). Environ. arine-dependent fish prey as the main trophic link leading to mercury Toxicol. 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