Marine Pollution Bulletin 60 (2010) 2350–2356

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Marine Pollution Bulletin

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Inorganic and methylmercury: Do they transfer along a tropical coastal food web?

Helena A. Kehrig a,⇑, Tércia G. Seixas b, Aída P. Baêta b, Olaf Malm a, Isabel Moreira b

a Lab. de Radioisótopos Eduardo Penna Franca, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-902, RJ, Brazilb Departamento de Química, PUC-Rio, 22453-900 Rio de Janeiro, RJ, Brazil

a r t i c l e i n f o

Keywords:BiomagnificationTropical ecosystemWaterAquatic biotaVertical trophic guildsTrophic transfer

0025-326X/$ - see front matter � 2010 Elsevier Ltd.doi:10.1016/j.marpolbul.2010.08.010

⇑ Corresponding author. Tel./fax: +55 21 2561 5339E-mail address: helena.kehrig@pq.cnpq.br (H.A. Ke

a b s t r a c t

Methylmercury (MeHg) and inorganic mercury (Hginorg) were evaluated in the water of a Brazilian estu-ary, with two size classes of plankton and seven fish species of different feeding habits. Water partitioncoefficients (PCs) in microplankton were fourfold higher for MeHg than for Hginorg; and water PCs in mes-oplankton were 26 times higher for MeHg than Hginorg. Difference between microplankton and meso-plankton MeHg bioaccumulation factor (BAF) was higher (0.60 log units) than Hginorg BAF (0.24 logunits), indicating that trophic transfer of MeHg between planktonic organisms is more efficient thanHginorg transference. MeHg concentrations, proportion of mercury as MeHg and its biotransference factors(BTFs) in the microplankton, mesoplankton and fish increased with increasing trophic level while bioticconcentrations of Hginorg and proportion of mercury as Hginorg decreased thus indicating that MeHg wasindeed the biomagnified species of mercury. MeHg reflected the vertical trophic guilds distribution, dueto the fact that the top predator fish presented the highest concentration (0.77 lg g�1 d.w.), followed bythe less voracious species (0.43 lg g�1 d.w.); while planktivorous fish presented the lowest concentra-tions (0.044 lg g�1 d.w.). Hginorg did not present the same behavior. Results suggest that feeding habitsand trophic guild are important parameters, influencing biotransference and biomagnification processes.

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Among the different metals subject to environmental interestthat also show naturally high concentrations in several regions ismercury. Environmental exposure to mercury via the food web,particularly for higher trophic level consumers, including humans,is significantly higher, since this metal presents high toxicity andthe ability to undergo biomagnification along the trophic webs(Agusa et al., 2007). Biomagnification is the process where mercurycompounds are transferred from food to an organism resulting inhigher concentrations compared with the source (Gray, 2002).

The trophic transfer of mercury along marine food webs hasbeen recognized as an important process, influencing bioaccumu-lation and the geochemical cycling of mercury (Fisher and Reinfel-der, 1995). The trophic transfer factors along the food web are auseful tool to assess the biomagnification of mercury from one tro-phic link to another. However, bioavailability and chemical species(especially free ions) influences mercury toxicity and its bioaccu-mulation by organisms in the marine environment (Wang andRainbow, 2005).

This metal in its more toxic organic form, methylmercury, isbioaccumulated up to a million times over the aquatic trophicweb, from its base (microorganisms) to organisms at the top ofthe food web (predatory fish and mammals), by adsorption tothe body surface and, mainly, by food ingestion. Methylmercury

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.hrig).

biotransfers from base to higher trophic levels via both benthicand pelagic pathways (Chen et al., 2009). It is a neurotoxic agentthat presents great risks especially for organisms from higher tro-phic levels, among which human beings are included when theymake use of fish as a protein source (WHO, 1990). As the aquaticbiota has a direct relationship with the environment, it becomescapable of being used as indicator of the adverse effects of mer-cury. Therefore, predatory fish that show the highest concentra-tions of mercury and, consequently, methylmercury, are the mostsensitive organisms to this element; due to the mercury loadassimilated and accumulated in their tissues from feeding, thesetop-chain organisms can be considered excellent sentinels of envi-ronmental quality (Altindag and Yigit, 2005).

The Brazilian coast presents large urban and industrial centers,which often release waste into aquatic systems as a result of theiractivities, such as domestic sewage, industrial effluents and pesti-cides, among others, without proper treatment. One of the most af-fected coastal regions regarding this type of contamination islocated in southeastern Brazil: Guanabara Bay (Fig. 1). This area re-ceives impacts in the form of domestic sewage and untreatedindustrial effluents from a densely populated area with over10,000 industries, besides a very active port and a complex petro-chemical pole (Jablonski et al., 2006). In this bay, an importantsource of mercury is a chlor-alkali plant, which is located in themost polluted area of its drainage basin, in the northwest portionof this aquatic system. Changes in its drainage areas, beginning

Fig. 1. Geographic location and distribution of sampling stations of water and microorganisms samples at Guanabara Bay, a eutrophic coastal area in the Brazilian Southeast.

H.A. Kehrig et al. / Marine Pollution Bulletin 60 (2010) 2350–2356 2351

at the early nineteenth century, have continued to cause severeenvironmental degradation. Consequently, the bay shows highconcentrations of toxic metals and hydrocarbons in sediments,and changes in the pelagic and benthic communities (Valentinet al., 1999). Guanabara Bay, one of the main productive coastalecosystems in this region, shows eutrophic conditions with highphytoplankton density and high nutrient concentrations, resultingin waters with of high biological production (Valentin et al., 1999).

The present study evaluated methylmercury (MeHg) and inor-ganic mercury (Hginorg) concentrations in water samples, two sizeclasses of plankton, microplankton and mesoplankton (70–290and P290 lm, respectively), and in muscle tissues of seven fishspecies with different feeding habits (Sardinella brasiliensis, Mugilliza, Bagre bagre, Orthopristis ruber, Micropogonias furnieri, Centrop-omus undecimalis and Trichiurus lepturus) from a eutrophic Brazil-ian coastal area, Guanabara Bay. The aims were to compare thepossible differences in the trophic transfer and biomagnificationof MeHg and Hginorg among the vertical trophic guilds, as well asalong the aquatic food web from the base level (planktonic com-munity) to its top level, represented by the predator fish, T.lepturus.

This study also calculated the biotransference factor (BTF),which is defined as the ratio that compares the concentration of

a certain chemical agent (MeHg and Hginorg) between the con-sumer and source (Gray, 2002).

The use of this set of different species of aquatic organisms al-lowed the comparison of MeHg and Hginorg concentrations accord-ing to vertical fish trophic guilds, since this is a factor thatsignificantly affects the accumulation of these contaminants inthe studied biota. As a result, a more complete picture of the trans-fer and magnification routes of these mercury species, toxic toaquatic biota, and, consequently, to humans who consume them,is obtained.

In the last decade some studies have been developed regardingthe biotransference and biomagnification of mercury in some fresh-water and marine ecosystems worldwide (Bowles et al., 2001;Baeyens et al., 2003; Chen et al., 2008, 2009). Therefore, a limitednumber of studies are available for comparison of trophic transferacross marine systems, mainly in coastal regions in southeasternBrazil (Kehrig et al., 2009a,b). Furthermore, tropical coastal watersare less monitored than marine environments in the Temperate andPolar Regions, in particular the South Atlantic Ocean, which is oftenconsidered less contaminated then the northern ocean.

Water and planktonic organisms were sampled from the super-ficial water layer (depth of 0.2–1.0 m) of Guanabara Bay, on 11August 2005. Sampling was performed at neap tide cycle during

2352 H.A. Kehrig et al. / Marine Pollution Bulletin 60 (2010) 2350–2356

the day, at tide amplitude of 0.1 m in the new moon phase. Theexperimental design was based on the tide chart from the BrazilianNavy’s Diretoria de Hidrografia e Navegação – DHN (http://www.mar.mil.br/dhn/chm/tabuas/index.htm). Estuarine waterand microorganisms were collected at five sampling stations alongthe lower estuary (points 1–5) (see Fig. 1). The sampling stationswere chosen according to natural hydrodynamic characteristicsof Guanabara Bay and pollution intensity established in previousstudies (Kehrig et al., 2006).

At each sampling station water samples were collected using5 L Van Dorn bottles, which were then stored in Teflon bottles at�10 �C. These bottles were previously washed with phosphorousfree detergent and cleaned with diluted hydrochloric acid (10%)in deionized water. Just before filling these bottles they werewashed with local water, at each sampling station. The planktonsamples were taken at the five sampling stations, by horizontalhauls at the water surface, using planktonic conical nets of 70and 290 lm mesh size, aiming to separate microplankton andmesoplankton, respectively. The plankton samples were stored inpre-cleaned Teflon bottles, separated per site and identified. Atthe laboratory these samples were freeze-dried and stored in her-metic vessels until chemical analysis.

In 2005 with the aid of a fishing colony, 136 individuals of sevenfish species with different feeding habits and occupying differenthabitats in the aquatic system of Guanabara Bay were collected(Table 1). After identification of fish species (S. brasiliensis, M. liza,B. bagre, O. ruber, M. furnieri, C. undecimalis and T. lepturus), theweight and total length of each individual were measured, andmuscle was removed from the dorso-lateral left side. The muscletissue samples were then freeze-dried.

Table 1 shows total length means and ranges, common names,number of individuals, food habits and habitat of aquatic biotasampled in Guanabara Bay in 2005, as well as the distribution offish species throughout the trophic guilds.

The fish species used in this study were grouped into three ver-tical trophic guilds according to their diet (voracious predator fish,intermediary voracious predatory fish and non-predatory fish),that is, in groups of fish species that feed on similar food sourcesand use those sources in the same manner (Townsend et al.,2000). The voracious predator fish, T. lepturus, presents carnivoroushabits, preferably piscivorous, actively pursuing their prey. In con-trast, the carnivorous species, B. bagre, O. ruber, M. furnieri and C.undecimalis are intermediary voracious predatory fish, since theyfeed mainly on invertebrates and small fish. The non-predatory fishspecies S. brasiliensis and M. liza are planktivorous species that liveassociated with the surface of the water mass.

The fish used in this study represent some of the most abundantand widely distributed species in the southeastern Brazilian coastand are also often consumed by the local population. Among thespecies of high commercial value caught in Guanabara Bay are M.furnieri M. liza, Mugil curema and S. brasiliensis. Species caught in

Table 1Means and range of total length (TL), common name (CN), number of sampling locations odistribution throughout the vertical trophic guilds (VTG).

Plankton CN N TL (lm)Microplankton Pooled species 5 (70–290)Mesoplankton 5 P290

Fish CN N TL (mm)Sardinella brasiliensis Brazilian sardinella 20 172 (170–180)Mugil liza Lebranche mullet 20 315 (290–355)Bagre bagre Catfish 18 401 (320–540)Orthopristis ruber Corocoro grunt 20 234 (215–260)Micropogoanias furnieri Whitemouth croaker 20 360 (330–430)Centropomus undecimalis Common snook 20 325 (280–400)Trichiurus lepturus Largehead hairtail 18 820 (620–1200)

this estuary in high quantity are T. lepturus and the Arius, Bagreand Genidens species, commonly known as ‘catfish’ (Jablonskiet al., 2006).

Total mercury and methylmercury concentrations were deter-mined based on the preconcentration of mercury from approxi-mately 2 L of water samples by solvent extraction of mercurydithizonates (Hg-Dz). The first step consisted of simultaneousextraction of inorganic mercury and methylmercury dithizonatesinto toluene. An aliquot of this extract was used for the determina-tion of the total mercury concentration (Hg) and the remainingfraction of the organic solvent was used for determination of meth-ylmercury (MeHg). For Hg, after removal of the organic solvent byrotary evaporation, Hg-Dz was decomposed by acid digestion andmeasured by cold vapor atomic absorption spectrometry with aFlow Injection Mercury System (FIMS) – FIAS 400 (Perkin Elmer)equipped with auto sampler and using sodium borohydride as areducing agent. For MeHg, the procedure consisted of clean-upsteps in which MeHg was stripped from the organic solvent intoaqueous Na2S solution, H2S was removed by evaporation and backextraction of MeHg-Dz was performed, into a small volume of tol-uene. Detection was conducted by gas chromatography coupledwith electron capture detection (GC-ECD). Recoveries obtained byspiking with aqueous MeHg–cysteine solution were almost quanti-tative, so no recovery corrections were necessary. A detaileddescription of the methods used is given elsewhere (Logar et al.,2001).

After the dry biological samples were decomposed by aciddigestion, Hg in the plankton and fish muscle was determined bycold vapor atomic absorption spectrometry with a FIMS using so-dium borohydride as a reducing agent. A detailed description ofthe method used is given elsewhere (Kehrig et al., 2006).

The MeHg analysis in the plankton and muscle was conductedby digesting samples with an alcoholic potassium hydroxide solu-tion, followed by dithizone-toluene extraction. After a series ofclean-up steps, MeHg dithizonate was identified and quantifiedin the toluene layer on a Shimadzu gas chromatograph GC-14 withan electron capture detector-ECD. A detailed description of themethod used is given elsewhere (Kehrig et al., 2006).

The values corresponding to the concentration of inorganicmercury (Hginorg) were calculated as the difference between thevalues found for total mercury and methylmercury concentrations.

The precision and accuracy of the analytical methods weredetermined and monitored using certified material from the Inter-national Atomic Energy Agency (IAEA 350-Tuna fish sample) andNational Research Council-Canada (DORM-2, Dogfish muscle sam-ple and TORT-2 Lobster hepatopancreas). Results for total mercuryDORM-2 (N = 12) ranged from 4.15 to 5.05 mg kg�1, with the CRMpresenting certified Hg values of 4.64 ± 0.26 mg kg�1. For TORT-2(N = 10), total mercury found ranged from 0.26 to 0.32 mg kg�1

with the CRM presenting certified Hg values of 0.27 ± 0.06 mg kg�1.Our routine methylmercury results for reference sample IAEA 350

r individuals (N), feeding habits (FH) and habitat of aquatic biota, and the fish species

FH HabitatSeveral Planktonic

FH Habitat VTGPlanktivorous Pelagic Non-predatorPlanktivorous Pelagic Non-predatorCarnivorous Demersal Intermediary voracious predatorCarnivorous Demersal Intermediary voracious predatorCarnivorous Demersal Intermediary voracious predatorCarnivorous Demersal Intermediary voracious predatorCarnivorous Pelagic-demersal Voracious predator

H.A. Kehrig et al. / Marine Pollution Bulletin 60 (2010) 2350–2356 2353

(N = 39) ranged from 3.21 to 3.97 mg kg�1; while the CRM MeHgvalue was 3.65 ± 0.35 mg kg�1. Recoveries of total mercury andmethylmercury were in agreement with certified values.

Statistical analyses were performed using STATISTICA� 7.0 forWindows (StatSoft, Inc 1984–2004, USA). Descriptive statisticswere used to determine the mean values for duplicates of eachsample (analytical blank CRM, estuarine water, aquatic biota tis-sue) as well as for determining the standard deviation and coeffi-cient of variation for each sample batch. Data was tested fornormal distribution (Shapiro–Wilk’s test) and non-parametric testswere then applied. The analysis of variance was conducted by theKruskal–Wallis test. ANOVA was followed by a post hoc test(Mann–Whitney U-test) in order to define significant differencesin MeHg and Hginorg concentrations among the vertical trophicguilds, as well as along the aquatic food web. A P value of less than0.05 was chosen to indicate statistical significance. Values are pre-sented as mean ± standard deviation (SD) based on a dry weightbasis.

The methylmercury (MeHg) and inorganic mercury (Hginorg)concentrations (on a dry weight basis), [MeHg]/[Hg] and[Hginorg]/[Hg] ratios in water, plankton and fish species sampledfrom Guanabara Bay are summarized in Table 2. The planktonicorganisms, which form the base of the food web at GuanabaraBay, are presented according to microorganism size classes[70–290 (microplankton) and P290 lm (mesoplankton)].

According to the data presented in Table 2, the predominantchemical species of mercury in estuarine water is inorganic, sinceonly 11.2% of the total mercury in water samples was presentedin its organic form, as MeHg. MeHg concentration in water samplescollected at five points in the estuarine portion of Guanabara Bay(Fig. 1) ranged from 0.16 to 0.42 ng L�1 (average 0.28 ± 0.09 ng L�1)(Table 2). The highest concentration of MeHg was found in sam-pling locations near the confluence of ocean and estuarine waters(1 and 5). According to Kehrig et al. (2009c), the microplanktonicsamples collected at these locations, along with samples of estua-rine water used in the present study, were composed of cyanobac-teria, approximately 2% of the total sampled microplankton. Theactivity of sulfate-reducing bacteria, or cyanobacteria, is associatedto the methylation process of inorganic mercury; i.e. with the for-mation of methylmercury (Coelho-Souza et al., 2006). The MeHgvalues in the water column observed in the present study are lowerthan those obtained in 2001 at Minamata Bay (0.53 ± 0.20 ng L�1),which is a reference area for methylmercury studies (Logar et al.,2001).

Planktonic organisms (microplankton and mesoplankton) hadthe lowest MeHg concentrations among all aquatic biota analyzed(Table 2). The MeHg concentration found in microplankton andmesoplankton are not significantly different (P > 0.10). It is worthnoting that the mean MeHg concentrations were approximately

Table 2Methylmercury ([MeHg]) and inorganic mercury ([Hginorg]) mean concentrations (on a dry w

Sample [MeHg] (ng L�1) [Hginorg

Unfiltered water 0.28 ± 0.09 2.22 ± 0[MeHg] (lg kg�1) [Hginorg

PlanktonMicroplankton 8.9 ± 3.6 18.8 ± 7Mesoplankton 35.9 ± 12.3 10.9 ± 1

Fish speciesSardinella brasiliensis 49.1 ± 22.3 33.6 ± 1Mugil liza 41.5 ± 18.4 27.5 ± 1Bagre bagre 297.3 ± 138.7 6.4 ± 3Orthopristis ruber 338.8 ± 283.3 16.7 ± 1Micropogonias furnieri 505.1 ± 283.1 9.3 ± 5Centropomus undecimalis 518.4 ± 137.8 21.6 ± 5Trichiurus lepturus 767.8 ± 368.8 6.2 ± 3

fourfold higher for mesoplankton than for microplankton fromthe five sampling stations within Guanabara Bay. On the otherhand, microplankton presented the highest Hginorg concentrationsand total mercury present as Hginorg. Hginorg concentrations wereapproximately twofold higher for microplankton than those foundin mesoplankton (Table 2).

According to Kehrig et al. (2009c), the microplankton samplesfrom all sampling stations within Guanabara Bay were primarilycomposed of protozooplankton and phytoplankton (59% and 41%,respectively) while approximately 70% of mesoplankton werecomposed mainly of microcrustacean.

In this study, bioaccumulation factor (BAF) is defined as the ra-tio that compares the incorporation of a certain chemical agent(MeHg and Hginorg) by plankton via estuarine water (Gray, 2002).It was expressed in logarithmic units (log units) as: [chemicalagent]plankton/[chemical agent]water.

Water partition coefficients (PCs) in microplankton wereapproximately fourfold higher for MeHg than for Hginorg whenaveraged across the five sampling stations within GuanabaraBay; and water PCs in mesoplankton were 26 times higher forMeHg than Hginorg when averaged across the same samplingstations.

The BAF values calculated for MeHg in microplankton and mes-oplankton from Guanabara Bay were 4.50 and 5.10, and Hginorg BAFscalculated were 3.93 and 3.69, respectively. These results were con-sistent with the known efficient bioaccumulation of these mercuryspecies from the water column by microplankton and mesoplank-ton (Watras et al., 1998). The BAF values for MeHg found in micro-plankton from Guanabara Bay were lower than those found in lakesof Wisconsin and Papua New Guinea (mean 5.43 and 5.36, respec-tively) (Watras et al., 1998; Bowles et al., 2001).

In this study, difference between microplankton and meso-plankton MeHg BAF values was higher (0.60 log units) than Hginorg

BAF (0.24 log units), indicating that trophic transfer of MeHg be-tween planktonic organisms is more efficient than Hginorg transfer-ence. This observation is consistent with Lawson and Mason(1998), once mesoplankton that feed on algal cells (microplankton)assimilate MeHg much more efficiently than Hginorg, presenting therelative assimilation efficiency of MeHg to Hginorg of 2.0.

The assimilation of dissolved mercury in the water column is animportant route for the bioaccumulation of contaminants by aqua-tic organisms that have small body size and greater relative surfacearea, such as microplankton (Reinfelder et al., 1998). However,with the increase in body size of aquatic organisms, as in the caseof mesoplankton, a decrease in the contribution of dissolved mer-cury in the water is observed, and consequently, the trophic trans-fer becomes the more efficient means for assimilation andaccumulation of mercury in the form of methylmercury (Masonet al., 2000).

eight basis), [MeHg]/[Hg] and [Hginorg]/[Hg] ratios in water, plankton and fish species.

] (ng L�1) [MeHg]/[Hg] (%) [Hginorg]/[Hg] (%)

.71 11.2 88.8] (lg kg�1) [MeHg]/[Hg] (%) [Hginorg]/[Hg] (%)

.5 33.8 66.2

.4 75.4 24.6

7.5 59.6 40.41.4 59.9 40.1.0 97.9 2.14.0 95.3 4.7.2 98.2 1.8.7 96.0 4.0.0 99.2 0.8

2354 H.A. Kehrig et al. / Marine Pollution Bulletin 60 (2010) 2350–2356

The Kruskal–Wallis ANOVA test demonstrated the presence ofhighly significant differences (P < 0.0001) in the concentrations ofMeHg and Hginorg between the studied aquatic biota, from theorganisms at the base of the food web of Guanabara Bay (microand mesoplankton), non-predatory fish (S. brasiliensis and M. liza),intermediary voracious predator fish (M. furnieri, C. undecimalis,O. ruber, B. bagre) to the top predator of the web, T. lepturus.

MeHg concentrations and proportion of total mercury present asMeHg increased successively with increasing trophic level in Guana-bara Bay (Table 2), from the planktonic organisms, non-predatoryfish, intermediary voracious predator fish to the voracious predatorfish, corresponding to a transfer between trophic levels from thelower trophic level to the top level predator. However, Hginorg

concentrations and proportion of total mercury as Hginorg presenteda tendency to decrease as trophic level increased, leading to theu-shaped behavior of total mercury in the biota. This indicates thatMeHg was indeed the biomagnified species of mercury. This findingis consistent with earlier observations on the biota of Guanabara Bay(Kehrig et al., 2009b), Gulf of Maine (Chen et al., 2009), North Sea andScheldt Estuary (Baeyens et al., 2003), Papua New Guinea (Bowleset al., 2001), fifteen Wisconsin lakes (USA) (Watras et al., 1998)and Azorean waters (Andersen and Depledge, 1997).

Biomagnification is defined in this study as the increasing con-centration of methylmercury at successively higher trophic levelsof a food web, i.e. when the concentrations in the tissues of oneorganism exceed those found in its food source (Barwick andMaher, 2003). According to Watras et al. (1998) this process resultsfrom trophic transport when consumers absorb contaminants fromcarbon sources (food) and then respire carbon at a rate faster thanthey depurate the contaminant.

Regarding methylmercury dietary intake, which can influencemercury uptake in marine organisms, there is a marked differencebetween the concentrations in microplankton, mesoplankton andfish. Furthermore, the variability of MeHg in the different fish spe-cies is likely to reflect interspecies dietary differences, with corre-sponding different MeHg levels (Frodello et al., 2000). According toWatras et al. (1998), MeHg concentrations at higher trophic levelsreflect an uptake from lower trophic levels, among other factors,such as diet and growth. Due to its lengthy persistence and high

(a)

Fig. 2. Biotransference factors (BTF) of (a) methylmercury and (b) inorganic mercury, whsource.

mobility in the marine ecosystem, methylmercury shows a high le-vel of biomagnification in the upper levels of the food web.

In our study there was a highly significant difference (P < 10�4)for the analyzed MeHg concentration between the muscle of thevoracious predator fish, intermediary voracious predator fish andnon-predatory fish (Table 2) thus indicating there is a significantdifference between MeHg concentrations between the three stud-ied vertical trophic guilds. The muscle tissue of the voracious pred-ator fish, T. lepturus presented the highest MeHg concentrations,followed by the intermediary voracious predator fish (see Table 2),which correspond to the food items of the top web predators(Bittar et al., 2008). MeHg concentrations in the muscle tissue ofT. lepturus were 8.5 times higher than those found in the same tis-sue of intermediary voracious predator fish species.

The intermediary voracious predator fish species, M. furnieri,C. undecimalis, O. ruber, and B. bagre, presented similar MeHg con-centrations in muscle and also feed on similar food sources (inverte-brates and small fish), in this manner they use these sources in thesame way.

The non-predatory fish species (M. liza and S. brasiliensis)showed lower MeHg concentrations in muscle tissue than thosefound in the same tissue of carnivorous fish (Table 2). Therefore,these two planktivorous species that live associated with the sur-face of the water mass and feed on similar food sources, are ex-posed to methylmercury through the planktonic organisms.

Therefore, MeHg concentration reflected the vertical trophicguilds distribution, confirming the initial prediction. The top pred-ator fish of Guanabara Bay, T. lepturus, presented the highest con-centration, followed by the less voracious species, M. furnieri,C. undecimalis, O. ruber and B. bagre, while M. liza and S. brasiliensispresented the lowest MeHg concentrations.

Methylmercury in fish tissues is expected to vary in a widerange of concentration, reflecting feeding behavior and exposureto environmental levels (Reinfelder et al., 1998). However, MeHgcontent in fish varies significantly among species from the samelocation. Rather, tissue MeHg concentrations are controlled bythe dietary habits and size of an organism, the physical and chem-ical characteristics of the system they inhabit, and the magnitudeof human activities in the catchment (Harris et al., 2008).

(b)

ich correspond to the ratio that compares the concentrations between consumer and

H.A. Kehrig et al. / Marine Pollution Bulletin 60 (2010) 2350–2356 2355

In the present study, the trophic transfer of MeHg and Hginorg alongthe food web at Guanabara Bay was assessed by the biotransference ofmercury species. The biotransference factor (BTF) corresponded tothe ratio of the mercury species concentrations, chemical agents,between consumer and source, i.e. [chemical agent]predator/[chemicalagent]prey. The MeHg and Hginorg BTF values are represented in Fig. 2.All trophic interactions examined demonstrated positive MeHg BTFvalues from food source to consumer, i.e. values higher than one unit(1) (Fig. 2a) while Hginorg BTF values did not present this behavior(Fig. 2b) due to they were lower than one unit.

Results demonstrated that all preys (Fig. 2a), which are fooditems for the fish at the top of the web, T. lepturus, showed a posi-tive trophic transfer of MeHg, since MeHg concentrations in pred-ator muscle was higher than those found in their prey, which arefish of different feeding habits and vertical trophic guilds. A posi-tive trophic transfer of MeHg can also be observed between thesefish and their respective prey, microplankton and mesoplankton.

The MeHg concentrations in muscle tissue of M. furnieri isapproximately 5 times the amount found in its preferred prey,mesoplankton, microcrustacean (Vazzoler, 1975), and is also abouteightfold lower than the value found in the tissues of its predator,T. lepturus (Bittar et al., 2008). The MeHg concentrations in themuscle tissue of M. liza is approximately fivefold higher than thevalues found in its preferential prey, microplankton, phytoplank-ton (Blabber, 1997) and is approximately 18 times lower thanthe values found in its predator, T. lepturus (Bittar et al., 2008).

The successive increase in MeHg concentrations along the foodweb accounted for the trophic transfer of MeHg from the base ofthe web, microplankton (primary producer), to mesoplankton (pri-mary consumer), and from these organisms to several fish species,up to the voracious predator fish species at the top of the web. Thesefacts suggest that MeHg biomagnification processes are occurringalong the aquatic food web of Guanabara Bay. However, regardinginorganic mercury, the links studied in this food web presentednegative trophic transfer, since the organisms at its base presentedhigher concentrations of Hginorg than the carnivorous fish.

As in the previous study (Baeyens et al., 2003), the trophictransfer of Hginorg along the food web at Guanabara Bay was notobserved, since the top predator fish of the web had Hginorg concen-trations lower than those obtained in muscle tissue of non-preda-tory fish, and also microplankton and mesoplankton.

Conclusions

Results demonstrated that only organic mercury species, meth-ylmercury, is responsible for mercury biotransference and biomag-nification processes along the aquatic food web of Guanabara Bay.The greatest biomagnification occurred at the bottom of the foodweb and involved the transfer of methylmercury from the watercolumn to planktonic organisms. The proposed dependency ofmethylmercury and inorganic mercury concentrations in plank-tonic organisms and fish on water quality indicates that land useand water quality standards must be more closely watched in or-der to guarantee that best possible practices are in place to preventbioaccumulation of methylmercury and its transfer along theGuanabara Bay food web. Based on our results, it may be suggestedthat feeding habits and vertical trophic guild are important factorsthat influence the patterns of accumulation, trophic transfer andbiomagnification of methylmercury in aquatic biota.

Acknowledgements

The authors would like to thank the Brazilian National Councilfor Scientific and Technological Development-CNPq for the finan-cial support through the course of this work (grant # 476735/

2003-3) and Fundação Carlos Chagas Filho de Amparo à Pesquisado Estado do Rio de Janeiro (FAPERJ # E-26/170.998/2002). Theauthors also thank Dr Ana Paula M. Di Beneditto (UENF) for theinsightful comments on the original version of this manuscript.The paper also was greatly improved by the comments of the anon-ymous reviewer. Special thanks to Rachel Hauser Davis for herassistance in providing this English version.

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