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Ecological Indicators 18 (2012) 291302

Contents lists available at SciVerse ScienceDirect

Ecological Indicators

j ournal homepage : www.elsevier .com/ locate /ecol ind

Trophic relationships and mercury biomagnification in Brazilian tropical coastalfood webs

Tatiana Lemos Bisi a,b,c, , Gilles Lepoint d , Alexandre de Freitas Azevedo b , Paulo Renato Dorneles b,c ,Leonardo Flach e, Krishna Das d, OlafMalm c,Jos Lailson-Brito b

a Programa de Ps-Graduaco em Ecologia, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro 21941-900, BrazilbAquatic Mammal and Bioindicator Laboratory (MAQUA), School of Oceanography, University of Rio de Janeiro State (UERJ), Rio de Janeiro 20550-013, Brazilc Radioisotope Laboratory, Biophysics Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro 21941-900, Brazild Laboratory forOceanology, MARE Centre, University of Liege, Liege B-4000, Belgiume Projeto Boto cinza,Mangaratiba, RJ 23860-000, Brazil

a r t i c l e i n f o

Article history:

Received 1 May 2011

Received in revised form 8 November 2011Accepted 12 November 2011

Keywords:

Tropical ecosystems

Food web

Stable isotope

Heavy metalBioaccumulation

Guiana dolphin

a b s t r a c t

The present study investigatedtrophic relationshipsand mercury flow through food webs ofthree tropical

coastal ecosystems: Guanabara,Sepetiba and Ilha Grande bays. The investigation was carried out throughcarbon and nitrogen stable isotopes (13C, 15N) and total mercury (THg) determination in muscle from

35 species, including crustacean, cephalopod, fish and dolphin species. Detritivorous species showed thelowest average 15N values in all bays. These species were 13C enriched in Sepetiba and Ilha Grande

bays, suggesting the presence of 13C enriched macroalgae in their diet. The highest mean 15N valueswere found in fish and benthic invertebrate feeders, as well as in species presenting demerso-pelagic

feeding habit. The carbon and nitrogen isotopic findings showed different trophic relationship in foodwebs from Sepetiba, Guanabara and Ilha Grande bays. Guanabara Bay showed to be depleted in 15Ncompared to both Sepetiba and Ilha Grande bays. The latter finding suggests substantial contribution of

atmospheric nitrogen fixation by cyanobacteria. A positive linear relationship was found between log THgconcentrations and15N values for Guanabaraand Ilha Grande bays, but not for Sepetiba Bay. Our findings

showed trophic magnification factors (TMF) above 1, demonstrating that THg is being biomagnified upthe food chains in Rio deJaneiro bays.

2011 Elsevier Ltd. All rights reserved.

1. Introduction

In ecosystems, organisms interact through complex trophicrelationships, which involve energy and nutrient flow between

trophic levels. Understanding trophic relationships, as well asquantitatively assessing trophic levels is of fundamental impor-tance for the comprehension of ecosystem structure (Lindeman,1942). In thiscontext, carbon and nitrogen stable isotope measure-

ments have been successfully used for determinating the potential

sources of primary productivity, as well as forassessing trophic lev-elsin food webs, respectively(Daset al., 2003a; Fryand Sherr,1984;Michener and Kaufman, 2007). Therefore, these measurements

provide important information about trophic structure and energyflow through ecological communities (Cabana and Rasmussen,1996; Peterson and Fry, 1987; Vander Zanden et al., 1999). This

Corresponding author at: Universidade Federal do Rio de Janeiro, Instituto de

Biofsica, Laboratrio de Radioistopos, 21941-900, Rio de Janeiro, RJ, Brazil.

Tel.: +5521 25615339; fax: +5521 22808193.

E-mail addresses: [email protected], [email protected] (T.L. Bisi).

approach is possible because the stable isotope composition of aconsumer is the weighting average of those of its food source ina predictive way (DeNiro and Epstein, 1978; Michener and Schell,1994; Minagawa and Wada, 1984; Peterson and Fry, 1987).

Some micropollutants, like mercury (Hg), undergo increasein concentrations upward trophic levels, reaching high concen-trations in top-chain organisms (Renzoni et al., 1998). The highpotential for Hg biomagnification in aquatic systems is due to

the organic form of the metal (mainly methylmercury MeHg),

which in marine vertebrates accumulates preferentially muscle(Baeyens et al., 2003; Francesconi and Lenanton, 1992; Wagemannet al., 1998). With regard to the absorption of mercurial species

through the gastrointestinal tract, MeHg is the most efficientlytaken up form of Hg (Wagemann et al., 1998). Therefore, study-ing trophic relationships among organisms is also important fora better understating of contaminant bioaccumulation and bio-

magnification processes. In this context, several studies have usednitrogen stable isotopes as indicators of trophic level forinvestigat-ing contaminant transfer upward marine food webs (Atwell et al.,1998; Das et al., 2003b; Dehn et al., 2006; Loseto et al., 2008a;

McKinney et al., 2011).

1470-160X/$ seefront matter 2011 Elsevier Ltd. Allrights reserved.

doi:10.1016/j.ecolind.2011.11.015
http://localhost/var/www/apps/conversion/tmp/scratch_5/dx.doi.org/10.1016/j.ecolind.2011.11.015http://www.sciencedirect.com/science/journal/1470160Xhttp://www.elsevier.com/locate/ecolindmailto:[email protected]:[email protected]://localhost/var/www/apps/conversion/tmp/scratch_5/dx.doi.org/10.1016/j.ecolind.2011.11.015http://localhost/var/www/apps/conversion/tmp/scratch_5/dx.doi.org/10.1016/j.ecolind.2011.11.015mailto:[email protected]:[email protected]://www.elsevier.com/locate/ecolindhttp://www.sciencedirect.com/science/journal/1470160Xhttp://localhost/var/www/apps/conversion/tmp/scratch_5/dx.doi.org/10.1016/j.ecolind.2011.11.015

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292 T.L. Bisi et al./ Ecological Indicators 18 (2012) 291302

Although there are a number of food web studies dealing with

stable isotope ratios and micropollutant flow, these investigationsusually focus on northern hemisphere areas, mainly in temperateand polar regions (e.g., Das et al., 2003a; Dehn et al., 2006; Hobsonet al., 2002). In tropical areas, only a few studies have dealt with

trophic relationships in estuarine and marine food webs using sta-ble isotope measurements (Abreu et al., 2006; Corbisieret al., 2006;Lin et al., 2007). Tropical regions are characterized by high speciesrichness (Begon et al., 2006), which probably promotes more com-

plex trophic relationships due to greater diversity of food items foreach species (Paine, 1966).

The present studyfocuses on threedifferent tropical coastal foodwebs located in a regionunderhighanthropogenic pressure,the Rio

de Janeiro State. Nevertheless, these environments present differ-ent degradation levels. Guanabara Bay is the most degraded areaamong the studied bays. The estuary is considered to be the mostdegraded system of Brazilian coast (FEEMA, 1990; Kjerfve et al.,

1997). Sepetiba Bay presents an intermediate degree of contami-nation, but it has undergone a significant increase in pollution overthe last decades (Lacerda et al., 1987; Molisani et al., 2004). Besides,the Sepetiba Bay drainage basin harbors an expanding industrial

park (IFIAS, 1998), which can result in worsening of the degrada-tion scenario. Among the systems considered in the present study,

Ilha Grande Bay is the most preserved one. The estuary is consid-ered to be a biodiversity hotspot and includes a high number of

protected areas (Creed et al., 2007a).The objectives of the present study were: (1) to investigate the

trophic relationships among organisms from food webs of threetropical coastal ecosystems: Guanabara, Sepetiba and Ilha Grande

bays, (2) to compare the trophic structure from the three foodwebs investigated, (3) to calculate the trophic magnification fac-tors (TMF) of total mercury (THg) between the Guiana dolphin andits prey, and (4) to assess the influence of several factors, such as

the trophic position of the Guiana dolphin, on Hg accumulation.

2. Material and methods

2.1. Sampling

Muscle samples were obtained from Guiana dolphins, Sotaliaguianensis, that were either incidentally captured in gillnet fisheryor stranded on the beaches of the three bays of Rio de Janeiro Statebetween 1995 and 2009: the Guanabara Bay (n= 20), the Sepetiba

Bay (n= 44) and the Ilha Grande Bay (n=10). All samples werestored at20 C until analysis.

The species preyed by S. guianensis were previously identifiedfrom stomach content analysis. They include fish, cephalopod and

crustacean species (Azevedo et al., 2008; Azevedo, unpublisheddata).Samplingwas performedin winter2008 (August to October

dry season) and summer 2009 (February and March wet season).Samples from 34 prey species (five invertebrate and 29 fish speciesfrom distinct feeding habitats) were acquired in fishing landingsinside Guanabara, Sepetiba and Ilha Grande bays (813 individuals).All specimens were sampled at the body length on which Guiana

dolphins prey (Azevedo et al., 2008; Azevedo, unpublished data).Concerning the scianid fish Micropogonias furnieri, the specimenswere sorted out in two groups regarding their length. M. furnierifitting the size on which Guiana dolphins exert predation were

categorized in group d, as well as individuals larger than 40cmwere placedin group 40. Thespecimenswere weighed, measuredand dissected. All samples were frozen and stored at 20 C untilanalysis.

Seston samples were collected using 75-nm-mesh plankton net

in the inner part, at low tide,as well as in theentrance, at high tide,

of each bay. This sampling wascarried out in July 2008(winter) and

January 2009 (summer).

2.2. Stable isotope measurements

Stable isotopes measurements of carbon and nitrogen werecarried out in muscle samples from Guiana dolphins, fishes andinvertebrates. After being dried at 60 C (72 h ), samples were

groundinto a homogeneous powder. Since allmuscle samples fromthe present study presented low lipid content (C:N< 4.0), no lipidextractions were carried out (Post et al., 2007). Stable isotope mea-surementswere performedon a V.G. Optima(Isoprime, UK)isotope

ratio mass spectrometer coupled to an N-C-S elemental analyzer(Carlo Erba). Reference materials (IAEA CH-6 and IAEA-N1) werealso analyzed and the precision of replicate analyses was 0.3.Stable isotope ratios are expressed in delta notation as part per

thousand. Carbon and nitrogen ratios are expressed relative to theV-PDB (Vienna Peedee Belemnite) standard and to atmosphericnitrogen, respectively.

2.3. Total mercury (THg) determination

Aliquots of approximately 0.4 g of muscle (wet weight) were

digested with 1 mLof hydrogen peroxide and 5 mLof sulfuric:nitricacid mixture (1:1). The solution was then heated to 60C for 2 hin a water bath, which was followed by the addition of 5mLofpotassiumpermanganate 5% solution and heating to 60 C for more15min. After overnight digestion, THg concentration was deter-

mined by Cold Vapor/AAS (FIMS-400, Perkin-Elmer) with sodiumborohydride as reducing agent. Blanks were carried through theprocedure in the same way as the sample. The standard referencematerial DORM-3 (National Research Council, Canada) was ana-

lyzed in every run and our results were in good agreement withcertified values (mean recoverySD=101.443.57%).

2.4. Statistical analysis

Mean carbon and nitrogen isotopic values were calculatedfor Guiana dolphins and for each prey species. The fish specieswere classified into five feeding types (see Tables 1 and 2). The

KolmogorovSmirnov test was used in order to test fornormality ofthe data. ANOVA and post hoc Tukey tests were used forcomparingnitrogen and carbon isotopic values amongfeeding types(includingcephalopod and crustacean species) and among the three bays. The

nonparametric KruskalWallis and post hoc multiple comparisontests were applied when the data distribution did not follow therules of normal distribution. The nonparametric MannWhitney

U test was performed for comparison between seasons (win-

ter summer sampling). Simple linear regression analysis wasused for investigating relationships between 15N and logarith-mic concentrations of THg, as well as for determinating trophic

magnification factors (TMF). TMF is calculated as the antilog ofthe regression slope with base 10 and can be used for quantify-ing food web biomagnification (Borg et al., 2011; Fisk et al., 2001).Therefore, this tool was used forcalculating Hg biomagnification indifferent ecosystems.

3. Results and discussion

3.1. Trophic relationships

Summaries of 13C and 15N values for cephalopods, crus-taceans, fishes and Guiana dolphins are given in Tables 1 and 2,respectively, as well in Fig. 1.

Carbon isotope ratioshave proved to be usefulin identifying the

relative input of dietaryresources from differentfood webs, as13

C

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Table 1

Mean 13C values() SD and numberof individuals (n) of seston, cephalopods, crustaceans,fishes and Guiana dolphin from Guanabara, Sepetibaand Ilha Grande bays, Rio

deJaneiro State.

Species Guanabara Bay Sepetiba Bay Ilha Grande Bay

Winter Summer Winter Summer Winter Summer

Seston

Inner 19.4 19.0 19.0 14.6 22.5 19.4

Entrance 18.5 n.d. 16.6 18.2 20.6 18.5

Cephalopods

LoliginidaeLoligoplei 18.90.5 16.10.1 18.60.3

(n= 6) (n= 3) (n= 6)

Loligo sanpaulensis 18.20.3 15.90.5 17.60.7

(n= 7) (n= 5) (n= 6)

Lolliguncula brevis 17.11.1 14.51.1

(n= 10) (n= 4)

Crustaceans

Penaeidae

Farfantepenaeus brasiliensis 15.30.7 15.10.9

(n= 5) (n= 5)

Litopenaeus schmitt 15.60.6 15.20.2 14.30.2 14.00.8

(n= 6) (n= 3) (n= 5) (n= 5)

Fishes

Ariidae

Aspistor luniscutisa 15.41.4 13.20.2

(n= 6) (n= 6)

BatrachoididaePorichthys porosissimusb 18.90.5 17.60.5 18.80.8 18.90.0 18.50.4

(n= 5) (n= 3) (n= 5) (n= 3) (n= 6)

Carangidae

Chloroscombrus chrysurusc 15.10.5 14.70.6 14.90.4 13.10.4 17.60.2 16.60.5

(n= 5) (n= 6) (n= 6) (n= 6) (n= 6) (n= 6)

CentropomidaeCentropomus spp.b 20.91.3 14.30.1 14.31.1 14.71.6 15.80.7 16.80.2

(n= 6) (n= 3) (n= 6) (n= 6) (n= 6) (n= 3)

Clupeidae

Sardinella brasiliensisd 15.60.4 19.60.6 16.30.6 15.20.6 15.70.1 18.31.0

(n= 6) (n= 6) (n= 6) (n= 6) (n= 5) (n= 6)

Cynoglossidae

Symphurus tesselatusa 15.20.3 14.20.6 16.70.5

(n= 6) (n= 3) (n= 6)

Engraulididae

Anchoa spp.d 15.90.3 15.10.3 14.90.2 14.10.4

(n= 6) (n= 6) (n= 6) (n= 6)Cetengraulis edentulusd 14.10.5 14.80.6 15.70.6 14.40.5

(n= 6) (n= 6) (n= 4) (n= 6)

Engraulis anchoitad 14.90.2

(n= 6)

Haemulidae

Orthopristis rubera 14.20.9 13.80.5

(n= 6) (n= 6)

Mugilidae

Mugil curemae 9.41.4 11.10.9

(n= 4) (n= 5)

Mugil Lizae 14.40.9 13.91.0(n= 5) (n= 6)

Mugil spp.e 17.80.7 10.91.4 10.61.1

(n= 5) (n= 5) (n= 6)

Paralichthydae

Paralichthys patagonicusa 18.030.5

(n= 4)

Sciaenidae

Ctenosciaena gracilicirrhusa 19.20.3 14.50.3

(n= 4) (n= 6)

Cynoscion guatucupab 17.2 17.00.8 17.10.4 16.3 17.90.1 17.70.3

(n= 1) (n= 6) (n= 6) (n= 1) (n= 6) (n= 6)Cynoscion jamaicensisb 18.90.3 15.80.9 15.61.1 16.20.7

(n= 6) (n= 6) (n= 6) (n= 6)

Cynoscion leiarchusb 16.30.1 13.90.4 12.61.1 14.00.6 16.70.8

(n= 5) (n= 6) (n= 5) (n= 6) (n= 5)

Isopisthus parviponnisb 15.30.6 14.20.4 18.00.7 16.50.6

(n= 6) (n= 6) (n= 6) (n= 6)

Larimus brevicepsb 17.70.7 15.340.7

(n= 6) (n= 6)

Menticirrhus americanusa 12.80.4 14.40.6

(n= 4) (n= 6)

Micropogonias furnieri da 16.30.8 16.21.0 13.81.7 13.41.4 16.51.2 16.20.7(n= 14) (n= 13) (n= 13) (n= 13) (n= 14) (n=13)

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Table 1 (Continued)



Micropogonias furnieri 40b 16.11.4 15.41.6 14.71.4 14.32.0 16.60.4 16.30.9

(n= 7) (n= 7) (n= 7) (n= 6) (n = 10) (n= 8)

Paralonchurus brasiliensisa 17.80.7 16.70.4 15.50.7 14.00.3 17.00.8 16.30.3

(n= 6) (n= 6) (n= 5) (n= 6) (n = 6) (n= 6)

Stellifer rastriferb 15.10.1 14.40.2 17.10.5 16.30.3

(n= 3) (n= 5) (n = 3) (n= 2)

Stellifer stelliferb 14.40.1 13.9 18.50.2 15.60.0(n= 3) (n= 1) (n = 2) (n= 2)

Umbrina canosaia 17.60.1 17.70.2

(n= 6) (n = 6)

Serranidae

Diplectrum radialea 14.20.2 14.50.4

(n= 6) (n= 2)

Serranus aurigaa 15.90.2 15.00.5 15.1 15.10.4

(n= 6) (n= 6) (n= 1) (n= 6)

Sparidae

Pagruspagrusc 18.50.4 18.70.3 18.90.7 16.90.2 18.20.2 17.30.2

(n= 6) (n= 6) (n= 6) (n= 6) (n = 6) (n= 6)

TrichiuridaeTrichiurus lepturusc 17.20.8 13.80.5 17.80.1 17.40.7

(n= 5) (n= 6) (n = 5) (n= 5)

Cetacea

Sotalia guianensis 14.00.7 14.51.0 16.60.4

(n= 20) (n= 44) (n=10)

n.d. notdetermined.

blank not analyzed.a Fish feeding type: benthic invertebrate feeder.b Fish feeding type: fish and benthic invertebrate feeder.c Fish feeding type: demerso-pelagic predator.d Fish feeding type: planktivorous.e Fish feeding type: detritivorous.

values are typically higher in species from coastal or benthic food

webs than in those from offshore or pelagic food webs (Hobson,1999; McConnaughey and McRoy, 1979). Some fish and cephalopodspecies were found to be depleted in 13C in Sepetiba and Guan-abara bays (Fig. 1) (from 18.9 to 17.1 in winter and from

16.9 to16.3 insummer, forSepetibaBay;as well asand from

20.8 to 17.2 in winter and from19.6 to 16.7 in sum-mer, for Guanabara Bay). Some of these species (e.g.,Paralonchurusbrasiliensis, Cynoscion guatucupa, Umbrina canosai and Porichthys

porosissimus) are marine organisms that use estuaries opportunis-tically or optionallyduring larval, juvenile, sub-adult and even adultstage (Sinque and Muelbert, 1997). Therefore, our findings may beindicatingthat, forsome species, the primary carbon source is from

a neritic food weboutside the bays. These findingssuggest complexprocesses and pointed to the need for detailed investigation for abetter understanding of the multiple sources of carbon in the foodwebs of Sepetiba and Guanabara bays.

Mean 13C and 15N values varied significantly amongprey feeding types of Sepetiba Bay (ANOVA, F6,132 =15.86 and

F6,132 = 72.92 in winter, F6,137 = 14.28 and F6,137 = 50.78 in summer,

p< 0.00001), Guanabara Bay (ANOVA, F6,69 = 9.8 and F6,69 = 5 .6 towinter, F6,66 =16.5andF6,66 = 3.7 to summer, respectively,p

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Table 2

Mean 15N values ()SD and number of individuals (n) of seston, cephalopods, crustaceans, fishes and Guiana dolphins from Guanabara, Sepetiba and Ilha Grande bays,

Rio de Janeiro State.



Seston

Inner n.d. n.d. n.d. 8.9 n.d. 7.1

Entrance n.d. n.d. 7.6 8.3 n.d. n.d.

Cephalopods

LoliginidaeLoligoplei 12.40.8 15.50.1 14.00.4

(n= 6) (n= 3) (n= 6)

Loligo sanpaulensis 13.90.6 14.20.4 14.50.7

(n= 7) (n= 5) (n= 6)


(n= 10) (n= 4)

Crustaceans

Penaeidae

Farfantepenaeus brasiliensis 12.20.4 11.80.9

(n= 5) (n= 5)

Litopenaeus schmitt 8.72.3 10.81.2 11.60.9 11.30.6

(n= 6) (n= 3) (n= 5) (n= 5)

Fishes

Ariidae

Aspistor luniscutisa 13.91.2 14.50.7

(n= 6) (n= 6)

BatrachoididaePorichthys porosissimusb 12.10.2 12.70.0 12.80.3 12.50.2 12.60.1

(n= 5) (n= 3) (n= 5) (n= 3) (n= 6)

Carangidae

Chloroscombrus chrysurusc 13.32.2 14.10.3 15.90.3 15.60.3 14.10.3 14.60.3

(n= 5) (n= 6) (n= 6) (n= 6) (n= 6) (n= 6)

CentropomidaeCentropomus spp.b 13.60.9 13.20.8 15.30.9 15.10.9 13.70.8 14.90.3

(n= 6) (n= 3) (n= 6) (n= 6) (n= 6) (n= 3)

Clupeidae

Sardinella brasiliensisd 10.50.2 10.50.3 13.00.3 13.30.2 13.20.5 11.60.4

(n= 6) (n= 6) (n= 6) (n= 6) (n= 5) (n= 6)

Cynoglossidae

Symphurus tesselatusa 14.20.7 14.31.2 12.10.4

(n= 6) (n= 3) (n= 6)

Engraulididae

Anchoa spp.d 12.30.7 13.40.5 14.60.3 14.90.53

(n= 6) (n= 6) (n= 6) (n= 6)Cetengraulis edentulusd 11.00.8 11.12.2 13.80.1 14.30.4

(n= 6) (n= 6) (n= 4) (n= 6)

Engraulis anchoitad 15.10.1

(n= 6)

Haemulidae

Orthopristis rubera 15.10.2 14.61.3

(n= 6) (n= 6)

Mugilidae

Mugil curemae 9.20.3 10.00.8

(n= 4) (n= 5)

Mugil Lizae 10.401.45 9.60.8(n= 5) (n= 6)

Mugil spp.e 9.32.1 9.40.7 8.81.3

(n= 5) (n= 5) (n= 6)

Paralichthydae

Paralichthys patagonicusa 13.20.5

(n= 4)

Sciaenidae

Ctenosciaena gracilicirrhusa 15.70.2 14.90.4

(n= 4) (n= 6)

Cynoscion guatucupab 15.7 13.90.2 14.30.2 13.9 14.20.2 13.90.2

(n= 1) (n= 6) (n= 6) (n= 1) (n= 6) (n= 6)Cynoscion jamaicensisb 14.20.1 13.90.3 14.30.8 14.80.5

(n= 6) (n= 6) (n= 6) (n= 6)

Cynoscion leiarchusb 9.60.4 12.71.1 15.90.2 15.10.5 13.40.2

(n= 5) (n= 6) (n= 5) (n= 6) (n= 5)

Isopisthus parviponnisb 15.80.3 16.060.43 14.30.3 14.50.9

(n= 6) (n= 6) (n= 6) (n= 6)

Larimus brevicepsb 14.80.5 15.80.5

(n= 6) (n= 6)

Menticirrhus americanusa 13.11.5 14.90.9

(n= 4) (n= 6)

Micropogonias furnieri da 10.31.6 11.31.9 13.21.1 13.41.1 14.10.8 13.80.9(n= 14) (n= 13) (n= 13) (n= 13) (n= 14) (n=13)

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Table 2 (Continued)



Micropogonias furnieri 40b 13.90.8 12.42.09 15.00.73 14.60.86 14.70.5 14.60.5

(n= 7) (n= 7) (n= 7) (n= 6) (n= 10) (n= 8)

Paralonchurus brasiliensisa 14.50.6 14.20.6 14.80.3 14.90.3 13.60.6 13.60.7

(n= 6) (n= 6) (n= 5) (n= 6) (n= 6) (n= 6)

Stellifer rastriferb 15.40.3 15.90.4 14.30.5 14.10.1

(n= 3) (n= 5) (n= 3) (n= 2)

Stellifer stelliferb 16.30.0 15.817 13.630.08 14.20.0(n= 3) (n= 1) (n= 2) (n= 2)

Umbrina canosaia 13.90.4 13.70.3

(n= 6) (n= 6)

Serranidae

Diplectrum radialea 14.90.3 14.30.2

(n= 6) (n= 2)

Serranus aurigaa 11.41.3 13.50.3 14.3 13.20.3

(n= 6) (n= 6) (n= 1) (n= 6)

Sparidae

Pagruspagrusc 12.90.2 12.10.8 13.10.6 14.10.2 13.60.2 14.20.2

(n= 6) (n= 6) (n= 6) (n= 6) (n= 6) (n= 6)

TrichiuridaeTrichiurus lepturusc 14.90.8 16.60.4 14.60.4 14.20.3

(n= 5) (n= 6) (n= 5) (n= 5)

Cetacea

Sotalia guianensis 14.20.9 14.00.6 14.20.6

(n= 20) (n= 44) (n=10)

n.d. notdetermined.

blank not analyzed.a Fish feeding type: benthic invertebrate feeder.b Fish feeding type: fish and benthic invertebrate feeder.c Fish feeding type: demerso-pelagic predator.d Fish feeding type: planktivorous.e Fish feeding type: detritivorous.

3.2. Comparison among bays

The carbon and nitrogen isotopic findings pointed to differenttrophic relationships in the food webs of Sepetiba, Guanabara andIlha Grande bays. The three studied bays are under anthropogenic

pressure, but in different degradation levels. As mentioned, Gua-

nabara Bay is the most degraded estuary among the three studiedbays. In fact, it is consideredto be oneof themost degraded systemsofBraziliancoast(FEEMA,1990;Kjerfveetal.,1997). The Guanabara

Bay food web showed less complex trophic relationships than didSepetiba andIlha Grande bays. In Sepetiba and Ilha Grande bays thetrophic relationships among the fish species were not well definedand the systems seem to be complex, as it is expected for tropical

food webs. The high biodiversity found in these systems probablypromotes great varietyof prey foreach predator (Paine, 1966). Con-cerning fish and benthic invertebrate feeders and demerso-pelagicspecies from Sepetiba and Ilha Grande bays, it was not possible to

determine specific groups of prey through nitrogen isotopic val-ues. This finding suggests that these species are preying on severaldifferent taxa.

Ilha Grande Bay showed significant depleted 13C values forall feeding types (except for detritivorous species), as well as

for Guiana dolphins, compared to Guanabara and Sepetiba baysboth in winter and summer season (Tukey HSD test, p

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Table 4

Mean 13C values () of invertebrate species, cephalopods, benthic invertebrate feeder, fish and benthic invertebrate feeder, demerso-pelagic predator, planktivorous and

detritivorous from Guanabara, Sepetiba and Ilha Grande bays, Rio de Janeiro State.

Guanabara Bay Sepetiba Bay Ilha Grande Bay


Invertebrates 15.6 15.2 14.8 14.6

Detritivorous 17.8 14.4 12.1 11.1 10.9 10.6

Planktivorous 15.2 14.9 15.6 14.7 15.7 18.2

Benthic invertebrate feeder 16.2 15.8 14.5 14.0 17.0 16.3

Fish and benthic invertebrate feeder 16.1 14.9 14.6 14.3 17.1 16.5Demerso-pelagic predator 15.1 14.7 14.9 13.3 17.9 17.1

Cephalopods 17.1 18.9 17.6 15.3 18.6 17.6

Fig. 1. Trophic structure of Sepetiba, Guanabara and Ilha Grande bays food webs as determinate from stable isotope carbon and nitrogen ratios (mean SE). seston,crustacean, cephalopod, detritivorous, planktivorous, benthic invertebratefeeder, fish and benthic invertebratefeeders, demerso-pelagic, Guianadolphin.

(For interpretation of thereferences to color in this figure legend, thereader is referred to theweb version of thearticle.)

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Table 5

Mean musculartotal mercury (THg) concentration(ng/g)SDand number of individuals (n) cephalopods,crustaceans,fishes and Guiana dolphins fromGuanabara, Sepetiba

and Ilha Grande bays,Rio de Janeiro State.a



Cephalopoda

Loliginidae

Loligoplei 21.187.3

(n= 6)

Loligo sanpaulensis 12.34.1(n= 6)


(n= 9) (n= 4)

Crustacea

Penaeidae

Litopenaeus schmitti 3.61.8 4.22.1 6.51.5

(n= 6) (n= 6) (n= 5)

Fishes

Ariidae

Aspistor luniscutis 24.226.1 8.52.7

(n= 6) (n= 6)

BatrachoididaePorichthys porosissimus 62.929.8 28.37.8

(n= 3) (n= 5)

Carangidae

Chloroscombrus chrysurus 20.27.1 44.7716.4 31.216.1 19.09.3 99.561.7 51.816.4

(n= 5) (n= 4) (n= 6) (n= 6) (n= 6) (n= 6)Centropomidae

Centropomus spp. 65.722.1 33.523.1 44.79.9 80.738.7 169.021.4

(n= 3) (n= 6) (n= 6) (n= 6) (n= 3)

Clupeidae

Sardinella brasiliensis 27.86.3 5.02.0 5.80.8 4.61.1 20.56.6

(n= 6) (n= 6) (n= 6) (n= 6) (n= 6)Cynoglossidae

Symphurus tesselatus 4.42.2 8.32.9 7.61.4

(n= 6) (n= 3) (n= 5)

Engraulididae

Anchoa spp. 93.150.4 43.48.0 29.87.1 32.612.2

(n= 6) (n= 6) (n= 6) (n= 6)

Cetengraulis edentulus 15.48.1 27.99.6 7.84.5 8.00.8

(n= 6) (n= 6) (n= 4) (n= 6)

Engraulis anchoita 59.67.1

(n= 6)

HaemulidaeOrthopristis ruber 15.810.6 15.46.9

(n= 6) (n= 6)

Mugilidae

Mugil liza 12.13.6

(n= 5)

Mugil spp. 6.71.3

(n= 5)

Paralichthydae

Paralichthys patagonicus 18.21.6

(n= 4)

SciaenidaeCtenosciaena gracilicirrhus 12.77.0 18.22.7

(n= 4) (n= 6)

Cynoscion guatucupa 41.79.5 19.65.0

(n= 6) (n= 6)

Cynoscion jamaicensis 54.939.4 47.030.2 27.87.4

(n= 6) (n= 6) (n= 6)

Cynoscion leiarchus 66.99.8 44.38.7 27.55.0 24.414.1 49.318.7

(n= 4) (n= 6) (n= 5) (n= 6) (n= 5)

Isopisthus parvipinnis 12.56.8 44.910.8 70.434.3 44.037.4

(n= 6) (n= 6) (n= 6) (n= 6)

Larimus breviceps 16.88.04(n= 6)

Menticirrhus americanus 10.57.5 19.938.40

(n= 4) (n= 6)

Micropogonias furnieri d 83.4107.9 23.823.4 7.16.5 7.465.9 33.133.4 49.743.2

(n= 14) (n= 13) (n= 12) (n= 12) (n= 11) (n=13)

Micropogonias furnieri 40 252.7214.5 111.246.4 107.6134.0 135.599.5 264.096.8 226.1126

(n= 7) (n= 7) (n= 7) (n= 5) (n= 10) (n= 7)

Paralonchurus brasiliensis 10.466.0 5.81.5 16.95.0 13.82.9

(n= 5) (n= 6) (n= 6) (n= 6)

Stelliferrastrifer 6.11.3 19.410.2 26.415.6 38.84.1

(n= 3) (n= 5) (n= 2) (n= 2)Stelliferstellifer 14.53.7 24.4 24.010.9 53.516.7

(n= 3) (n= 1) (n= 3) (n= 2)

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Table 5 (Continued)



Umbrina canosai 126.531.1

(n= 6)

Serranidae

Diplectrum radiale 15.87.3 20.40.2

(n= 6) (n= 2)

Serranus auriga 66.523.9 90.321.3 9.5 12.51.2

(n= 6) (n= 6) (n= 1) (n= 6)Sparidae

Pagruspagrus 39.212.1 34.85.9

(n= 6) (n= 6)

Trichiuridae

Trichiurus lepturus 36.39.5 37.112.8 22.517.1

(n= 6) (n= 5) (n= 5)

Cetacea

Sotaliaguianensis 920.3656.2 269.2332.3 688.4221.8

(n = 12) (n= 42) (n= 9)

Blank notanalyzed.a Total mercury determination was notcarried out in species that were depleted in13 C.

16.7 in winterand from 13.7 to16.8 in summer) andfor those

species of demerso-pelagic feeding habit (from 15.5 to 16.5in winter and from 15.2 to 17.1 in summer) (multiple com-parison test, p< 0.0012). Since 15N values can vary from systemto system even when the same species is considered (Cabana andRasmussen, 1996), caution should be taken when comparing 15N

values between food webs.Several studies have reported more 15N-enriched values in

organisms from areas undergoing eutrophication process due tocity sewage, effluents of industries and agricultural fertilizers

(Abreu et al., 2006; McClelland and Valiela, 1998; Olsen et al.,2010). Interestingly, Guanabara Bay, the most eutrophicated sys-tem among the three sampled areas, showed depleted 15N valuescompared to both Sepetiba and Ilha Grande bays. Phytoplankton in

Guanabara Bay is dominated by nanoplanktonic and cyanobacte-

ria species (Valentin et al., 1999). Therefore, our findings may bereflecting a substantial input of atmospheric nitrogen fixation bycyanobacteria, which results in low 15N values (Carpenter et al.,

1997; McClelland et al., 2003). In contrast, Kalas et al. (2009) foundenriched15N valuesin particulate organic matter from GuanabaraBay. The authors suggested it could be due to the incorporationof isotopically heavy residual NH4+ by the phytoplankton. How-

ever, the sampling was performed in 1999 and 2000. The distinctresults obtained through this 10-year interval between the inves-tigation carried out by Kalas et al. (2009) and the present studymay suggest worsening in the Guanabara Bay degradation process

over thetime.The presence ofcyanobacteriais usually associated tothe eutrophication process. The fact that organism from GuanabaraBay food web present relatively low nitrogen isotopic values prob-ably reflects elevated cyanobacteria density in this estuary. These

findings point out an accelerated eutrophication process that indi-cates a much higher degradation condition in Guanabara Bay thanit could be assumed previously.

3.3. THg15N relationships

Average muscular total mercury concentration (THg) was low-est in Litopenaeus schmitt (3.6ng/g in Guanabara Baywinter and

4.2 ng/g in Sepetiba Baywinter)andin Sardinella brasiliensis (4.6ng/gin Ilha Grande Baywinter) and highest in Guiana dolphin (920.3 ng/gin Guanabara Bay, 269.2ng/g in Sepetiba Bay and 688.4 ng/g inIlha Grande Bay) (Table 5). THg concentrations in prey species

increased successively with increasing trophic level in Guan-

abara, Sepetiba and Ilha Grande bays, except for those species of

demerso-pelagic feeding habitat. Detritivorous and invertebrate

species displayed the lowest mean 15N values as well as thelowest THg concentrations, while fish and benthic invertebratefeeders showed the highest mean 15N values and THg concentra-tions (KruskalWallis test, p< 0.0009). However, demerso-pelagicspecies present equivalent high15N values, but their THg concen-

trations were intermediate.A positive linear relationship was found between log-

transformed concentrations of THg and15N values for Guanabaraand Ilha Grande bays (linear regression, p0.06) (Fig. 2). Trophic magnification factors (TMF) were above1 (Table 6), which indicates mercury accumulation in the food weband suggests diet as the major exposure route for this element

(Borg et al., 2011; Gray, 2002) in these bays. Muscular mercury in

fish and marine mammals exists predominantly in organic forms,which are efficiently incorporated by food intake (Francesconi andLenanton, 1992; Wagemann et al., 1998).

The TMF values for Guanabaraand Ilha Grande bays (1.511.67)were similar to those observed in arctic marine food web (1.59 value converted from slope of the regression to TMF for com-parison to our results) by Atwell et al. (1998) and in Gulf of St.

Lawrence (1.48 value converted) by Lavoie et al. (2010). They areslightly lower than those reported for three food webs from Beau-fort Sea (ca. 1.8 value converted) by Loseto et al. (2008a). ForAlaskan Arctic region, Dehn et al. (2006) found an extremely high

TMF value (25.12 value converted). Differently from Atwell et al.(1998), Loseto et al. (2008a), Lavoie et al. (2010) and the presentstudy, the investigation performed by Dehn et al. (2006) focusedlargely on marine mammals rather than on overall mercury bio-

magnification through many taxonomic groups. Unbalanced studydesigns that include large numbers of high trophic level species,as in the investigation performed by Dehn et al. (2006), may affectthe TMF results, so that TMF values can reflect biomagnification at

these higher trophic levels rather than at full food web (Borg et al.,2011).

Conversely, aspects other than biomagnification may be influ-encing mercury bioaccumulation in some species from Rio de

Janeiro bays. This is especially evident in Sepetiba Bay, where alinear relationship between logTHg concentrations and 15N val-ues was not observed. Guiana dolphin showed the highest meanmercury concentration (269.23ng/g) for Sepetiba Bay, but not the

highest 15N values. This finding may be associated to bioaccumu-lation over the time as well as to a great body mass, which requires

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Table 6

Trophic Magnification factors (TMF) and simple linear regression values among log of THg concentration and15N value to Sepetiba, Guanabara and Ilha Grande bays food

webs, Riode Janeiro Coast.

n Slope SEslope TMF Intercept R2 p-Value

Sepetiba Baywinter 155 0.07 0.04 1.19 0.31 0.02 0.0942

Sepetiba Baysummer 175 0.07 0.04 1.17 0.46 0.02 0.0665

Guanabara Baywinter 86 0.19 0.03 1.55 0.52 0.36 0.0001Guanabara Baysummer 74 0.18 0.03 1.51 0.51 0.30 0.0001

Ilha Grande Baywinter 105 0.21 0.07 1.63 1.22 0.07 0.0053

Ilha Grande Baysummer 100 0.22 0.05 1.67 1.50 0.19 0.0001

a higher food intake by the species. There is little evidence that THg

accumulates in muscle tissue with age in cetaceans (Atwell et al.,1998; Loseto et al., 2008b), but positive relationship between THgand body length was found (Loseto et al., 2008b).

Regarding most fish species and Guiana dolphins, higher THg

concentrations were found in Guanabaraand Ilha Grande bays thanin Sepetiba Bay (p< 0.05). Ilha Grande and Sepetiba bays are adja-cent bodies of waterthat are connected to each other by a channel.

Fig. 2. Relationship between 15N values and log-transformed concentrations of total mercury (THg) in organisms from the Sepetiba, Guanabara and Ilha Grande bays

food webs, Rio de Janeiro Coast. crustacean, cephalopod, detritivorous, planktivorous, benthic invertebrate feeder, fish and benthic invertebrate feeders,

demerso-pelagic, Guiana dolphin.

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