Trophic relationships and mercury biomagnification in Brazilian tropical coastal food webs

Ecological Indicators 18 (2012) 291–302

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Trophic relationships and mercury biomagnification in Brazilian tropical coastal food 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 , Olaf Malm c , José Lailson-Brito b a

Programa de Pós-Graduac¸ão em Ecologia, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro 21941-900, Brazil Aquatic Mammal and Bioindicator Laboratory (MAQUA), School of Oceanography, University of Rio de Janeiro State (UERJ), Rio de Janeiro 20550-013, Brazil c Radioisotope Laboratory, Biophysics Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro 21941-900, Brazil d Laboratory for Oceanology, MARE Centre, University of Liege, Liege B-4000, Belgium e Projeto Boto cinza, Mangaratiba, RJ 23860-000, Brazil b

a r t i c l e

i n f o

Article history: Received 1 May 2011 Received in revised form 8 November 2011 Accepted 12 November 2011 Keywords: Tropical ecosystems Food web Stable isotope Heavy metal Bioaccumulation Guiana dolphin

a b s t r a c t The present study investigated trophic relationships and mercury flow through food webs of three tropical coastal ecosystems: Guanabara, Sepetiba and Ilha Grande bays. The investigation was carried out through carbon and nitrogen stable isotopes (␦13 C, ␦15 N) and total mercury (THg) determination in muscle from 35 species, including crustacean, cephalopod, fish and dolphin species. Detritivorous species showed the lowest average ␦15 N values in all bays. These species were 13 C enriched in Sepetiba and Ilha Grande bays, suggesting the presence of 13 C enriched macroalgae in their diet. The highest mean ␦15 N values were 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 food webs from Sepetiba, Guanabara and Ilha Grande bays. Guanabara Bay showed to be depleted in ␦15 N compared 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 THg concentrations and ␦15 N values for Guanabara and Ilha Grande bays, but not for Sepetiba Bay. Our findings showed trophic magnification factors (TMF) above 1, demonstrating that THg is being biomagnified up the food chains in Rio de Janeiro bays. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction In ecosystems, organisms interact through complex trophic relationships, which involve energy and nutrient flow between trophic levels. Understanding trophic relationships, as well as quantitatively assessing trophic levels is of fundamental importance for the comprehension of ecosystem structure (Lindeman, 1942). In this context, carbon and nitrogen stable isotope measurements have been successfully used for determinating the potential sources of primary productivity, as well as for assessing trophic levels in food webs, respectively (Das et al., 2003a; Fry and Sherr, 1984; Michener and Kaufman, 2007). Therefore, these measurements provide important information about trophic structure and energy flow 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 Biofísica, Laboratório de Radioisótopos, 21941-900, Rio de Janeiro, RJ, Brazil.

Tel.: +55 21 25615339; fax: +55 21 22808193.

E-mail addresses: tbisi@yahoo.com.br, tatibisi@gmail.com (T.L. Bisi).

1470-160X/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecolind.2011.11.015

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

Some micropollutants, like mercury (Hg), undergo increase in concentrations upward trophic levels, reaching high concentrations in top-chain organisms (Renzoni et al., 1998). The high potential 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; Wagemann et al., 1998). With regard to the absorption of mercurial species through the gastrointestinal tract, MeHg is the most efficiently taken up form of Hg (Wagemann et al., 1998). Therefore, studying trophic relationships among organisms is also important for a better understating of contaminant bioaccumulation and biomagnification processes. In this context, several studies have used nitrogen stable isotopes as indicators of trophic level for investigating 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).

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Although there are a number of food web studies dealing with stable isotope ratios and micropollutant flow, these investigations usually focus on northern hemisphere areas, mainly in temperate and polar regions (e.g., Das et al., 2003a; Dehn et al., 2006; Hobson et al., 2002). In tropical areas, only a few studies have dealt with trophic relationships in estuarine and marine food webs using stable isotope measurements (Abreu et al., 2006; Corbisier et al., 2006; Lin et al., 2007). Tropical regions are characterized by high species richness (Begon et al., 2006), which probably promotes more complex trophic relationships due to greater diversity of food items for each species (Paine, 1966).

The present study focuses on three different tropical coastal food webs located in a region under high anthropogenic pressure, the Rio de Janeiro State. Nevertheless, these environments present different degradation levels. Guanabara Bay is the most degraded area among the studied bays. The estuary is considered to be the most degraded system of Brazilian coast (FEEMA, 1990; Kjerfve et al., 1997). Sepetiba Bay presents an intermediate degree of contamination, but it has undergone a significant increase in pollution over the 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 degradation scenario. Among the systems considered in the present study, Ilha Grande Bay is the most preserved one. The estuary is considered 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 three tropical coastal ecosystems: Guanabara, Sepetiba and Ilha Grande bays, (2) to compare the trophic structure from the three food webs investigated, (3) to calculate the trophic magnification factors (TMF) of total mercury (THg) between the Guiana dolphin and its prey, and (4) to assess the influence of several factors, such as the trophic position of the Guiana dolphin, on Hg accumulation.

of each bay. This sampling was carried out in July 2008 (winter) and January 2009 (summer).

2.2. Stable isotope measurements Stable isotopes measurements of carbon and nitrogen were carried out in muscle samples from Guiana dolphins, fishes and invertebrates. After being dried at 60 ◦ C (72 h), samples were ground into a homogeneous powder. Since all muscle samples from the present study presented low lipid content (C:N < 4.0), no lipid extractions were carried out (Post et al., 2007). Stable isotope measurements were performed on 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) were also 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 the V-PDB (Vienna Peedee Belemnite) standard and to atmospheric nitrogen, respectively.

2.3. Total mercury (THg) determination Aliquots of approximately 0.4 g of muscle (wet weight) were digested with 1 mL of hydrogen peroxide and 5 mL of sulfuric:nitric acid mixture (1:1). The solution was then heated to 60 ◦ C for 2 h in a water bath, which was followed by the addition of 5 mL of potassium permanganate 5% solution and heating to 60 ◦ C for more 15 min. After overnight digestion, THg concentration was determined by Cold Vapor/AAS (FIMS-400, Perkin-Elmer) with sodium borohydride as reducing agent. Blanks were carried through the procedure in the same way as the sample. The standard reference material DORM-3 (National Research Council, Canada) was analyzed in every run and our results were in good agreement with certified values (mean recovery ± SD = 101.44 ± 3.57%).

2.4. Statistical analysis

2. Material and methods 2.1. Sampling Muscle samples were obtained from Guiana dolphins, Sotalia guianensis, that were either incidentally captured in gillnet fishery or stranded on the beaches of the three bays of Rio de Janeiro State between 1995 and 2009: the Guanabara Bay (n = 20), the Sepetiba Bay (n = 44) and the Ilha Grande Bay (n = 10). All samples were stored at −20 ◦ C until analysis.

The species preyed by S. guianensis were previously identified from stomach content analysis. They include fish, cephalopod and crustacean species (Azevedo et al., 2008; Azevedo, unpublished data). Sampling was performed in winter 2008 (August to October – dry season) and summer 2009 (February and March – wet season).

Samples from 34 prey species (five invertebrate and 29 fish species from distinct feeding habitats) were acquired in fishing landings inside 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 specimens were sorted out in two groups regarding their length. M. furnieri fitting the size on which Guiana dolphins exert predation were categorized in group “d”, as well as individuals larger than 40 cm were placed in group “40”. The specimens were weighed, measured and dissected. All samples were frozen and stored at −20 ◦ C until analysis.

Seston samples were collected using 75-nm-mesh plankton net in the inner part, at low tide, as well as in the entrance, at high tide,

Mean carbon and nitrogen isotopic values were calculated for Guiana dolphins and for each prey species. The fish species were classified into five feeding types (see Tables 1 and 2). The Kolmogorov–Smirnov test was used in order to test for normality of the data. ANOVA and post hoc Tukey tests were used for comparing nitrogen and carbon isotopic values among feeding types (including cephalopod and crustacean species) and among the three bays. The nonparametric Kruskal–Wallis and post hoc multiple comparison tests were applied when the data distribution did not follow the rules of normal distribution. The nonparametric Mann–Whitney U test was performed for comparison between seasons (winter × summer sampling). Simple linear regression analysis was used for investigating relationships between ␦15 N and logarithmic concentrations of THg, as well as for determinating trophic magnification factors (TMF). TMF is calculated as the antilog of the regression slope with base 10 and can be used for quantifying food web biomagnification (Borgå et al., 2011; Fisk et al., 2001).

Therefore, this tool was used for calculating Hg biomagnification in different ecosystems.

3. Results and discussion 3.1. Trophic relationships Summaries of ␦13 C and ␦15 N values for cephalopods, crustaceans, fishes and Guiana dolphins are given in Tables 1 and 2, respectively, as well in Fig. 1.

Carbon isotope ratios have proved to be useful in identifying the relative input of dietary resources from different food webs, as ␦13 C

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293

Table 1 Mean ␦13 C values (‰) ± SD and number of individuals (n) of seston, cephalopods, crustaceans, fishes and Guiana dolphin from Guanabara, Sepetiba and Ilha Grande bays, Rio de Janeiro State.

Species

Guanabara Bay

Seston Inner Entrance Cephalopods Loliginidae Loligo plei

Sepetiba Bay Summer

Winter

Summer

Winter

Summer

−19.4 −18.5

−19.0 n.d.

−19.0 −16.6

−14.6 −18.2

−22.5 −20.6

−19.4 −18.5

−18.9 ± 0.5 (n = 6)

−16.1 ± 0.1 (n = 3) −18.2 ± 0.3 (n = 7)

Loligo sanpaulensis −17.1 ± 1.1 (n = 10)

Lolliguncula brevis Crustaceans Penaeidae Farfantepenaeus brasiliensis

−15.6 ± 0.6 (n = 6)

Litopenaeus schmitt

−15.2 ± 0.2 (n = 3)

Fishes Ariidae Aspistor luniscutisa Batrachoididae Porichthys porosissimusb Carangidae Chloroscombrus chrysurusc Centropomidae Centropomus spp.b Clupeidae Sardinella brasiliensisd

d

Cetengraulis edentulus

−15.4 ± 1.4 (n = 6)

−13.2 ± 0.2 (n = 6)

−18.8 ± 0.8 (n = 5)

−15.1 ± 0.5 (n = 5)

−14.7 ± 0.6 (n = 6)

−14.9 ± 0.4 (n = 6)

−20.9 ± 1.3 (n = 6)

−14.3 ± 0.1 (n = 3)

−15.6 ± 0.4 (n = 6)

−19.6 ± 0.6 (n = 6)

−15.1 ± 0.3 (n = 6) −14.8 ± 0.6 (n = 6)

Mugilidae Mugil curemae −14.4 ± 0.9 (n = 5)

Mugil Lizae

−18.5 ± 0.4 (n = 6)

−13.1 ± 0.4 (n = 6)

−17.6 ± 0.2 (n = 6)

−16.6 ± 0.5 (n = 6)

−14.3 ± 1.1 (n = 6)

−14.7 ± 1.6 (n = 6)

−15.8 ± 0.7 (n = 6)

−16.8 ± 0.2 (n = 3)

−16.3 ± 0.6 (n = 6)

−15.2 ± 0.6 (n = 6)

−15.7 ± 0.1 (n = 5)

−18.3 ± 1.0 (n = 6)

−15.2 ± 0.3 (n = 6)

−14.2 ± 0.6 (n = 3)

−14.9 ± 0.2 (n = 6) −15.7 ± 0.6 (n = 4)

−14.1 ± 0.4 (n = 6) −14.4 ± 0.5 (n = 6) −14.9 ± 0.2 (n = 6)

−14.2 ± 0.9 (n = 6)

−13.8 ± 0.5 (n = 6)

−9.4 ± 1.4 (n = 4) −13.9 ± 1.0 (n = 6)

−11.1 ± 0.9 (n = 5)

−17.8 ± 0.7 (n = 5)

Mugil spp.e

Cynoscion jamaicensisb Cynoscion leiarchusb

−17.2 (n = 1) −18.9 ± 0.3 (n = 6) −16.3 ± 0.1 (n = 5)

−17.0 ± 0.8 (n = 6) −15.8 ± 0.9 (n = 6) −13.9 ± 0.4 (n = 6)

Isopisthus parviponnisb b

Larimus breviceps

−17.7 ± 0.7 (n = 6)

Menticirrhus americanusa Micropogonias furnieri “d”a

−10.6 ± 1.1 (n = 6)

−18.03 ± 0.5 (n = 4)

Sciaenidae Ctenosciaena gracilicirrhusa Cynoscion guatucupa

−16.7 ± 0.5 (n = 6)

−10.9 ± 1.4 (n = 5)

Paralichthydae Paralichthys patagonicusa

b

−17.6 ± 0.7 (n = 6)

−18.9 ± 0.0 (n = 3)

Engraulis anchoitad Haemulidae Orthopristis rubera

−15.9 ± 0.5 (n = 5) −14.5 ± 1.1 (n = 4)

−15.1 ± 0.9 (n = 5) −14.0 ± 0.8 (n = 5)

−17.6 ± 0.5 (n = 3)

−15.9 ± 0.3 (n = 6) −14.1 ± 0.5 (n = 6)

−18.6 ± 0.3 (n = 6)

−15.3 ± 0.7 (n = 5) −14.3 ± 0.2 (n = 5)

−18.9 ± 0.5 (n = 5)

Cynoglossidae Symphurus tesselatusa Engraulididae Anchoa spp.d

Ilha Grande Bay

Winter

−16.3 ± 0.8 (n = 14)

−16.2 ± 1.0 (n = 13)

−19.2 ± 0.3 (n = 4) −17.1 ± 0.4 (n = 6)

−12.6 ± 1.1 (n = 5) −15.3 ± 0.6 (n = 6) −15.34 ± 0.7 (n = 6) −12.8 ± 0.4 (n = 4) −13.8 ± 1.7 (n = 13)

−14.5 ± 0.3 (n = 6) −16.3 (n = 1) −15.6 ± 1.1 (n = 6) −14.0 ± 0.6 (n = 6) −14.2 ± 0.4 (n = 6)

−14.4 ± 0.6 (n = 6) −13.4 ± 1.4 (n = 13)

−17.9 ± 0.1 (n = 6)

−17.7 ± 0.3 (n = 6) −16.2 ± 0.7 (n = 6)

−16.7 ± 0.8 (n = 5) −18.0 ± 0.7 (n = 6)

−16.5 ± 0.6 (n = 6)

−16.5 ± 1.2 (n = 14)

−16.2 ± 0.7 (n = 13)

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Table 1 (Continued) Species

Guanabara Bay

Micropogonias furnieri “40”b Paralonchurus brasiliensisa

Sepetiba Bay

Winter

Summer

Winter

Summer

Winter

Summer

−16.1 ± 1.4 (n = 7) −17.8 ± 0.7 (n = 6)

−15.4 ± 1.6 (n = 7) −16.7 ± 0.4 (n = 6)

−14.7 ± 1.4 (n = 7) −15.5 ± 0.7 (n = 5) −15.1 ± 0.1 (n = 3) −14.4 ± 0.1 (n = 3)

−14.3 ± 2.0 (n = 6) −14.0 ± 0.3 (n = 6) −14.4 ± 0.2 (n = 5) −13.9 (n = 1)

−16.6 ± 0.4 (n = 10) −17.0 ± 0.8 (n = 6) −17.1 ± 0.5 (n = 3) −18.5 ± 0.2 (n = 2) −17.7 ± 0.2 (n = 6)

−16.3 ± 0.9 (n = 8) −16.3 ± 0.3 (n = 6) −16.3 ± 0.3 (n = 2) −15.6 ± 0.0 (n = 2)

−14.5 ± 0.4 (n = 2) −15.1 ± 0.4 (n = 6)

Stellifer rastriferb Stellifer stelliferb −17.6 ± 0.1 (n = 6)

Umbrina canosaia Serranidae Diplectrum radialea a

Serranus auriga Sparidae Pagrus pagrusc

−15.9 ± 0.2 (n = 6)

−15.0 ± 0.5 (n = 6)

−14.2 ± 0.2 (n = 6) −15.1 (n = 1)

−18.5 ± 0.4 (n = 6)

−18.7 ± 0.3 (n = 6)

−18.9 ± 0.7 (n = 6)

−16.9 ± 0.2 (n = 6)

−18.2 ± 0.2 (n = 6)

−17.3 ± 0.2 (n = 6)

−17.2 ± 0.8 (n = 5)

−13.8 ± 0.5 (n = 6)

−17.8 ± 0.1 (n = 5)

−17.4 ± 0.7 (n = 5)

Trichiuridae Trichiurus lepturusc Cetacea Sotalia guianensis

Ilha Grande Bay

−14.0 ± 0.7 (n = 20)

−14.5 ± 1.0 (n = 44)

−16.6 ± 0.4 (n = 10)

n.d. – not determined. 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 cephalopod species were found to be depleted in 13 C in Sepetiba and Guanabara bays (Fig. 1) (from −18.9‰ to −17.1‰ in winter and from −16.9‰ to −16.3‰ in summer, for Sepetiba Bay; as well as and from −20.8‰ to −17.2‰ in winter and from −19.6‰ to −16.7‰ in summer, for Guanabara Bay). Some of these species (e.g., Paralonchurus brasiliensis, Cynoscion guatucupa, Umbrina canosai and Porichthys porosissimus) are marine organisms that use estuaries opportunistically or optionally during larval, juvenile, sub-adult and even adult stage (Sinque and Muelbert, 1997). Therefore, our findings may be indicating that, for some species, the primary carbon source is from a neritic food web outside the bays. These findings suggest complex processes and pointed to the need for detailed investigation for a better understanding of the multiple sources of carbon in the food webs of Sepetiba and Guanabara bays.

Mean ␦13 C and ␦15 N values varied significantly among prey 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 to winter, F6,66 = 16.5 and F6,66 = 3.7 to summer, respectively, p < 0.003) and Ilha Grande Bay food webs (Kruskal–Wallis test, H = 41.55 and H = 26.88 in winter, H = 40.07 and H = 42.34 in summer, p < 0.0001).

The detritivorous fish Mugil spp. was highly 13 C-enriched in Sepetiba (Tukey HSD test, p < 0.001) and Ilha Grande bays (multiple comparison test, p < 0.01) (Fig. 1). These findings suggest food web inputs of microalgae and/or macroalgae, that are typically higher in 13 C than marine phytoplankton (Boutton, 1991; Fry and Sherr, 1984).

Regarding nitrogen stable isotopes, detritivorous and invertebrate species displayed the lowest mean ␦15 N values. Intermediate mean ␦15 N values were observed in planktivorous and in feeder of benthic invertebrate fishes. Fish and benthic invertebrate feeders as well as those species of demerso-pelagic feeding habitat showed

the highest ␦15 N values (p < 0.01). Cephalopod displayed intermediate mean ␦15 N results in Sepetiba and Guanabara Bays, but higher ␦15 N values in Ilha Grande Bay (p < 0.01) (Table 3). These findings followed the usual food-web nitrogen pattern, in which ␦15 N values typically show a trophic enrichment between prey and consumer tissue (Minagawa and Wada, 1984). Consequently, higher trophic position organisms showed the highest ␦15 N values, as observed to those species that feed on fishes (fish and benthic invertebrate feeders and species of demerso-pelagic feeding habitat).

Chloroscombrus chrysurus and Trichiurus lepturus are the two demerso-pelagic species sampled in this study. Stomach content analysis has showed that C. chrysurus prey on broad taxonomic groups, presenting variable feeding habits among populations (Vasconcelos-Filho et al., 1984; Carvalho and Soares, 1997; Hofling et al., 1997). The high average ␦15 N results suggest fish as an important prey to C. chrysurus in the Rio de Janeiro bays. Regarding T. lepturus, its diet is composed of pelagic and demersal prey species, especially fish, associated with estuarine and coastal areas (Bittar et al., 2008; Martins et al., 2005). In summer sampling, the highest ␦15 N was verified in T. lepturus (16.61‰), suggesting the species as the top predator in Sepetiba Bay. It was expected that Guiana dolphins presented the highest trophic level, but the average ␦15 N value for these mammals was lower than those found in several prey species from Sepetiba (14.0‰) and Ilha Grande bays (14.2‰). On the other hand, in Guanabara Bay, Guiana dolphin was on the top of the food web, showing the highest mean ␦15 N value of that food web. Along the species distribution, stomach analyses have showed different fish species as preferential prey in distinct Guiana dolphin populations (e.g., Azevedo et al., 2008; Di Beneditto and Ramos, 2004; Gurjão et al., 2003). In fact, our findings suggest that Guiana dolphin feeds on organisms that occupy distinct trophic levels among the three bays studied here. In Sepetiba and Ilha Grande bays, Guiana dolphin probably feeds on organisms that occupy relatively lower trophic levels than in Guanabara Bay.

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Table 2 Mean ␦15 N 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.

Species

Guanabara Bay

Seston Inner Entrance Cephalopods Loliginidae Loligo plei

Sepetiba Bay Summer

Winter

Summer

Winter

Summer

n.d. n.d.

n.d. n.d.

n.d.

7.6

8.9 8.3

n.d. n.d.

7.1 n.d.

12.4 ± 0.8 (n = 6)

15.5 ± 0.1 (n = 3) 13.9 ± 0.6 (n = 7)

Loligo sanpaulensis 11.9 ± 1.2 (n = 10)

Lolliguncula brevis Crustaceans Penaeidae Farfantepenaeus brasiliensis

8.7 ± 2.3 (n = 6)

Litopenaeus schmitt

10.8 ± 1.2 (n = 3)

Fishes Ariidae Aspistor luniscutisa Batrachoididae Porichthys porosissimusb Carangidae Chloroscombrus chrysurusc Centropomidae Centropomus spp.b Clupeidae Sardinella brasiliensisd

d

Cetengraulis edentulus

13.9 ± 1.2 (n = 6)

14.5 ± 0.7 (n = 6)

12.8 ± 0.3 (n = 5)

13.3 ± 2.2 (n = 5)

14.1 ± 0.3 (n = 6)

15.9 ± 0.3 (n = 6)

13.6 ± 0.9 (n = 6)

13.2 ± 0.8 (n = 3)

10.5 ± 0.2 (n = 6)

10.5 ± 0.3 (n = 6)

13.4 ± 0.5 (n = 6) 11.1 ± 2.2 (n = 6)

Mugilidae Mugil curemae 10.40 ± 1.45 (n = 5)

Mugil Lizae

12.6 ± 0.1 (n = 6)

15.6 ± 0.3 (n = 6)

14.1 ± 0.3 (n = 6)

14.6 ± 0.3 (n = 6)

15.3 ± 0.9 (n = 6)

15.1 ± 0.9 (n = 6)

13.7 ± 0.8 (n = 6)

14.9 ± 0.3 (n = 3)

13.0 ± 0.3 (n = 6)

13.3 ± 0.2 (n = 6)

13.2 ± 0.5 (n = 5)

11.6 ± 0.4 (n = 6)

14.2 ± 0.7 (n = 6)

14.3 ± 1.2 (n = 3)

14.6 ± 0.3 (n = 6) 13.8 ± 0.1 (n = 4)

14.9 ± 0.53 (n = 6) 14.3 ± 0.4 (n = 6) 15.1 ± 0.1 (n = 6)

15.1 ± 0.2 (n = 6)

14.6 ± 1.3 (n = 6)

9.2 ± 0.3 (n = 4) 9.6 ± 0.8 (n = 6)

10.0 ± 0.8 (n = 5)

9.3 ± 2.1 (n = 5)

Mugil spp.e

Cynoscion jamaicensisb Cynoscion leiarchusb

15.7 (n = 1) 14.2 ± 0.1 (n = 6) 9.6 ± 0.4 (n = 5)

13.9 ± 0.2 (n = 6) 13.9 ± 0.3 (n = 6) 12.7 ± 1.1 (n = 6)

Isopisthus parviponnisb b

Larimus breviceps

14.8 ± 0.5 (n = 6)

Menticirrhus americanusa Micropogonias furnieri “d”a

8.8 ± 1.3 (n = 6)

13.2 ± 0.5 (n = 4)

Sciaenidae Ctenosciaena gracilicirrhusa Cynoscion guatucupa

12.1 ± 0.4 (n = 6)

9.4 ± 0.7 (n = 5)

Paralichthydae Paralichthys patagonicusa

b

14.5 ± 0.7 (n = 6)

12.5 ± 0.2 (n = 3)

Engraulis anchoitad Haemulidae Orthopristis rubera

14.2 ± 0.4 (n = 5) 15.2 ± 0.8 (n = 4)

11.8 ± 0.9 (n = 5) 11.3 ± 0.6 (n = 5)

12.7 ± 0.0 (n = 3)

12.3 ± 0.7 (n = 6) 11.0 ± 0.8 (n = 6)

14.0 ± 0.4 (n = 6)

12.2 ± 0.4 (n = 5) 11.6 ± 0.9 (n = 5)

12.1 ± 0.2 (n = 5)

Cynoglossidae Symphurus tesselatusa Engraulididae Anchoa spp.d

Ilha Grande Bay

Winter

10.3 ± 1.6 (n = 14)

11.3 ± 1.9 (n = 13)

15.7 ± 0.2 (n = 4) 14.3 ± 0.2 (n = 6)

15.9 ± 0.2 (n = 5) 15.8 ± 0.3 (n = 6) 15.8 ± 0.5 (n = 6) 13.1 ± 1.5 (n = 4) 13.2 ± 1.1 (n = 13)

14.9 ± 0.4 (n = 6) 13.9 (n = 1) 14.3 ± 0.8 (n = 6) 15.1 ± 0.5 (n = 6) 16.06 ± 0.43 (n = 6)

14.9 ± 0.9 (n = 6) 13.4 ± 1.1 (n = 13)

14.2 ± 0.2 (n = 6)

13.9 ± 0.2 (n = 6) 14.8 ± 0.5 (n = 6)

13.4 ± 0.2 (n = 5) 14.3 ± 0.3 (n = 6)

14.5 ± 0.9 (n = 6)

14.1 ± 0.8 (n = 14)

13.8 ± 0.9 (n = 13)

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Table 2 (Continued) Species

Guanabara Bay

Micropogonias furnieri “40”b Paralonchurus brasiliensisa

Sepetiba Bay

Winter

Summer

Winter

Summer

Winter

Summer

13.9 ± 0.8 (n = 7) 14.5 ± 0.6 (n = 6)

12.4 ± 2.09 (n = 7) 14.2 ± 0.6 (n = 6)

15.0 ± 0.73 (n = 7) 14.8 ± 0.3 (n = 5) 15.4 ± 0.3 (n = 3) 16.3 ± 0.0 (n = 3)

14.6 ± 0.86 (n = 6) 14.9 ± 0.3 (n = 6) 15.9 ± 0.4 (n = 5) 15.817 (n = 1)

14.7 ± 0.5 (n = 10) 13.6 ± 0.6 (n = 6) 14.3 ± 0.5 (n = 3) 13.63 ± 0.08 (n = 2) 13.7 ± 0.3 (n = 6)

14.6 ± 0.5 (n = 8) 13.6 ± 0.7 (n = 6) 14.1 ± 0.1 (n = 2) 14.2 ± 0.0 (n = 2)

14.3 ± 0.2 (n = 2) 13.2 ± 0.3 (n = 6)

Stellifer rastriferb Stellifer stelliferb 13.9 ± 0.4 (n = 6)

Umbrina canosaia Serranidae Diplectrum radialea a

Serranus auriga Sparidae Pagrus pagrusc

11.4 ± 1.3 (n = 6)

13.5 ± 0.3 (n = 6)

14.9 ± 0.3 (n = 6) 14.3 (n = 1)

12.9 ± 0.2 (n = 6)

12.1 ± 0.8 (n = 6)

13.1 ± 0.6 (n = 6)

14.1 ± 0.2 (n = 6)

13.6 ± 0.2 (n = 6)

14.2 ± 0.2 (n = 6)

14.9 ± 0.8 (n = 5)

16.6 ± 0.4 (n = 6)

14.6 ± 0.4 (n = 5)

14.2 ± 0.3 (n = 5)

Trichiuridae Trichiurus lepturusc Cetacea Sotalia guianensis

Ilha Grande Bay

14.2 ± 0.9 (n = 20)

14.0 ± 0.6 (n = 44)

14.2 ± 0.6 (n = 10)

n.d. – not determined. 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 different trophic relationships in the food webs of Sepetiba, Guanabara and Ilha Grande bays. The three studied bays are under anthropogenic pressure, but in different degradation levels. As mentioned, Guanabara Bay is the most degraded estuary among the three studied bays. In fact, it is considered to be one of the most degraded systems of Brazilian coast (FEEMA, 1990; Kjerfve et al., 1997). The Guanabara Bay food web showed less complex trophic relationships than did Sepetiba and Ilha Grande bays. In Sepetiba and Ilha Grande bays the trophic relationships among the fish species were not well defined and the systems seem to be complex, as it is expected for tropical food webs. The high biodiversity found in these systems probably promotes great variety of prey for each predator (Paine, 1966). Concerning fish and benthic invertebrate feeders and demerso-pelagic species from Sepetiba and Ilha Grande bays, it was not possible to determine specific groups of prey through nitrogen isotopic values. This finding suggests that these species are preying on several different taxa.

Ilha Grande Bay showed significant depleted ␦13 C values for all feeding types (except for detritivorous species), as well as for Guiana dolphins, compared to Guanabara and Sepetiba bays both in winter and summer season (Tukey HSD test, p < 0.05) (Tables 1 and 4). Ilha Grande Bay is not a confined estuary like the other two bays. In addition to this feature, this body of water receive colder and more saline water by marine current flow from continental shelf than the other bays considered herewith (Signorini, 1980a,b). Therefore, the carbon isotopic values probably reflect higher marine influence in Ilha Grande Bay than in Guanabara and Sepetiba bays.

Planktivorous and benthic invertebrate feeder fishes from Sepetiba and Ilha Grande bays showed higher ␦15 N values than those feeding type groups from Guanabara Bay in the winter season (Kruskal–Wallis test, H = 26.68 and H = 47.24, respectively, p < 0.0001). These values ranged from 11.5‰ to 15.8‰ for Sepetiba Bay and from 12.5‰ to 15.6‰ for Ilha Grande Bay. In Guanabara Bay, the nitrogen isotopic values ranged from 7.4‰ to 13.3‰ for these two feeding types. Additionally, Sepetiba Bay showed the highest ␦15 N for fish and benthic invertebrate feeders (from 13.7‰ to

Table 3 Mean ␦15 N 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

Invertebrates Detritivorous Planktivorous Benthic invertebrate feeder Fish and benthic invertebrate feeder Demerso-pelagic predator Cephalopods

Sepetiba Bay

Ilha Grande Bay

Winter

Summer

Winter

Summer

Winter

Summer

8.7 9.3 11.3 10.7 12.1 13.3 11.9

10.7 10.4 12.3 12.3 13.0 14.1 12.4

11.9 9.4 13.8 14.2 15.6 15.9 14.4

11.4 10.3 14.7 14.2 15.3 16.1 14.6

– 9.4 13.2 13.8 14.2 14.1 14.0

– 8.8 11.6 13.3 14.5 14.3 14.5

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297

Table 4 Mean ␦13 C 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

Invertebrates Detritivorous Planktivorous Benthic invertebrate feeder Fish and benthic invertebrate feeder Demerso-pelagic predator Cephalopods

Sepetiba Bay

Ilha Grande Bay

Winter

Summer

Winter

Summer

Winter

Summer

−15.6 −17.8 −15.2 −16.2 −16.1 −15.1 −17.1

−15.2 −14.4 −14.9 −15.8 −14.9 −14.7 −18.9

−14.8 −12.1 −15.6 −14.5 −14.6 −14.9 −17.6

−14.6 −11.1 −14.7 −14.0 −14.3 −13.3 −15.3

– −10.9 −15.7 −17.0 −17.1 −17.9 −18.6

– −10.6 −18.2 −16.3 −16.5 −17.1 −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 invertebrate feeder, fish and benthic invertebrate feeders, demerso-pelagic, Guiana dolphin.

(For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

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Table 5 Mean muscular total mercury (THg) concentration (ng/g) ± SD and number of individuals (n) cephalopods, crustaceans, fishes and Guiana dolphins from Guanabara, Sepetiba and Ilha Grande bays, Rio de Janeiro State.a Species

Guanabara Bay Winter

Sepetiba Bay Summer

Winter

Ilha Grande Bay Summer

Cephalopoda Loliginidae Loligo plei

Winter

21.18 ± 7.3 (n = 6) 12.3 ± 4.1 (n = 6)

Loligo sanpaulensis Lolliguncula brevis Crustacea Penaeidae Litopenaeus schmitti

36.3 ± 21.1 (n = 9)

12.9 ± 7.0 (n = 4)

3.6 ± 1.8 (n = 6)

Fishes Ariidae Aspistor luniscutis

4.2 ± 2.1 (n = 6)

6.5 ± 1.5 (n = 5)

24.2 ± 26.1 (n = 6)

8.5 ± 2.7 (n = 6)

Batrachoididae Porichthys porosissimus Carangidae Chloroscombrus chrysurus

20.2 ± 7.1 (n = 5)

Centropomidae Centropomus spp.

Clupeidae Sardinella brasiliensis

Cetengraulis edentulus

19.0 ± 9.3 (n = 6)

99.5 ± 61.7 (n = 6)

51.8 ± 16.4 (n = 6)

65.7 ± 22.1 (n = 3)

33.5 ± 23.1 (n = 6)

44.7 ± 9.9 (n = 6)

80.7 ± 38.7 (n = 6)

169.0 ± 21.4 (n = 3)

5.0 ± 2.0 (n = 6)

5.8 ± 0.8 (n = 6)

4.6 ± 1.1 (n = 6)

20.5 ± 6.6 (n = 6)

4.4 ± 2.2 (n = 6)

8.3 ± 2.9 (n = 3)

29.8 ± 7.1 (n = 6) 7.8 ± 4.5 (n = 4)

32.6 ± 12.2 (n = 6) 8.0 ± 0.8 (n = 6) 59.6 ± 7.1 (n = 6)

15.8 ± 10.6 (n = 6)

15.4 ± 6.9 (n = 6)

43.4 ± 8.0 (n = 6) 27.9 ± 9.6 (n = 6)

Engraulis anchoita Haemulidae Orthopristis ruber Mugilidae Mugil liza Mugil spp.

6.7 ± 1.3 (n = 5) 18.2 ± 1.6 (n = 4)

Sciaenidae Ctenosciaena gracilicirrhus

12.7 ± 7.0 (n = 4)

18.2 ± 2.7 (n = 6) 41.7 ± 9.5 (n = 6)

Cynoscion guatucupa Cynoscion jamaicensis 66.9 ± 9.8 (n = 4)

54.9 ± 39.4 (n = 6) 44.3 ± 8.7 (n = 6)

Isopisthus parvipinnis Larimus breviceps Menticirrhus americanus Micropogonias furnieri “d” Micropogonias furnieri “40” Paralonchurus brasiliensis Stellifer rastrifer Stellifer stellifer

7.6 ± 1.4 (n = 5)

12.1 ± 3.6 (n = 5)

Paralichthydae Paralichthys patagonicus

Cynoscion leiarchus

28.3 ± 7.8 (n = 5)

31.2 ± 16.1 (n = 6)

27.8 ± 6.3 (n = 6)

93.1 ± 50.4 (n = 6) 15.4 ± 8.1 (n = 6)

62.9 ± 29.8 (n = 3) 44.77 ± 16.4 (n = 4)

Cynoglossidae Symphurus tesselatus Engraulididae Anchoa spp.

Summer

83.4 ± 107.9 (n = 14) 252.7 ± 214.5 (n = 7)

23.8 ± 23.4 (n = 13) 111.2 ± 46.4 (n = 7)

27.5 ± 5.0 (n = 5) 12.5 ± 6.8 (n = 6) 16.8 ± 8.04 (n = 6) 10.5 ± 7.5 (n = 4) 7.1 ± 6.5 (n = 12) 107.6 ± 134.0 (n = 7) 10.46 ± 6.0 (n = 5) 6.1 ± 1.3 (n = 3) 14.5 ± 3.7 (n = 3)

19.6 ± 5.0 (n = 6) 27.8 ± 7.4 (n = 6)

47.0 ± 30.2 (n = 6) 24.4 ± 14.1 (n = 6) 44.9 ± 10.8 (n = 6)

49.3 ± 18.7 (n = 5) 70.4 ± 34.3 (n = 6)

44.0 ± 37.4 (n = 6)

19.93 ± 8.40 (n = 6) 7.46 ± 5.9 (n = 12) 135.5 ± 99.5 (n = 5) 5.8 ± 1.5 (n = 6) 19.4 ± 10.2 (n = 5) 24.4 (n = 1)

33.1 ± 33.4 (n = 11) 264.0 ± 96.8 (n = 10) 16.9 ± 5.0 (n = 6) 26.4 ± 15.6 (n = 2) 24.0 ± 10.9 (n = 3)

49.7 ± 43.2 (n = 13) 226.1 ± 126 (n = 7) 13.8 ± 2.9 (n = 6) 38.8 ± 4.1 (n = 2) 53.5 ± 16.7 (n = 2)

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299

Table 5 (Continued) Species

Guanabara Bay Winter

Sepetiba Bay Summer

Winter

Ilha Grande Bay Summer

Serranidae Diplectrum radiale Serranus auriga

Winter

Summer

126.5 ± 31.1 (n = 6)

Umbrina canosai

66.5 ± 23.9 (n = 6)

90.3 ± 21.3 (n = 6)

15.8 ± 7.3 (n = 6) 9.5 (n = 1)

20.4 ± 0.2 (n = 2) 12.5 ± 1.2 (n = 6)

Sparidae Pagrus pagrus Trichiuridae Trichiurus lepturus Cetacea Sotalia guianensis

36.3 ± 9.5 (n = 6) 920.3 ± 656.2 (n = 12)

269.2 ± 332.3 (n = 42)

39.2 ± 12.1 (n = 6)

34.8 ± 5.9 (n = 6)

37.1 ± 12.8 (n = 5)

22.5 ± 17.1 (n = 5) 688.4 ± 221.8 (n = 9)

Blank – not analyzed. a Total mercury determination was not carried out in species that were depleted in 13 C.

16.7‰ in winter and from 13.7‰ to 16.8‰ in summer) and for those species of demerso-pelagic feeding habit (from 15.5‰ to 16.5‰ in winter and from 15.2‰ to 17.1‰ in summer) (multiple comparison test, p < 0.0012). Since ␦15 N values can vary from system to system even when the same species is considered (Cabana and Rasmussen, 1996), caution should be taken when comparing ␦15 N values between food webs.

Several studies have reported more ␦15 N-enriched values in organisms from areas undergoing eutrophication process due to city 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 system among the three sampled areas, showed depleted ␦15 N values compared to both Sepetiba and Ilha Grande bays. Phytoplankton in Guanabara Bay is dominated by nanoplanktonic and cyanobacteria species (Valentin et al., 1999). Therefore, our findings may be reflecting a substantial input of atmospheric nitrogen fixation by cyanobacteria, which results in low ␦15 N values (Carpenter et al., 1997; McClelland et al., 2003). In contrast, Kalas et al. (2009) found enriched ␦15 N values in particulate organic matter from Guanabara Bay. The authors suggested it could be due to the incorporation of isotopically heavy residual NH4 + by the phytoplankton. However, the sampling was performed in 1999 and 2000. The distinct results obtained through this 10-year interval between the investigation carried out by Kalas et al. (2009) and the present study may suggest worsening in the Guanabara Bay degradation process over the time. The presence of cyanobacteria is usually associated to the eutrophication process. The fact that organism from Guanabara Bay food web present relatively low nitrogen isotopic values probably reflects elevated cyanobacteria density in this estuary. These findings point out an accelerated eutrophication process that indicates a much higher degradation condition in Guanabara Bay than it could be assumed previously.

3.3. THg–ı15 N relationships Average muscular total mercury concentration (THg) was lowest in Litopenaeus schmitt (3.6 ng/g in Guanabara Baywinter and 4.2 ng/g in Sepetiba Baywinter ) and in Sardinella brasiliensis (4.6 ng/g in Ilha Grande Baywinter ) and highest in Guiana dolphin (920.3 ng/g in Guanabara Bay, 269.2 ng/g in Sepetiba Bay and 688.4 ng/g in Ilha Grande Bay) (Table 5). THg concentrations in prey species increased successively with increasing trophic level in Guanabara, Sepetiba and Ilha Grande bays, except for those species of

demerso-pelagic feeding habitat. Detritivorous and invertebrate species displayed the lowest mean ␦15 N values as well as the lowest THg concentrations, while fish and benthic invertebrate feeders showed the highest mean ␦15 N values and THg concentrations (Kruskal–Wallis test, p < 0.0009). However, demerso-pelagic species present equivalent high ␦15 N values, but their THg concentrations were intermediate.

A positive linear relationship was found between logtransformed concentrations of THg and ␦15 N values for Guanabara and Ilha Grande bays (linear regression, p < 0.005), and was just above the significance level at Sepetiba Bay (linear regression, p > 0.06) (Fig. 2). Trophic magnification factors (TMF) were above 1 (Table 6), which indicates mercury accumulation in the food web and suggests diet as the major exposure route for this element (Borgå 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 and Lenanton, 1992; Wagemann et al., 1998).

The TMF values for Guanabara and Ilha Grande bays (1.51–1.67) were similar to those observed in arctic marine food web (1.59 – value converted from slope of the regression to TMF for comparison to our results) by Atwell et al. (1998) and in Gulf of St. Lawrence (1.48 – value converted) by Lavoie et al. (2010). They are slightly lower than those reported for three food webs from Beaufort Sea (ca. 1.8 – value converted) by Loseto et al. (2008a). For Alaskan 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 present study, the investigation performed by Dehn et al. (2006) focused largely on marine mammals rather than on overall mercury biomagnification through many taxonomic groups. Unbalanced study designs that include large numbers of high trophic level species, as in the investigation performed by Dehn et al. (2006), may affect the TMF results, so that TMF values can reflect biomagnification at these higher trophic levels rather than at full food web (Borgå et al., 2011).

Conversely, aspects other than biomagnification may be influencing mercury bioaccumulation in some species from Rio de Janeiro bays. This is especially evident in Sepetiba Bay, where a linear relationship between log THg concentrations and ␦15 N values was not observed. Guiana dolphin showed the highest mean mercury concentration (269.23 ng/g) for Sepetiba Bay, but not the highest ␦15 N values. This finding may be associated to bioaccumulation 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 and ␦15 N value to Sepetiba, Guanabara and Ilha Grande bays food webs, Rio de Janeiro Coast.

Sepetiba Baywinter Sepetiba Baysummer Guanabara Baywinter Guanabara Baysummer Ilha Grande Bay winter Ilha Grande Baysummer

n

Slope

SEslope

TMF

Intercept

R2

p-Value

155 175 86 74 105 100

0.07 0.07 0.19 0.18 0.21 0.22

0.04 0.04 0.03 0.03 0.07 0.05

1.19 1.17 1.55 1.51 1.63 1.67

0.31 0.46 −0.52 −0.51 −1.22 −1.50

0.02 0.02 0.36 0.30 0.07 0.19

0.0942 0.0665 0.0001 0.0001 0.0053 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 THg and body length was found (Loseto et al., 2008b).

Regarding most fish species and Guiana dolphins, higher THg concentrations were found in Guanabara and Ilha Grande bays than in Sepetiba Bay (p < 0.05). Ilha Grande and Sepetiba bays are adjacent bodies of water that are connected to each other by a channel.

Fig. 2. Relationship between ␦15 N 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, 䊉 planktivorous, benthic invertebrate feeder, fish and benthic invertebrate feeders, demerso-pelagic, ♦ Guiana dolphin.

T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302

Sepetiba Bay receives a substantial input of Hg from effluents of industries and cities located in its drainage basin, as well as from transposition of Paraíba do Sul River (Molisani et al., 2007). Several studies investigated the behavior of Hg in the latter bay and it was observed that a high percentage of the bioavailable Hg is transported to adjacent areas, such as Ilha Grande Bay and continental shelf waters. This transport would occur due to the high Hg-complexing capacity demonstrated by the dissolved organic matter (Lacerda and Malm, 2008; Molisani et al., 2007). The fact that higher THg concentrations were found in Ilha Grande Bay than in Sepetiba Bay (present study; Marins et al., 1998) suggests a lower bioavailability in the latter body of water (Lacerda and Malm, 2008).

This low bioavailability of THg in Sepetiba Bay may reflect in lower trophic transfer efficiency, explaining the lack of a linear relationship between log THg concentrations and ␦15 N values in Sepetiba Bay food web.

It is important to emphasize that the THg concentrations in biota from Ilha Grande Bay are not only higher than in organisms from Sepetiba Bay but also comparable to the THg levels in biota from Guanabara Bay. This finding may be a result of two factors: (1) the South Atlantic Central Water (SACW) influence over Ilha Grande Bay, as well as (2) partial transport of Hg complexed to organic matter from Guanabara Bay to continental shelf waters. Regarding the first aspect, it is important to mention that the SACW is considered to be a significant source of Hg to the continental shelf via upwelling (Cossa et al., 1996; Mason and Fitzgerald, 1993). Advection by upwelling is an example of a physical transport process with important implications in organic compound redistribution, especially for nektonic organisms (Dorneles et al., 2010). The SACW reach the superficial water during the summer and its influence over the southeast Brazilian region is well-know (Brandini et al., 1997), including the Ilha Grande Bay (Creed et al., 2007b). Concerning the second factor, it becomes interesting to consider that, in many estuaries, a significant percentage of the received Hg burden is exported from the body of water after being complexed to the organic matter (Kremling, 1988). Besides, it was observed that the eutrophication conditions of Guanabara Bay influences the bioavailability of Hg to organisms, promoting a decrease in its trophic transfer efficiency through the food web of that estuarine system (Kehrig et al., 2009).

The distinct TMF values found for the three food webs could be associated to the differences in THg bioavailability in each bay. The highest TMF value verified in the Ilha Grande Bay food web is likely to be a consequence of a higher percentage of bioavailable Hg in this estuary than in Sepetiba Bay or in Guanabara Bay. Although Ilha Grande Bay is the most preserved system among those considered herewith, our findings suggest that the highest THg trophic transfer efficiency observed in its food web results in higher THg concentrations in organisms from that Bay.

4. Conclusions Carbon and nitrogen isotopic findings revealed different trophic relationships in the food webs of Sepetiba, Guanabara and Ilha Grande bays. Variations in the THg biomagnification processes among the three food webs suggest that particular characteristics of each area are more likely to affect the TMF than the Hg burden received by each bay. Nitrogen isotopic values were successfully used for investigating trophic relationships and hence trophic magnification of Hg in the studied food webs. More studies are needed to explain variations in the trophic transfer of Hg in each bay, as well as among the food webs.

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Acknowledgments This work was supported by Rio de Janeiro State Government Research Agency – FAPERJ (“Pensa Rio” Program – Proc.

E-26/110.371/2007), Ministry of Education of Brazil – CAPES (“Ciencias do Mar” – Proc. 23038.051661/2009-18), Brazilian Research Council – CNPq (Proc. 482938/2007-2 and Proc. 480701/2009-1) and Cetacean Society International grant. TL Bisi has a scholarship from the Ministry of Education of Brazil – CAPES, J Lailson-Brito has a research grant from FAPERJ/UERJ (“Prociência” Program) and CNPq (grant #305303/2010-4), AF Azevedo has a research grant from CNPq (grant #304826/2008-1) and FAPERJ (JCNE #101.449/2010). G Lepoint and K Das are F.R.S. – FNRS Research Associates. We thank to Aquatic Mammal and Bioindicator Laboratory (MAQUA/UERJ) team for invaluable assistance in sampling, as well as in sample preparation for stable isotopes and total mercury determination. We particularly thank to Adriana Nascimento Gomes, Sylvia Chada, Regis Pinto de Lima and José Carlos from Estac¸ão Ecológica Tamoios (ESEC Tamoios-ICMBio) for logistical support in Ilha Grande Bay. We also thank two anonymous reviewers who made useful suggestions that have helped to improve the manuscript.

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