Ecological Indicators 18 (2012) 291–302
Contents lists available at SciVerse ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
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-Graduação 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: [email protected], [email protected] (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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T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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)
294
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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.
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
295
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)
13.4 ± 0.2
(n = 5)
14.3 ± 0.3
(n = 6)
14.5 ± 0.9
(n = 6)
14.9 ± 0.9
(n = 6)
13.4 ± 1.1
(n = 13)
14.1 ± 0.8
(n = 14)
13.8 ± 0.9
(n = 13)
14.2 ± 0.2
(n = 6)
13.9 ± 0.2
(n = 6)
14.8 ± 0.5
(n = 6)
296
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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.)
298
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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)
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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
300
T.L. Bisi et al. / Ecological Indicators 18 (2012) 291–302
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.
301
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
Estação 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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