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Bulletin of EnvironmentalContamination and Toxicology ISSN 0007-4861Volume 91Number 3 Bull Environ Contam Toxicol (2013)91:292-297DOI 10.1007/s00128-013-1058-8

Accumulation of Trace Metals in TwoCommercially Important Shrimp Speciesfrom Camamu Bay, Northeastern Brazil

Vitor Hugo Migues, Marcos de AlmeidaBezerra, Ana Karina de Francisco, MariaCecília Guerrazzi & Paulo RobertoAntunes de Mello Affonso

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Accumulation of Trace Metals in Two Commercially ImportantShrimp Species from Camamu Bay, Northeastern Brazil

Vitor Hugo Migues • Marcos de Almeida Bezerra •

Ana Karina de Francisco • Maria Cecılia Guerrazzi •

Paulo Roberto Antunes de Mello Affonso

Received: 23 February 2013 / Accepted: 2 July 2013 / Published online: 16 July 2013

� Springer Science+Business Media New York 2013

Abstract Camamu Bay is the second largest estuary in

Bahia state, northeastern Brazil, being recognized by its high

diversity and economical relevance for fisheries and tourism.

To evaluate the impacts of environmental disturbances in

Camamu Bay, trace metals (Cr, Mn, Fe, Co, Ni, Cu, and Pb)

were quantified in two widespread and commercially

exploited shrimp species (Farfantepenaeus paulensis and

Xiphopenaeus kroyeri). High concentrations of all metals but

Pb were observed in both species by ICPOES. The concen-

tration values for Cr, Co, and Mn were invariably higher than

the accepted limits for human consumption in Brazil. Inter

and intraspecific variation in metal levels might be related to

biological particularities and body size. The accentuated

contamination by trace metals in both species validated them

as efficient bioindicators of environmental quality. Thus,

effective planning, monitoring and regulatory policies

should be adopted to inspect and remediate the metal con-

tamination in natural resources from Camamu Bay.

Keywords Estuary � ICPOES � Farfantepenaeus

paulensis � Xiphopenaeus kroyeri

Tropical estuaries are biodiversity hotspots rich in natural

resources and threatened by different pollution sources.

Since estuaries are the final destination of surrounding

drainages, they are vulnerable to pollutants by runoffs and

effluents from areas up to hundreds of kilometers away

(Lacerda et al. 2002). Among these, urban-industrial

effluents are particularly harmful on estuaries and coastal

ecosystems, causing contamination of sediments, water and

organisms (Christophoridis et al. 2009; Sudhanandh et al.

2011).

Trace and heavy metals are easily measurable pollutants

that might determine long-term effects in communities

(Sudhanandh et al. 2011; Kabir et al. 2012). In marine

species such as fish, shellfish and crustaceans, trace metals

can accumulate at hazardous levels once either essential or

non-essential elements are toxic to organisms at high

concentrations (Jones et al. 2000). As a result, richness and

abundance of macrobenthos or even pelagic organisms

might decrease in contaminated estuaries (Venturini et al.

2008). In turn, this process awakes to economical and

public health damages inasmuch as marine species are an

important income for fisheries (Hossain and Khan 2001;

Mitra et al. 2012).

Camamu Bay is a shallow estuarine system on southern

coast of Bahia state, northeastern Brazil, encompassing

nearly 384 km2. Although Camamu Bay represents an

important location for growth and reproduction of coastal

species, this ecosystem has been affected by oil and gas

industry over fields located a few miles towards the ocean

and by former barite extraction around two islands in this

bay (Hatje et al. 2008; Paixao et al. 2010).

In 2003, fish mortality was documented in Camamu Bay

and environmental agencies carried out extensive chemical

analyses in this region reporting high levels of As, Cd, and

Hg afterwards (GEIA and EVEREST 2003). Nonetheless,

V. H. Migues � M. de Almeida Bezerra

Department of Chemistry and Exact Sciences,

Universidade Estadual do Sudoeste da Bahia,

Jequie, BA, Brazil

A. K. de Francisco � M. C. Guerrazzi �P. R. A. de Mello Affonso (&)

Department of Biological Sciences, Universidade Estadual do

Sudoeste da Bahia, Av. Jose Moreira Sobrinho, s/n, Jequie,

BA 45206-190, Brazil

e-mail: paulomelloaffonso@yahoo.com.br

123

Bull Environ Contam Toxicol (2013) 91:292–297

DOI 10.1007/s00128-013-1058-8

Author's personal copy

Camamu Bay has further regarded as a relatively low

impacted area in relation to other coastal systems based on

studies of macrobentho communities and quantification of

metals in sediment (Hatje et al. 2008).

On the other hand, chemical analysis of water and

sediments might be insufficient to evaluate contaminated

areas and their effects in living organisms (Abdel-Moneim

et al. 2012). Therefore, the goal of this study was to ana-

lyze the concentration of trace metals in shrimp species

from Camamu Bay, NE Brazil, in order to determine

environmental quality and the accumulation potential of

these elements in seafood from this region.

Materials and Methods

Samples of Farfantepenaeus paulensis and Xiphopenaeus

kroyeri were collected with trawl nets in January, June and

October 2011 and July 2012 in three collection sites along

Camamu Bay (Fig. 1). The salinity levels ranged from

40 ppm in Serinhaem coast (site 1) to 36 ppm in Flores

Island (site 3), without significant differences among sea-

sons inasmuch as rainfall remained similar over seasons.

Sandy to muddy bottom was observed in all collection

sites.

The samples were placed in identified by collection site/

period and kept under refrigeration. The wet weight of

individuals varied from 2.2195 to 10.1204 g in F. paulensis

and from 1.5362 to 8.3352 g in X. kroyeri. The material

was dehydrated at 105�C for 24 h in a drying oven. The

dehydrated matter was ground with pestle in porcelain

mortar and then sieved through a nylon sieve to obtain a

homogenous dust. Dry samples (100 mg) of muscle and

other tissues were used after removal of exoskeleton and

digested in open-system with 5.0 mL of 65 % (v/v) of

HNO3 (Merck) and 2.0 mL of 30 % (v/v) of H2O2 (Vetec)

for 4 h at 120�C up to full digestion. The digested material

was dissolved in HNO3 at 1.00 mol L-1 and stored at 4�C

to quantification of trace elements (Cr, Mn, Fe, Co, Ni, Cu,

and Pb).

The analytical curves were established using diluted

solutions with different metal concentrations. All elements

were analyzed in triplicates using ICPOES (Optima 3000DV

sequential Perkin-Elmer). Method validation was assured by

comparing two certified reference materials (CRM) for trace

metals in fish (DORM-2) and mussel (SRM 2976), following

the same digestion procedure of shrimp samples. The limits

of detection (LOD) and quantification (LOQ) were calcu-

lated using background equivalent concentration (BEC) to

establish the lowest concentration of trace metals (mg kg-1)

(Table 1). The values of each trace metal in shrimp were

compared to the allowed levels in food by resolution n.

685/98 of the National Agency of Sanitary Care from Brazil

(ANVISA 1998), when available.

Fig. 1 Map of Camamu Bay, Bahia state, NE Brazil, showing collection sites of F. paulensis (FP) and X. kroyeri (XK): 1 Serinhaem coast;

2 Tubarao coast; 3 Flores Island

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Results and Discussion

The recovery percentages of concentration values in cer-

tified samples were consistent, ranging from 96 % to

117.87 % for most of studied metals, except Pb (Table 1).

These results represent the accuracy of data and precision

of measured values.

The mean concentration of trace metals in samples of

F. paulensis (FP) and X. kroyeri (XK) were established

after triplicate analysis. In the case of Pb, the concentra-

tions were below the LOQ by ICPOES (Table 2).

High levels of Co (7.05–14.37 lg g-1), Cr (8.05–18.2

lg g-1), Cu (15.75–41.76 lg g-1), Fe (24.69–344.4 lg g-1),

Mn (10.51–23.51 lg g-1) and Ni (8.02–16.58 lg g-1) were

observed in all shrimp samples, being above the allowed

levels in food (ANVISA 1998) (Table 2). In the case of Fe,

this limit refers to the maximum amount of daily con-

sumption since iron is an essential micronutrient (Martins

2012). The maximum concentration values for Cu and Ni

are not established for food in Brazil although accumula-

tion of these elements in inorganic state is harmful (Luoma

and Rainbow 2008).

Lead was the only element that could not be quantified

by ICPOES (\LOQ). This result in particular differs from

previous studies in sediment of Camamu Bay and nearby

estuaries in which high levels of Pb have been detected

(Hatje and Andrade 2009; Paixao et al. 2010). On the other

hand, the mean concentration of trace metals in this study

followed the pattern Cu [ Ni [ Cr commonly reported

(Biney and Ameyibor 1992; Pourang and Dennis 2005).

These results can be related to distinct pollution spots in

Camamu Bay. Extraction and transportation of oil close to

the estuary are potential sources of metal contamination

(Hatje et al. 2008). For instance, Todos os Santos Bay,

located 120 km northwards, is highly impacted by indus-

tries and urbanization, including Salvador (about 3 million

people) (Hatje and Andrade 2009). Thus, toxic substances

from Todos os Santos Bay could be carried to Camamu

Bay by the north–south Brazil Current. Indeed, Santos-

Echeandıa et al. (2012) reported large amounts of waste

debris at beaches southern to Salvador coast, including

Camamu Bay. In addition, Grande Island in Camamu Bay

had served as the main barite mine in Brazil (MME 2009).

Although this mining site is currently abandoned, trace

metals could have contaminated this bay during extraction

and accumulated in aquatic organisms (Paixao et al. 2010).

Usually, the distribution of trace metals along estuaries

decreases from inner zones towards open sea (Hatje and

Andrade 2009). Based on mean concentration of trace

metals per site (Fig. 2), this pattern was only identified for

Cu. This result indicates that this metal has a preferential

lithogenic origin (Santos-Echeandıa et al. 2012), possibly

related to inland sewage, once this is a main source of Cu

contamination (Thomson et al. 1984).

On the other hand, the mean concentration of other metals

in shrimps from each collection site along Camamu Bay

revealed a distinct scenario, being higher in samples from

Tubarao (Mn, Ni, Co) and/or Serinhaem coast (Fe, Cr)

(Fig. 2). Similar results were reported in some estuaries and

have been related to adsorption of suspended metals, bio-

genic origin and widespread human impacts along the nearby

drainages, all leading to a scattered distribution pattern

(Hatje et al. 2001; Santos-Echeandıa et al. 2012). High

amounts of Fe, Cr and other metals were also reported in

sediment samples of Camamu Bay by Hatje et al. (2008),

putatively derived from untreated urban and industrial

sewage. Analogously, these activities could determine the

bioaccumulation in macrobenthos, like shrimps, once they

live in association with sea bottom and are directly affected

by sediment contamination (Campbell et al. 1988). There-

fore, these organisms provide reliable estimative of envi-

ronmental pollution and risk assessment.

The differential metal accumulation between both shrimp

species is noteworthy. In Serinhaem coast, the levels of trace

metals were higher in X. kroyeri than in F. paulensis

(Table 2). Such pattern might be related to behavioral traits

Table 1 Certified and obtained measurements (mean ± SD) of reference material (CRM), percentage of recovery, and LOD and LOQ values

(mg kg-1) for each metal

Metal SRM 2976 DORM 2 LOD LOQ

Certified Measureda Recovery (%) Certified Measureda Recovery (%)

Co 0.610 ± 0.02 0.601 ± 0.04 98.36 0.182 ± 0.031 0.178 ± 0.023 97.80 0.42 9 10-2 1.40 9 10-2

Cr 0.500 ± 0.16 0.485 ± 0.13 96.00 34.7 ± 5.5 33.4 ± 1.3 96.25 0.12 9 10-2 0.40 9 10-2

Cu 4.02 ± 0.33 3.99 ± 0.17 99.25 2.34 ± 0.16 2.42 ± 0.11 103.4 0.09 9 10-2 0.30 9 10-2

Fe 171 ± 4.9 201 ± 5.6 117.8 142 ± 10 144 ± 7.9 101.4 0.45 9 10-2 2.00 9 10-2

Mn - – – 3.66 ± 0.34 3.82 ± 0.22 103.4 0.18 9 10-2 0.60 9 10-2

Ni 0.930 ± 0.12 0.974 ± 0.24 104.3 19.4 ± 3.1 21.4 ± 2.8 110.3 0.16 9 10-2 0.57 9 10-2

Pb 1.19 ± 0.18 1.17 ± 0.13 98.31 0.0652 ± 0.007 \LOQ – 28.79 9 10-2 95.97 9 10-2

a Based on triplicates

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of each species, once bioaccumulation is influenced by

environmental diffusion and feeding (Campbell et al. 1988;

Chou et al. 2002). Once F. paulensis is an estuarine species

recruited to the coast only during breeding season (Dall et al.

1990), this species could be less exposed to trace metals in

sediments of Serinhaem once feeding is reduced or absent

during recruitment and the individuals would spend shorter

periods in this area.

Inversely, X. kroyeri is less dependent on estuaries,

inhabiting shallow coastal areas over most of life cycle

(Castro et al. 2005). Actually, the sampling of X. kroyeri in

Flores Island is unusual and might be associated to the

Table 2 Concentration (mean ± SD) of trace metals (lg g-1) in shrimp samples

Site Samples Co Cr Cu Fe Mn Ni

Serinhaem coast FP1 10.42 ± 0.02 14.91 ± 0.10 16.10 ± 0.50 95.10 ± 0.60 19.81 ± 0.11 11.23 ± 0.42

FP2 10.51 ± 0.01 14.32 ± 0.10 24.08 ± 2.04 162.1 ± 2.60 18.15 ± 0.13 10.71 ± 0.16

FP3 10.62 ± 0.01 18.54 ± 0.20 16.04 ± 1.02 344.4 ± 30.20 11.43 ± 0.12 11.07 ± 0.11

FP4 10.62 ± 0.03 17.55 ± 0.10 36.06 ± 1.03 166.7 ± 10.10 14.70 ± 0.11 11.13 ± 0.14

FP5 10.73 ± 0.01 18.26 ± 0.20 22.01 ± 6.04 245.8 ± 10.10 10.82 ± 0.09 10.92 ± 0.13

FP6 10.54 ± 0.02 14.16 ± 0.10 18.07 ± 4.01 95.10 ± 0.90 19.87 ± 0.15 11.75 ± 0.15

FP7 10.41 ± 0.01 14.64 ± 0.10 24.04 ± 1.04 62.15 ± 0.60 18.15 ± 0.14 10.40 ± 0.10

FP8 10.37 ± 0.01 16.52 ± 0.10 17.05 ± 1.02 280.4 ± 20.30 12.26 ± 0.08 11.26 ± 0.42

XK1 14.23 ± 0.05 16.08 ± 0.06 41.76 ± 0.45 112.9 ± 3.18 20.93 ± 0.22 15.97 ± 0.06

XK2 14.35 ± 0.09 16.25 ± 0.03 39.10 ± 2.02 85.16 ± 3.09 21.45 ± 0.02 16.58 ± 0.42

XK3 14.34 ± 0.07 16.02 ± 0.18 21.39 ± 0.25 57.36 ± 2.86 18.39 ± 2.01 16.20 ± 0.34

XK4 14.37 ± 0.02 16.35 ± 0.02 40.38 ± 0.06 136.1 ± 0.20 21.51 ± 0.03 16.13 ± 0.02

XK5 14.37 ± 0.01 16.12 ± 0.19 38.47 ± 1.66 58.51 ± 0.28 19.52 ± 0.17 16.05 ± 0.07

XK6 14.21 ± 0.18 15.93 ± 0.01 38.65 ± 1.02 83.60 ± 0.68 21.52 ± 0.25 16.03 ± 0.09

XK7 14.16 ± 0.02 15.68 ± 0.02 17.64 ± 0.02 24.69 ± 0.65 17.35 ± 0.15 16.12 ± 0.02

XK8 14.32 ± 0.07 16.29 ± 0.08 29.63 ± 0.04 221.65 ± 4.38 23.51 ± 0.12 16.25 ± 0.02

XK9 14.26 ± 0.06 16.13 ± 0.06 37.80 ± 0.02 100.02 ± 0.68 21.29 ± 0.06 16.05 ± 0.06

XK10 14.28 ± 0.08 15.68 ± 0.07 24.65 ± 0.42 126.37 ± 0.12 14.24 ± 0.05 16.25 ± 0.03

XK11 14.27 ± 0.02 15.81 ± 0.02 15.75 ± 0.03 146.34 ± 0.15 17.24 ± 0.02 16.25 ± 0.02

XK12 14.34 ± 0.07 17.84 ± 0.09 27.32 ± 0.13 128.76 ± 2.35 16.15 ± 0.06 16.22 ± 0.03

Tubarao coast FP9 10.52 ± 0.02 14.5 ± 0.010 34.50 ± 2.00 66.72 ± 0.20 17.71 ± 0.06 11.09 ± 0.18

FP10 10.64 ± 0.01 14.2 ± 0.010 22.09 ± 1.50 99.08 ± 0.10 15.82 ± 0.11 10.62 ± 0.17

FP11 10.62 ± 0.01 15.9 ± 0.010 24.20 ± 1.01 80.05 ± 0.10 15.42 ± 0.14 10.54 ± 0.12

FP12 10.53 ± 0.01 13.9 ± 0.010 25.12 ± 3.02 126.1 ± 1.00 10.51 ± 0.13 10.73 ± 0.16

FP13 10.58 ± 0.04 15.2 ± 0.010 17.15 ± 1.05 179.1 ± 1.10 17.33 ± 0.11 10.41 ± 0.11

FP14 10.58 ± 0.02 14.7 ± 0.010 20.09 ± 1.03 63.50 ± 0.10 14.81 ± 0.12 10.94 ± 0.13

FP15 10.14 ± 0.03 16.4 ± 0.020 18.05 ± 1.01 66.00 ± 0.100 14.62 ± 0.07 12.07 ± 0.34

FP16 10.27 ± 0.02 17.4 ± 0.010 23.03 ± 1.02 96.00 ± 0.500 16.60 ± 0.02 11.33 ± 0.22

Flores Island XK13 7.050 ± 0.009 8.005 ± 0.003 33.10 ± 2.50 72.56 ± 5.09 11.15 ± 0.02 8.483 ± 0.01

XK14 7.342 ± 0.002 8.012 ± 0.008 29.39 ± 1.25 77.86 ± 1.86 12.22 ± 0.01 8.231 ± 0.03

XK15 7.174 ± 0.005 8.005 ± 0.002 40.38 ± 2.06 76.10 ± 6.20 11.71 ± 0.03 8.372 ± 0.02

XK16 7.136 ± 0.007 8.204 ± 0.009 38.47 ± 1.06 78.11 ± 4.28 12.52 ± 0.07 8.254 ± 0.02

XK17 7.217 ± 0.004 8.074 ± 0.003 35.65 ± 2.02 73.30 ± 3.18 13.52 ± 0.05 8.111 ± 0.04

XK18 7.604 ± 0.001 8.205 ± 0.004 31.04 ± 1.02 74.79 ± 2.33 13.35 ± 0.05 8.692 ± 0.05

XK19 7.322 ± 0.003 8.036 ± 0.006 26.43 ± 2.04 71.05 ± 3.54 12.11 ± 0.02 8.342 ± 0.05

XK20 7.553 ± 0.008 8.022 ± 0.006 31.80 ± 2.02 70.92 ± 2.68 11.29 ± 0.06 8.227 ± 0.03

XK21 7.154 ± 0.006 8.041 ± 0.005 29.65 ± 1.42 76.17 ± 2.15 11.21 ± 0.03 8.156 ± 0.07

XK22 7.431 ± 0.006 8.065 ± 0.002 36.75 ± 1.03 76.44 ± 3.17 11.18 ± 0.02 8.049 ± 0.04

XK23 7.349 ± 0.002 8.090 ± 0.009 40.02 ± 3.13 78.06 ± 2.66 11.15 ± 0.06 8.022 ± 0.02

ANVISA 0.2–0.7 0.1 – 18 4.0 –

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bottom type and high salinity of this location (36 ppm).

Moreover, high amounts of sediment are reported in

stomach of X. kroyeri, probably due to accidental ingestion

during feeding (Branco and Junior 2001). Therefore, the

bioaccumulation levels in X. kroyeri could reflect more

proportionally the metal levels in sediments of Serinhaem

coast (Hatje et al. 2008) and the long-term exposition to

pollutants from other contamination sources along Bahia

shore (e.g. Todos os Santos Bay). Unfortunately, the lack

of detailed biological studies in penaeids from Brazilian

coast restrains further inferences on species-specific con-

tamination patterns.

Intraspecific variation per locality was also identified

(Table 2) and can be caused by size variation of individuals

(1.5362–10.1204 g). A linear relationship between body

size and metal contamination is commonly reported

showing that large individuals, putatively exposed for

longer periods to contaminants, would have increased

metal levels (Han et al. 1997). However, there are few

studies correlating individual size and bioaccumulation in

shrimps (Garcia and Niencheski 2012) but the distinction

of samples according to body size might be useful to relate

bioaccumulation processes to development stage.

Finally, the bioaccumulation of trace metals in shrimp

stocks from Camamu Bay are important for monitoring this

region, validating F. paulensis and X. kroyeri as bioindi-

cators of metal contamination. The presence of toxic con-

taminants in these samples is a threat to biodiversity and

public health, since both species are important fishery

resources and play a key role in coastal ecosystems. Thus,

effective policies to control environmental contamination

in Camamu Bay and nearby areas should be implemented

to minimize the risks of toxicity to both biota and humans.

Acknowledgments The authors acknowledge Fundacao de Amparo

a Pesquisa do Estado da Bahia (FAPESB) for the financial support

(PET0035/2010) and Instituto Chico Mendes (ICMBio) for autho-

rizing sample collection (SISBIO 27027-1).

References

Abdel-Moneim AM, Al-Kahtani MA, Elmenshawy OM (2012)

Histopathological biomarkers in gills, liver of Oreochromis

niloticus from polluted wetland environments, Saudi Arabia.

Chemosphere 88:1028–1035

ANVISA (1998) Resolution n. 685 on March 24th. Available at

http://www.anvisa.gov.br/legis/portarias/685_98.htm. Accessed

20 Feb 2013

Biney CA, Ameyibor E (1992) Trace metal concentrations in the pink

shrimp Penaeus notialis from the coast of Ghana. Water Air Soil

Poll 63:273–279

Branco JO, Junior HCM (2001) Alimentacao natural do camarao sete-

barbas, Xıphopenaeus kroyeri (Heller) (Crustacea, Decapoda), na

Armacao do Itapocoroy, Penha, Santa Catarina. Rev Bras Zool

18(1):53–61

Campbell PGC, Lewis AG, Chapman PM, Crowder AA, Fletcher

WK, Imber B, Luoma SN, Stokes PM, Winfrey M (1988)

Biologically available metals in sediments. Publications NRCC/

CNRC, Ottawa

Castro RH, Costa RC, Fransozo A, Mantelatto FLM (2005) Popula-

tion structure of the seabob shrimp Xiphopenaeus kroyeri

(Heller, 1862) (Crustacea: Penaeoidea) in the litoral of Sao

Paulo. Brazil Sci Mar 69(1):105–112. doi:10.3989/scimar.2005.

69n1105

Chou CL, Paon LA, Moffatt JD (2002) Cadmium, copper, manganese,

silver and zinc in rock crab (Cancer irroratus) from highly

copper contaminated sites in the Inner Bay of Fundy, Atlantic

Canada. Bull Environ Contam Toxicol 68:885–892

Christophoridis C, Dedepsidis D, Fytianos K (2009) Occurrence,

distribution of selected heavy metals in the surface sediments of

Thermaikos Gulf, N. Greece: assessment using pollution indica-

tors. J Hazard Mater 168(2–3):1082–1091. doi:10.1016/j.jhazmat.

2009.02.154

Dall W, Hill BJ, Rothlisberg PC, Staples DJ (1990) The biology of the

penaeidae. In: Blaxter J, Southward A (eds) Advances in marine

biology, vol 27. Academic Press, London, pp 1–489

Garcia JG, Niencheski LFH (2012) Avaliacao temporal da acumu-

lacao de elementos traco no camarao-rosa Farfantepenaeus

paulensis no estuario da Lagoa dos Patos, RS, Brasil. Trop

Oceanogr 40(2):327–339. doi:10.5914/to.2011.0077

GEIA (Grupo de Estudo de Impacto Ambiental UFPR) e EVEREST

(Tecnologia em Servicos ES) (2003) Gerenciamento Ambiental

da Atividade de Aquisicao de Dados Sısmicos Marıtimos da PGS

e sua contribuicao para elucidacao das causas de mortandade de

peixes na regiao da Baıa de Camamu (BA). Vol. II and

Appendixes I to IV. Brazil

Han BC, Jeng WL, Jeng MS, Kao LT, Meng PJ, Huang YL (1997)

Rock-shells (Thais clavigera) as an indicator of As, Cu, and Zncontamination on the Putai coast of the black-foot disease area in

Taiwan. Arch Environ Contam Toxicol 32(4):456–461

Hatje V, Andrade JA (2009) Baıa de Todos os Santos: aspectos

oceanograficos. EDUFBA, Salvador, BA. Brazil. ISBN:978-85-

232-0597-3

Hatje V, Birch GF, Hill DM (2001) Trace metal, total suspended

solids concentrations in freshwater: the importance of small-

scale temporal variation. J Environ Monit 3:251–256

Hatje V, Barros F, Magalhaes W, Riatto VB, Amorim FN, Figueiredo

MB, Spano S, Cirano M (2008) Trace metals, benthic macro-

fauna distributions in Camamu Bay, Brazil: sediment quality

prior oil, gas exploration. Mar Pollut Bull 56:348–379

Fig. 2 Mean concentration of trace metals in analyzed samples

according to collection site

296 Bull Environ Contam Toxicol (2013) 91:292–297

123

Author's personal copy

Hossain MS, Khan YSA (2001) Trace metals in penaeid shrimp and

spiny lobster from the Bay of Bengal. Sci Asia 27:165–168

Jones GB, Mercurio P, Olivier F (2000) Zinc in fish, crabs, oysters,

and mangrove flora, fauna from Cleveland Bay. Mar Pollut Bull

41:345–352

Kabir E, Ray S, Kim KH, Yoon HO, Jeon EC, Kim YS, Cho YS, Yun

ST, Brown RJC (2012) Current status of trace metal pollution in

soils affected by industrial activities. Sci World J. doi:10.1100/

2012/916705

Lacerda LD, Kremer HH, Kjerfve B, Salomons W, Marshall-

Crossland JI, Crossland JC (2002) South American basins:

LOICZ global change assessment, synthesis of river catchment –

coastal sea interaction and human dimensions. LOICZ R&S 21

Reports & Studies n. 21

Luoma NS, Rainbow OS (2008) Metal contamination in aquatic

environments. Science lateral management. Cambridge Univer-

sity Press, Cambridge

Martins JM (2012) Universal iron fortification of foods: the view of a

hematologist. Rev Bras Hematol Hemoter 34(6):459–463

Mitra A, Barua P, Zaman S, Banerjee K (2012) Analysis of trace

metals in commercially important crustaceans collected from

UNESCO protected world heritage site of Indian Sundarbans.

Turk J Fish Aquat Sci 12:53–66

MME—Ministerio de Minas e Energia (2009) Perfil da barita.

Relatorio Tecnico 42. www.mme.gov.br/sgm/galerias/…/P28_

RT42_Perfil_da_Barita.pdf

Paixao JF, Oliveira OMC, Dominguez JML, Coelho ACD, Garcia KS,

Carvalho GC, Magalhaes WF (2010) Relationship of metal

content, bioavailability with benthic macrofauna in Camamu

Bay (Bahia, Brazil). Mar Pollut Bull 60:474–481

Pourang N, Dennis JH (2005) Distribution of trace elements in tissues

of two shrimp species from the Persian Gulf, roles of metallo-

thionein in their redistribution. Environ Int 31:325–341

Santos-Echeandıa J, Prego R, Cobelo-Garcıa A, Caetano M (2012)

Metal composition, fluxes of sinking particles, post-depositional

transformation in a ria coastal system (NW Iberian Peninsula).

Mar Chem 134–135:36–46

Sudhanandh VS, Udayakumar P, Ouseph PP, Amaldev S, Babu KN

(2011) Dispersion, accumulation trend of heavy metals in

coastal, estuarine sediments, its textural characteristics and a

case study in India. J Hum Ecol 36(2):85–90

Thomson EA, Luoma SN, Johansson CE, Cain DJ (1984) Comparison

of sediments and organisms in identifying sources of biologically

available trace metal contamination. Water Res 18(6):755–765

Venturini N, Muniz P, Bıcego MC, Martins CC, Tommasi LR (2008)

Petroleum contamination impact on macrobenthic communities

under the influence of an oil refinery: integrating chemical,

biological multivariate data. Estuar Coast Shelf Sci 78:457–467

Bull Environ Contam Toxicol (2013) 91:292–297 297

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