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Concentration and Bioavailability of Heavy Metals in Sediments from NiteróiHarbour (Guanabara Bay/S.E. Brazil)Author(s): José Antônio Baptista Neto, Mirian Crapez, John J. McAlister, and Claudia Gutterres VilelaSource: Journal of Coastal Research, Number 214:811-817. 2005.Published By: Coastal Education and Research FoundationDOI: http://dx.doi.org/10.2112/012-NIS.1URL: http://www.bioone.org/doi/full/10.2112/012-NIS.1

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Journal of Coastal Research 21 4 811–817 West Palm Beach, Florida July 2005

Concentration and Bioavailability of Heavy Metals inSediments from Niteroi Harbour(Guanabara Bay/S.E. Brazil)Jose Antonio Baptista Neto†, Mirian Crapez‡, John J. McAlister§, and Claudia Gutterres Vilela††

†Depto de Geografia—FFP/UERJ

Departamento de Geologia—LAGEMAR/UFF/Brazil

jneto@igeo.uff.br

‡Laboratorio de MicrobiologiaMarinha—PPGBM/UFF/Brazil

mirian@vm.uff.br

§School of GeographyThe Queen’s University of

Belfast, UKj.mcalister@qub.ac.uk

††Depto de Geologia/IGEO/CCMN

Universidade Federal do Riode Janeiro, Brazil

vilela@igeo.ufrj.br

ABSTRACT

BAPTISTA NETO, J.A.; CRAPEZ, M.; MCALISTER, J.J., and VILELA, C.G., 2005. Concentration and bioavailabilityof heavy metals in sediments from Niteroi Harbour (Guanabara Bay/S.E. Brazil). Journal of Coastal Research, 21(4),811–817. West Palm Beach (Florida), ISSN 0749-0208.

The coastal area of Niteroi is marked by intensive naval activities and holds one of the countries main naval estates.The harbour and dockyards have been sited in the international literature as potential sources and sinks for accu-mulation of heavy metals and hence contaminated sediments. The aim of this paper is to assess the concentrationsof heavy metals in Niteroi Harbour and verify their bioavailability by determining the catalytic effects of the bacteriausing esterase activity (EST) and electron transport system activity (ETSA). Samples were analysed for Ni, Zn, Pb,Cr and Cu and normalisation procedures were used to assess whether their concentrations represent background orcontamination of the sediment. Heavy metal concentrations, especially for Cu, Zn and Pb were found to be muchhigher than natural background levels and the index of ‘‘geoaccumulation’’ shows moderate to extreme contamination.However, the absence of the inhibition of dehydrogenase activity indicated that the analysed heavy metals are notbioavailable in the EC50 values.

ADDITIONAL INDEX WORDS: Heavy metals, bacteria, bioavailability.

INTRODUCTION

One of the unfortunate side effects of industrialization isthe discharge of heavy metals into the environment and it isnow accepted that the study of heavy metal distribution inthe associated sediments is a useful way to monitor the inputof such pollutants (STOFFERS et al., 1986; SALOMONS andFORSTNER, 1984; SUMMERHAYERS et al., 1985; ANGELIDIS

and ALOUPI, 2000).Guanabara Bay is considered to be one of the most polluted

environments of the Brazilian coastline. Heavy metal con-tamination accounts for a high percentage of this pollution(REBELLO et al., 1986; VANDENBERG and REBELLO, 1986;LEAL and WAGENER, 1993; BAPTISTA NETO et al., 2000), andit is very important to access their main sources. In recentyears, discussions concerning the pollution in Guanabara Bayhave considered sewage and litter to be the main sources,however, other sources of pollution, such as dockyards andharbours should also be assessed. Dockyards and harbour ar-eas have been described in the international literature as typ-ical locations where sediment-associated pollutants can ac-cumulate. A study carried out by BELLINGER and BENHAM

(1978) on the concentration of metals in dockyard sedimentsand water deals particularly with contributions from ship-bottom paints. They concluded that high levels of Cu and Zn

DOI: 10.2112/012-NIS.1 received and accepted in revision 8 March2004.

probably stem from this source and lead may also be intro-duced from anticorrosive and primer paints. Most heavy met-al studies in harbours have been conducted in higher lati-tudes, as outlined by FORSTNER and WITTMAN (1981). Ac-cording to GIBBS (1993), heavy metals present a serious prob-lem and industrialized areas of North America and Europehave some of the most polluted harbours in the world. Thedisposal of dredged material, containing toxic metals hasposed an environmental problem for many years. Researchon the heavy metal pollution of harbours in tropical regionsis limited, however, work has been carried out in Fiji (NAIDU

and MORRISON, 1994); Hong Kong (OWEN and SANDHU,2000; TANNER et al., 2000) and Australia (GIBBS, 1993).

Coastal marine sediments are recognized as being impor-tant locations for nutrient regeneration, where bacteria con-stitute the primary agents of the early diagenesis of organicmatter. The mineralization of organic matter depends onboth the intensity and composition of its supply and environ-mental conditions. One of the most fundamental character-istics is probably the unique catalytic property of bacteriasince they contain extracellular enzymes that act on biopoly-mers and transform them into low-molecular-weight organiccarbon. An overall estimate of extracellular enzymes can beobtained by measuring the esterase activity (EST). The prod-ucts of the enzymatic hydrolysis are incorporated in the cells,where the oxidation processes are carried out. Oxidation oforganic matter occurs mostly in organisms that present re-

812 Baptista Neto et al.

Journal of Coastal Research, Vol. 21, No. 4, 2005

Figure 1. Map of the study area and sample stations.

Figure 2. Particle size of the bottom sediments from Niteroi Harbour.

spiratory chains and an overall estimate of aerobic and an-aerobic metabolism can be obtained by measuring the ETSA(RELEXANS, 1996). The biomass formed through microbial ac-tivity represents an important nutrient source for benthic or-ganisms (MEYER-REIL, 1986).

The aim of this paper is to determine the concentration ofheavy metals in Niteroi Harbour and also verify their bio-availability by determining the EST and ETSA activities ofthe bacteria.

METHODOLOGY

Surface Marine Sediments

Fifteen samples were collected using a Dietz Lafond grabsampler, from locations designed to provide a wide geograph-ic coverage of Niteroi Harbour (Figure 2).

Laboratory Analysis

Samples were stored in sealed polythene bags, transportedto the laboratory, air dried at 30–358C in a fan assisted oven,and separated into three sub-samples. One portion was usedfor chemical analysis, one for bacterial carbon, which includ-ed ETSA, EST, protein and lipid contents, and the other forphysical analysis. Samples for chemical analysis were ovendried at 1058C and the ,63 mm fractions separated by pass-ing them through a nylon mesh sieve. Sub-samples (0.1 g) ofthese fractions were digested in 5 ml of an aqua regia solutionunder pressure in PTFE digestion bombs. Oxidizable organiccarbon was determined using the WALKLEY and BLACK

(1934) technique and particle size analysis was carried outusing wet sieving (2 mm–63 mm) and pipette analysis (,63mm) techniques (VAN DOESBURG, 1996). Elemental analysiswas carried out using a Perkin Elmer Model 3100 atomic ab-sorption spectrophotometer. Bacterial carbon (CARLUCCI etal., 1986), ETSA (DAVIGNON and RELEXANS, 1989; TREVORS,1984), EST (STUBBERFIELD and SHAW, 1990), protein (LOW-RY et al., 1951) and lipid (FOLCH et al., 1957) contents werealso determined. The ETSA was measured without a surplusof electron donors.

813Concentration of Heavy Metals in Niteroi Harbour

Journal of Coastal Research, Vol. 21, No. 4, 2005

Figure 3. Diagram with the heavy metals concentrations in the study area.

RESULTS AND DISCUSSION

Particle Size Distribution

Both estuarine and bay environments are influenced bycontinental and marine factors. Sediment is generally a com-bination of minerals and organic detritus and its character-istics vary with depth and distance from the river mouthsand water movement patterns (tidal and wave-energy re-gimes) (BIGARELLA et al., 1978). In submarine channels thesediments are mostly residuals since strong tidal currents re-move the fine fraction. Sediments form a textural continuumranging from a sand-silt-clay mix on one side to well-sortedsand on the other, which represents the final product fromthe reworking of the sediments by wave and tidal action. Thewave and tidal currents lose energy in the inner part of thebay and when human influences become important in thecatchments, the sediment pattern and rate of sedimentationcan be completely disturbed. According to AMADOR (1997),poor sediment sorting is related to the superposition of dif-ferent sediment sources and the low energy of the tidal cur-rent circulation is due to the restricted nature of the area. Alarge number of particle size classes were also observed inthe study area (Figure 2), revealing very poor sediment sort-ing. This behaviour is also associated with the proximity andsuperposition of different sediment sources and with the in-fluence of anthropogenic sediments derived from the indus-trial and naval activities.

Geochemistry of the Sediments

Concentration values for Pb, Zn, Cu, Cr, Ni, Mn and Fe inthe surface sediments from Niteroi Harbour, marinas anddockyard are shown in Figure 3. Heavy metal distribution inthe marine sediments are influenced by texture, clay-miner-

als, organic matter, oxides, oxyhydroxides of iron and man-ganese and calcium carbonate (SALOMONS and FORSTNER,1984). The harbour, marinas and dockyards are normally re-stricted areas and consequently have a low circulation, whichmakes them preferential sites for the deposition of pollution.Figure 3 shows the concentrations of Cu, Pb, Zn, Ni and Crin Niteroi litoral, where Zn, Cr and Ni show similar patterns.Higher concentrations were found in sample 6, which is lo-cated in one side of the harbour that has an active dockyardwith ship painting activities. These elements have been foundin the paints used in the naval industry (BELLINGER andBENHAM, 1978). Figure 3 indicated higher concentrations inthose samples located close to Niteroi harbour (see Figure 1)and the dockyard than those recorded in the internationalliterature (FORSTNER and WITTMANN, 1983; SMITH and OR-FORD, 1989; SUBRAMANIAN et al., 1988).

It is difficult to estimate the extent of the anthropogenicinput from heavy metals in many polluted environments,since there is no direct evidence relating to their concentra-tions in sediment from pre-industrial periods (GROOT et al.,1976). However, in this study area, data for heavy metal con-centrations in rocks, soils, coastal lagoons and JurujubaSound are available (Table 1). Data for heavy metal concen-trations in sediments collected in the base of a dated corefrom Jurujuba Sound also exists and is used as backgroundvalues for others areas along the Niteroi litoral. This impor-tant data allows us to make comparisons and evaluate thelevel of pollution in the study area.

Maximum, minimum and average concentrations of heavymetal concentrations in different environments in the Niteroimunicipality are shown in Table 1. These levels show thisstudy area to be one of the most polluted in the region.

814 Baptista Neto et al.

Journal of Coastal Research, Vol. 21, No. 4, 2005

Table 1. Concentrations of heavy metals in the study area (minimum–maximum) (average), compared with values from the literature.

Location Pb (ppm) Zn (ppm) Cu (ppm) Cr (ppm) Ni (ppm) Fe (ppm) Mn (ppm)

This study Niteroi Harbour

Jurujuba Sound1

Background1

45–12084

5–12361

15–4024.4

115–85029915–337158

212.2–13258.4

35–14502415–213

516.3–17.5

9

75–230116

10–22389

30–4940.5

30–11063

15–7948

11–4927

18500–550026900

1000–2125012573

13750–2975021775

105–405160

10–414182

50–200117

Soils from Niteroi1

Rock–augen gneiss2

Piratininga Lagoon3

11–110333047

41–537945428

18–84412811

24–1167715—

14–704078—

5250–553752858622652

—

7.5–787273354—

Itaipu Lagoon3

Average Shale4

Average sandstone4

24207

449516

194510

—9035

—682

—470009800

—85050

1 Baptista Neto et al. (1999); 2 B. Sanches, personal communication (1993); 3 Knoppers et al. (1989); 4 Turekian and Wedepohl (1961).

Table 2. The range of enrichment factors for the metals in the sedimentsfrom Niteroi Harbour.

Sample Ni/Fe Cr/Fe Cu/Fe Zn/Fe Ph/Fe

12345

2.92.82.51.83.3

1.11.11.11.21.2

13.54.88.0

25.017.3

5.82.33.23.45.3

4.82.43.02.15.3

6789

10

1.71.81.82.31.8

1.01.01.11.11.2

66.011.313.812.311.0

5.74.34.93.82.9

2.14.04.83.74.0

1112131415

2.31.71.21.11.3

1.11.00.90.91.0

40.526.05.35.89.5

6.63.02.82.73.9

4.21.42.12.13.5

Enrichment Factors

To reduce the effects caused by grain size and mineralogyin metal variability and identify possible anomalous metalcontributions, geochemical normalisation of the heavy metaldata to conservative elements such as Fe was used in thisstudy (RULE, 1986). Resulting Metal/Fe ratios indicate thelevel of the metal enrichment by providing enrichment fac-tors, (EF) for each metal (ERGIN et al. (1991).

(conc. /conc. )sampleme FeE.F.(me) 5 (1)(conc. /conc. )backgroundme Fe

Baseline levels for metals in the deeper layers of the corescollected in Jurujuba Sound (BAPTISTA NETO et al., 1999)were used as a background for trace metals, to give a commonreference point for comparison. A value of 1 means neitherenrichment nor depletion occurred in relation to the back-ground level. Enrichment factors for Cu, Zn and Pb (Table 2)show high values and these elements are indicative of an-thropogenic sources, which form very insoluble sulphides andshould therefore be immobile and remain fixed in reducingestuarine sediments.

Index of Geoaccumulation

In order to compare present day heavy metal concentrationwith pre-civilisation background values and for a quantita-tive measure of possible contamination in these sediments,an ‘‘index of geoaccumulation’’ (Igeo) was used (MULLER,1979). This index is defined as:

Igeo 5 log2 Cn/1.5 Bn (2)

Where Cn is the measured concentration of the element (n)in the pelitic sediment fraction and Bn represents the geo-chemical background concentration of element (n)—eithermeasured directly in pre-civilisation sediments or taken fromthe literature (average shale value—TUREKIAN and WEDE-POHL, 1961). A factor of 1.5 is introduced to include possiblevariations of the background values which are attributableto lithologic variations in the sediment.

The index of geoaccumulation compares present day heavymetal concentrations with those from pre-civilisation back-ground values and has been used successfully to determinethe intensity of pollution by heavy metals in various otherlocations (PONS et al., 1988; ERGIN et al., 1991; STOFFERS etal., 1986). Indices of geoaccumulation (Igeo) (Table 3) wouldindicate moderate to extreme contamination of sedimentsfrom Niteroi harbour. Highest values were recorded for Znand Cu, with the former showing higher concentrations in themajority of the samples analyzed. However, Cr, Pb and Nialso show moderate to strong contamination in these sedi-ments. High values for Zn and Cu may suggest the sameanthropogenic source, since both elements are present inpaint materials used in the naval industry. These metals areknown to be adsorbed by organic matter (BODUR and ERGIN,1994) and this area, being very restricted and associated withsewage input, results in high organic matter levels being pre-sent in the sediments.

Bioavailability

Highest protein values were found in samples 1 and 10(59,00 and 52,03 mg g21 respectively and highest lipid con-tents in samples 1, 2 and 8 (6,00 mg g21), 10 and 13 (5,00 mgg21) (Table 4). Analysis were also carried out on samples from

815Concentration of Heavy Metals in Niteroi Harbour

Journal of Coastal Research, Vol. 21, No. 4, 2005

Table 3. Seven Igeo-classes were established based on the numerical valueof the index and the index of geoaccumulation in the sediments of the studyarea.

Igeo Igeo-Class Designation of sediment quality

.54–53–42–31–20–10

6543210

Extremely contaminatedStrongly/extremely contaminatedStrong contaminatedModerately/strong contaminatedModerately contaminatedUncontaminated/moderately contaminatedUncontaminated

Sample Zn Cu Cr Pb Ni

12345

41.32.33.53.7

62.65.566

1.71.41.72.61.7

31.21.91.93.2

21.51.71.72.2

6789

10

63.14.22.52.6

66666

3.81.61.91.62.2

3.12.63.72.23.1

2.71.21.51.51.5

1112131415

4.43.71.81.92.3

663.34.11.9

1.62.71.21.41.3

2.41.51.21.41.9

1.52.00.70.70.7

Table 4. Protein (mg g21), lipid (mg g21), bacterial carbon (mg C cm23),EST activity (mg fluorescein h21 g21) and ETSA (ml O2 h21 g21) at Gua-nabara Bay sediment samples.

SampleProtein(mg g21)

Lipid(mg g21)

BacterialCarbon

(mg C cm23)

EST (mgfluorescein

h21 g21)ETSA

(ml O2 h21 g21)

12345

59.0035.3237.8524.6030.06

6.006.004.004.003.00

1.011.020.921.160.88

1.142.971.632.672.76

2.963.022.993.282.79

6789

10

13.5217.8224.2121.3552.03

4.004.006.003.005.00

0.941.160.070.970.88

3.182.903.142.802.29

2.482.232.002.742.25

1112131415

22.3221.6122.0219.1642.49

3.002.005.003.004.00

1.130.851.201.080.94

2.823.052.123.632.33

3.382.912.792.312.53

Boa Viagem and Itaipu which are close to the study area(BISPO et al., 2001) and on comparison, protein levels werefound to be lower for the area under study. Protein and lipidcontents are considered as a parameter to monitor organicmatter quality, since they are thought to represent mainlybiopolymers and the most degradable molecules (RELEXANS,1996). The highest bacteria biomass was found in sample 13(1.20 mg C cm23), followed by samples 6 and 8 (1.16 mg Ccm23) respectively (Table 4). One gram of sediment, rangingfrom 10–50 mm in particle size, has a superficial area equiv-alent of 3–8 m2 which can contain 109 bacteria (WATLING,1991) and this is equivalent to 12 mg C cm23 (CARLUCCI etal., 1986). The long term occurrence of biomass oscillatingbetween 0.07–1.20 mg C cm23 can be linked to the availabilityof biopolymers in the study area. This facilitated not onlybacteria growth, but also the occurrence of populations withless them 109 cells, because of the action of bacteria preda-tors.

EST activity was highest in samples 14 (3,63 mg fluoresceinh21 g21), 6 (3,18 mg fluorescein h21 g21) and 8 (3,14 mg fluo-rescein h21 g21) and highest ETSA values were found in thesamples 11 (3,38 ml 02 h21g21), 4 (3,28 ml 02 h21g21) and 2(3,02 ml 02 h21g21) (Table 4). Values for EST activity andETSA were significantly higher than those found in the inter-tidal area of Itaipu and Boa Viagem beaches (,1,00 ml 02

h21g21), except for one ETSA, where the highest value wasobtained in summer 1998 at Boa Viagem Beach (7.48 ml 02

h21g21).Dehydrogenases are the major representatives of the oxido-

reductase enzymes and they catalyse the oxidation of sub-strates to produce electrons that can enter the cells ETSA.The determation of the dehydrogenases activity, in the pres-

ence of an artificial electron acceptor (INT: 2-p-iodophenyl-3-p-nitrophenyl-5-phenyl tetrazolium chloride) supply the elec-tron transport system activity (TREVORS, 1984). The dehy-drogenase assay is an effective primary test for assessing thepotential toxicity of metals to soil microbial activity.

EC50 values are defined as the concentration of test com-pound resulting in a 50% reduction in dehydrogenase activity(ROGERS and LI, 1985). EC50 values were obtained from anon-linear least-squares curve fit of individual data sets tothe exponential equation:

Y 5 a [1 2 e2bd] (3)

Were Y is the percentage inhibition observed for a given com-pound concentration, d is the compound concentration, a theasymptotic value represented by 100 percent inhibition andb is the dose dependent rate parameter. EC50 values werecalculated by setting Y equal to 50 and solving equation (3)for d.

The EC50 values for the metal ions Cu, Zn, Ni, and Cr are29, 177, 114 and 216 ppm respectively (ROGERS and LI,1985). The values determined in the studied sites exceededthe EC50 values, for these heavy metals, and it was not ver-ified an inhibition of dehydrogenase activity.

CONCLUSIONS

Sediment deposition in the study area, influenced by navalactivities (Harbour, Marinas and Dockyards) are formed bythe superposition of natural and anthropogenic sources,which makes their composition very variable. This results inpoorly sorted fine fractionated sediments, which are very im-portant for the transport and accumulation of heavy metalsand other pollutants (FORSTNER and SALOMON, 1980; ELLIS

and REVITT, 1982).Concentrations of Cu, Pb, Zn, Ni and Cr are higher than

those found in other coastal areas of the Niteroi municipalityplus in the surrounding soils and rocks. and this may be dueto the naval activities practiced in this area. Normalised con-centrations using enrichment factors and an index of geoac-

816 Baptista Neto et al.

Journal of Coastal Research, Vol. 21, No. 4, 2005

cumulation showed extremely high concentrations and pointstowards evidence for a strong anthropogenic influence in thispolluted area.

The highest values for protein and lipids have an anthro-pogenic origin and bioavailability of the polymers character-ise the higher enzymatic bacterian activities, expressed bythe EST activity and ETSA. The absence of the inhibition ofdehydrogenase activity indicates that the analysed heavymetals are not bioavailable in the EC50 values.

ACKNOWLEDGEMENTS

This research was supported by FAPERJ (Rio de JaneiroState Science foundation) and CNPq, the Department of Ge-ology and Biology from Universidade Federal Fluminense/Ni-teroi and The School of Geography from Queen’s Universityof Belfast/UK.

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