Concentration and Bioavailability of Heavy Metals in Sediments from Niterói Harbour (Guanabara Bay/S.E. Brazil

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

*Laborat6rio de MicrobiologiaMarinha—PPGBM/UFF/Brazil

[email protected]

''Scbool of GeographyThe Queen's University of

Belfast, UKj .mcahster@qub. ac.uk

fifffftn

"Depto de Geologia/IGEO/CCMN

Universidade Federal do Riode Janeiro, Brazil

[email protected]

ABSTRACT I

BAPTISTA NETO, J,A.; CRAPEZ, M,; MCALISTER, J,J., and VILELA, C.G., 2005. Concentration and bioavailabihtyof heavy metals in sediments from Niteroi Harbour iGuanabara Bay/S.E. Brazil). Journal of Coastal Research 2114)811-817. West Palm Beach (Florida), ISSN 0749-0208.

Tbe coastal area of Niteroi is marked by intensive naval activities and bolds one of the countries main naval estates.Tbe harbour and dockyards have been sited in tbe international literature as potential sources and sinks for accu-mulation of beavy metals and bence contaminated sediments. Tbe aim of this paper is to assess tbe concentrationsof heavy metals in Niteroi Harbour and verify their bioavailability by determining tbe catalytic efTects of tbe bacteriausing esterase activity (EST) and electron transport system activity lETSAl. Samples were analysed for Ni, Zn, Pb,Cr and Cu and normalisation procedures were used to assess wbetber tbeir concentrations represent background orcontamination of tbe sediment. Heavy metal concentrations, especially for Cu, Zn and Pb were found to be muchbigber than natural background levels and the index of "geoaccumulation" shows moderate to extreme contamination.However, the absence of tbe inhibition of debydrogenase activity indicated tbat tbe analysed beavy metals are notbioavailable in the EC, ,, 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 (STOFFKRS et al. 1986; SALOMONS andFoRSTNHK, 1984; SUMMERHAYERS et al. 1985; ANGELIDISand ALOUPI, 2000).

Guanabara Bay is considered to be one of the most pollutedenvironments of the Brazilian coastline. Heavy metal con-tamination accounts for a high percentage of this pollution(REHELLO et ai, 1986; VANDENBERG and REBELLO, 1986;LEAL and WAGENKR, 1993; BAITIBTA NETO et ai, 2000), andit is very important to access their main sources. In recentyears, discussions concerning the pollution in Guanabara Baybave considered sewage and litter to be the main sources,however, otber sources of pollution, sucb as dockyards andharbours should also be assessed. Dockyards and harbour ar-eas bave been described in the international literature as typ-ical locations wbere sediment-associated pollutants can ac-cumulate. A study carried out by BELLINGKR and BENHAM(1978) on tbe 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: 10.2U2I012-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 beavy met-al studies in harbours bave 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, bowever, work has been carried out in Fiji (NAIDU

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

Coastal marine sediments are recognized as being impor-tant locations for nutrient regeneration, where bacteria con-stitute tbe primary agents of the early diagenesis of organicmatter. The mineralization of organic matter depends onbotb 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 tbe cells,wbere the oxidation processes are carried out. Oxidation oforganic matter occurs mostly in organisms that present re-

812 Baptista Neto et al.

GuanabaraBay

Niterbi

Rio de Janeirol

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

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-RKIL, 1986).

The aim ofthis 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 diisigned to provide a wide geograph-ic coverage of Niteroi Harbour (Figure 2).

Laboratory Analysis

Samples were stored in sealed polythene bags, transportedto tbe laboratory, air dried at SO-SS C 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 105°C and the <63 (im fractions separated hy pass-ing them through a nylor, mesh sieve. Suh-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 WALKLf:Y and BLACK(1934) technique and particle size analysis was carried outusing wet sieving (2 mm-63 p.m) and pipette analysis (<63.m) techniques (VAN DOESBURG, 1996). Elemental analysis

was 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 ai, 1951) and lipid (EOLCH et a/., 1957) contents werealso determined. The ETSA was measured without a surplusof electron donors.

100%

80%

60%

40%

20%

0%4,00 2,00 1,00 0,50 0.25 0,125 0,062 0,015 0,004 0,001 0,00025

Samplei—Sample2

-Sample3— - •Sample4

Sample5Sample6Sample7

SamplesSample9SamplelOSamplei 1

— - -Samplei?Sample13Sample14SampleiS

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

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

Concentration of Heavy Metals in Niter(5i Harbour 813

1400

1200

?g 1000

N 800

cCD 6003o

400

200

0

V1 ™i—1—

A A XMV\Ani ^ \

--160

140

120 -p-

a100 B

Q.80 -o

cCD

60 ~

40 O

20

01 2 3 4 5 8 7 8 9 10 11 12 13 14 15

samples

Cu (ppm)Zn (ppm)

(ppm)Ni (ppm)

(ppm)

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 hehaviour 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 hy 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, 19781. Figure 3 indicated higher concentrations inthose samples located close to Niteroi harhour (see Figure 1)and the dockyard than those recorded in the internationalliterature (FORSTNER and WITTMANN, 1983; SMITH and OR-

FORD, 1989; SuBRAMANiAN e aZ., 1988).It is difficult to estimate the extent of the anthropogenic

input 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 JurujuhaSound are available (Table 1), Data for heavy metal concen-trations in sediments collected in the hase 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.

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

814

Table 1, Cancentrations of heavy metah in

Location

This study Niteroi Harboui

Jurujuba Sound'

Background'

Soils from Niteroi'

Rock-augen gneias^Piratininga Lagoon^Itaipu Lagoon-'Average Shale *Average sandstone''

Pbfppml

45-12084

5-12361

15-iO24.4

11-1103330472420

7

Baptista Neto et at.

the study area 1 minimum-maximum) (average), compared with values from the literature.

Zn (ppml

115-85029915-337158

212,2-13258,4

41-537945428449516

Cu (ppml

35-14502415-213

516,3-17.5

918-84

412811194510

Cr (ppm)

75-230116

10-22389

30-1940.5

24-1167715——9035

Ni (ppml

30-11063

15-7948

11^927

14-704078——68

2

Fe Ippm)

18500-550026900

1000-2125012573

13750-2975021775

5250-553752858622652

——

470009800

Mn (ppml

105-105160

10-414182

50-200117

7.5-787273354——

85050

Baptiata Neto et al. (19991; ^ B, Sanches, personal communication (1993); •' Knoppers et at. (1989);' Turekian and Wedepohl (1961).

Enrichment Factors

To reduce the effects caused hy grain size and mineralogyin metal variahility and identify possihle anomalous metalcontrihutions, 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 hy providing enrichment fac-tors, (EF) for each metal (ERGIN et al. (1991),

E.F.(me) =I cone . p /cone. p^ )hackgroun d

(1)

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 (Tahle 2)show high values and these elements are indicative of an-thropogenic sources, which form very insoluhle sulphides andshould therefore be immobile and remain fixed in reducingestuarine sediments.

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

Sample

123456789

101112131415

Ni/Fe

2,92.82.61.83.31.71.81.82,31.82.31.71.21.11,3

Cr/Fe

1,11.11.11.21.21.01.01,11,11,21,1LO0.90.91.0

Cu/Fe

13,54.88.0

25.017.366-011.313,812,311.040.526,0

5,35.89,5

Zn/Fe

5.82.33,23,45,35,74,34,93.82.96,63,02,82,73.9

Ph^e

4,82.43,02,15.32.14.04,83,74,04.21,42,12.13,5

Index of Geoaccumulaldon

In order to compare present day heavy metal concentrationwith pre-civilisation background values and for a quantita-tive measure of possihle contamination in these sediments,an "index of geoaccumulation" (Igeo) was used (MULLER,

1979), This index is defined as:

Igeo 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-(;ivi]isation 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 ai, 1988; ERGIN et al, 1991; STOFFKRSefal, 1986), Indices of geoaccumulation (Igeo) (Table 3) wouldindicate moderate to extreme contamination of sedimentsfrom Niteroi harhour. Highest values were recorded for Znand Cu, with the former showing higher concentrations in themajority of the samples analyzed. However, Cr, Ph 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 EK(JIN,1994) and this area, heing very restricted and associated withsewage input, results in high organic matter levels heing pre-sent in the sediments.

Bioavailability

Highest protein values were found in samples 1 and 10(59,00 and 52,03 |jLg g ' respectively and highest lipid con-tents in samples 1, 2 and 8 (6,00 jig g '), 10 and 13 (5,00 \x.gg ') (Table 4J. Analysis were also carried out on samples from

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

Concentration of Heavy Metals in Nit«n3i Harbour 815

Table 3. Set>en Igeo-classes were established based on the numerical valueof the index and the index of geoaccumulation in the sediments of the study

Igeo Igeo-Class Designation of sediment quality

> 54-5Z-A2-31-20-10

Sample

123456789

101112131415

6543210

Zn

41.32.33.53.763.14.22.52.64.43.71.81.92.3

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

Cu

62.65.56666666663.34.11.9

Cr

1.71.41.72.61.73.81.61.91.62.21,62.71.21.41.3

Pb

31.21.91,93.23.12.63.72.23.12.41.51.21.41.9

Ni

21.51.71.72.22.71.21.51.51.51.52.00.70.70.7

Boa Viagem and Itaipu which are close to the study area(Bispo et al, 20011 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 fig C cm ^), followed by samples 6 and 8 (1.16 .g Ccm ) respectively (Table 4i. One gram of sediment, rangingfrom 10-50 jxm in particle size, has a superficial area equiv-alent of 3-8 m^ which can contain 10'' bacteria (WATLING,19911 and this is equivalent to 12 \i.g C cm •'' (CARLUCCI etal, 1986), The long term occurrence of biomass oscillatingbetween 0.07-1,20 \Lg C cm •' can be linked to the availabilityof biopolymers in the study area. This facilitated not onlybacteria growth, but also the occurrence of populations withless them 10 cells, because of the action of bacteria preda-tors.

EST activity was highest in samples 14 (3,63 (i,g fluoresceinh ' g-'), 6 (3,18 (xg fluorescein h " g-') and 8 (3,14 tig fluo-rescein h ' g 'I and highest ETSA values were found in thesamples 11 (3,38 jil 0, h-^g-'K 4 (3,28 [xl 0, h ' g ' ) and 2(3,02 Ll 0 h-ig-M (Table 4), Values for EST activity andETSA were significantly higher than those found in the inter-tidal area of Itaipu and Boa Viagem beaches (<l,00 jjul O2h"'g-'i, except for one ETSA, where the highest value wasobtained in summer 1998 at Boa Viagem Beach (7.48 |xl 0;,h 'g ').

Dehydrogenases are tbe 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 tbe dehydrogenases activity, in the pres-

Tabie 4. Protein (fjg g •>. lipid (fig g •), bacterial earbon (fig C cm 'J,EST activity Ifig fluorescein h ' g-'i and ETSA (/ji 0^ h ' g ') at Gua-ruxbara Bay sediment samples.

ProteinSample

LipidBacterialCarbon

ESTlM.gfluorescein

h ' g 'IETSA

123456789

101112131415

59.0035,3237.8524.6030.0613.5217.8224.2121.3552.0322,3221.6122.0219.1642.49

6.006.004.004,003,004,004.006.003.005.003.002.005.003,004.00

1.011.020.921.160.880,941.160.070.970.881.130.851.201.080.94

1.142.971.632.672.763.182.903.142,802.292.823.052.123.632.33

2.963.022.993.282-792.482.232.002.742.253.382.912.792.312.53

ence of an artificial electron acceptor (INT: 2-p-iodopbenyl-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.

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

Y = a [1 - (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. EC ,, values werecalculated by setting Y equal to 50 and solving equation (3)ford.

The ECso 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 EC ,, 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. Tbis 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; ELLISand REVITT, 1982).

Concentrations of Cu, Pb, Zn, Ni and Cr are higher thanthose 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 tbis area. Normalised con-centrations using enrichment factors and an index of geoac-

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

816 Baptista Neto et al.

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 EC,-,, 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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