benthic foraminifera as proxies of pollution: the case of guanabara bay (brazil)

Marine Pollution Bulletin 64 (2012) 2015–2028

Contents lists available at SciVerse ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier .com/locate /marpolbul

Benthic foraminifera as proxies of pollution: The case of Guanabara Bay (Brazil)

Sandra Donnici a,⇑, Rossana Serandrei-Barbero a, Maurizio Bonardi a, Marcelo Sperle b

a CNR - National Research Council of Italy, ISMAR - Marine Sciences Institute in Venice, Arsenale Tesa 104, Castello 2737F, 30122 Venice, Italyb Institute of Oceanography, Rua São Francisco Xavier 524, S.4018E, Universidade do Estado do Rio de Janeiro, Maracaña, 20550-013 Rio de Janeiro, Brazil

a r t i c l e i n f o

Keywords:Benthic foraminiferaPollutionHeavy metalsGuanabara Bay

0025-326X/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.marpolbul.2012.06.024

⇑ Corresponding author. Tel.: +39 41 2407923; fax:E-mail address: [email protected] (S. Do

a b s t r a c t

Due to economic importance of Guanabara Bay, a multidisciplinary approach was adopted to investigate88 surficial sediment samples in order to use the benthic foraminifera as indicators for the characteriza-tion of environmental variations. Grain-size analyses indicate that bottom sediments of the inner part ofthe bay are mainly muddy while those close to the entrance of the bay are sandy. Geochemical data showhigh concentration of heavy metals mainly in the northern region of the bay. Micropalaeontological anal-yses indicate the boundaries of the areas with the highest concentration of heavy metals. The dominantbenthic foraminifera in the bay are Ammonia beccarii and Buliminella elegantissima, taxa capable of differ-entiating the presence of pollutants of different sources. B. elegantissima, in particular, has shown to be anindicator of anthropogenic pollution. The study highlights the worsening of environmental conditionssince 2000 and those areas of the bay in need of a priority recovery.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The Guanabara Bay, like the majority of the coastal areas aroundthe world, is undergoing an alarming environmental stress due tothe uncontrolled urbanization and industrialization of itscatchment.

Over the past decades, the bay has experienced a multitude ofanthropogenic activities (intense urbanization, industrial, chemi-cal, recreational, agricultural etc.). Their negative environmentalimpact urgently requires an updated and ecologically sustainableplan of management.

Recently several studies have been carried out on the grain size,mineralogy and heavy metal distribution in the surficial sedimentsof Guanabara Bay (Baptista Neto et al., 1999, 2006; Faria de Meloand Sanchez, 2001; Vilela et al., 2004). Baptista Neto et al. (2006)in particular reported a strong correlation between regional distri-bution patterns of heavy metal concentrations and particle sizeand organic carbon content.

The main aims of this study are to provide additional data for abetter understanding of the complexity of the Guanabara Bay eco-system and to identify the areas in ecological critical conditionsdue to a high level of heavy metal contents in order to take properrecovery actions. For this purpose, the foraminifera, unicellular(single-celled) organisms with a shell usually referred as test,which is well preserved in marine sediments, are considered in

ll rights reserved.

+39 41 2407930.nnici).

environmental sciences as the organisms most suitable to behaveas indicators of environmental conditions (Debenay et al., 2001;Armynot du Châtelet et al., 2004; Albani et al., 2007; Eichleret al., 2012).

Following the January 2000 fuel oil spill of about 1300 m3 froma pipeline of a refinery North of the Governador Island (Eichleret al., 2003a), several studies were initiated with the aim ofevaluating the impact on the ecosystem through the comparisonof analytical data of sediments collected before (1999) and after(2000–2001) the oil spill.

Because of the limited mobility of the benthic fauna, directlyaffected by the local environmental conditions and the short vitalcycle of the foraminifera (between 6 and 12 months) (Yankoet al., 1999; Murray, 2006, p. 32) the benthic foraminifera wereconsidered ideal environmental indicators of short and middleterm impact of the oil spill on the ecosystem (Vilela et al., 2003,2004; Eichler et al., 2003b).

Although the effect of each pollutant is not yet very well under-stood (Alve, 1995; Yanko et al., 1999; Morvan et al., 2004; Saraswatet al., 2004), their cumulative impact is particularly evident in thediversity and abundance of the foraminifera assemblages (see,among others, Romano et al., 2008, 2009; Martins et al., 2010).

The percentage of deformed shells, up to 20% of the total fauna,could be related to the presence of pollutants (Yanko et al., 1998;Samir et al., 2000; Martins et al., 2010; Coccioni et al., 2009). Traceelements, hydrocarbons, sewage and low oxygen concentrationwere identified as possible causes of shell deformation (Geslinet al., 2000). However, the boundary between morphological vari-ations within the same species and deformed specimens is not verywell defined and rather bound to subjective interpretation. In fact,

http://dx.doi.org/10.1016/j.marpolbul.2012.06.024

mailto:[email protected]

http://dx.doi.org/10.1016/j.marpolbul.2012.06.024

http://www.sciencedirect.com/science/journal/0025326X

http://www.elsevier.com/locate/marpolbul

7480000

7485000

7490000

T11T36TCC

R2R3

R5R6

R18

R23Test Area

Iguagu River

Saracuruna River

2016 S. Donnici et al. / Marine Pollution Bulletin 64 (2012) 2015–2028

a study carried out in the Biscayne Bay (Florida), shows that theabundance of malformed shells is not always related to the highestconcentrations of trace metals (Carnahan, 2005).

Diversity and abundance were therefore considered in thisstudy as environmental indicators because, in general, they tendto diminish in those areas where the heavy metal concentrationsare high (Cearreta et al., 2002; Debenay et al., 2001; Armynot duChâtelet et al., 2004).

675000 680000 685000 690000 695000 700000 705000

7450000

7455000

7460000

7465000

7470000

7475000

R1

R13

R14

R16

R27R28

R29

R30R31

R32R33R34

R35R36

R38R39

Atlantic Ocean

Rio de Janeiro

GovernadorIsland

sample stationnon-sterile sample stationTest Area sample stationTest Area non-sterile samplestation

Niterói Bridge

Fig. 1. Location map of the study area and locations of samples stations.

2. Environmental setting

The Guanabara Bay is a tropical embayment located in the Riode Janeiro State, Southeast Brazil, within 22�400 and 23�000 S of lat-itude and 43�020 and 43�180 W of longitude (Baptista Neto et al.,2006). It is 28 km E-W wide and 30 km N-S long and covers an areaof about 384 km2 including several islands. It is one of the largestcoastal bays in Brazil.

The bay communicates with the open sea through a narrow en-trance 1.6 km wide. The complex bathymetry presents a 400 mwide central channel that stretches from the mouth, more than5 km into the bay. The channel has an average depth of 30 m withthe deepest point of the bay at �58 m (Kjerfve et al., 1997). The bayis quite shallow with an average depth of 5.7 m for the sectionnorth of the Niteroi Bridge. It is an estuarine environment highlyeutrophic, driven mainly by tidal currents, partially stratified withsurface water supersaturated with oxygen whereas anoxic condi-tions are found in the near-bottom water layer.

The geology of the Guanabara basin is characterized by granitesand gneiss belonging to the Precambrian basement folded duringthe Cenozoic and eroded since then. Guanabara Bay correspondsto a tectonic depression known as Baixada Fluminense and it isaligned with the Cenozoic structural lineations SW-NE characteris-tic of the region. It is characterized by numerous outcrops of Pre-cambrian rocks, as the well known 400-m-high Sugar Loaflocated at the south-west end of the bay, while at the northernedge of Guanabara Bay a Neo-Cenozoic terrigenous nonmarine de-posit (Macacu Formation) outcrops (Kjerfve et al., 2001).

The hydrographic basin is drained by a total of 45 rivers, 6 ofthem responsible for the 85% of the mean annual fresh water dis-charge (Baptista Neto et al., 2006). The bay receives the untreatedagricultural runoffs and the urban and industrial sewage from therivers, from the Rio de Janeiro metropolitan area, from two harbors,from refineries, from the thousands of industries in the surround-ing basin and from the atmospheric fallout (Baptista Neto et al.,2006; Kjerfve et al., 1997).

3. Materials and methods

3.1. Sediment sampling

Surficial sediments samples were collected in 2003 using a Van-Veen grab from 43 sites within the entire bay area (samples R). Inaddition, 45 bottom sediment samples were collected in a 4 km2

test area (samples T) that was chosen for a more detailed investi-gation of possible correlation between foraminifera and sedimentcharacteristics. A total number of 88 samples (Fig. 1) was consid-ered for grain-size, organic matter content, geochemical analyses,and benthic foraminifera analysis.

To avoid metal contamination, the sediment samples 1 cm thickwere taken from the middle of Van-Veen grab, with a plastic spat-ula, subdivided into several fractions for grain-size, geochemical,textural and benthic foraminifera investigations, placed in poly-thene bags and frozen at �5 �C before analysis.

A Global Positioning System (GPS) was used to determine andrecord the position of each sampling site.

3.2. Sediment analyses

After the removal of the organic matter by H2O2 (35%) attack,the proportions of sand, silt and clay were determined by wet siev-ing for the fraction >63 lm, while the fraction <63 lm was ana-lyzed using a FRITSCH photosedigraph, model Analysette 20.

The percentage of organic matter (OM) in the samples was ob-tained by weight difference after calcination.

The concentrations of major (Fe, Al, Ti, Ca, Mg, P and K) andtrace (Mn, Cr, Ni, Cu, Zn, Pb, Cd, As, Ag, Co, Mo, Sn, Ba, Th, Sr, V,La, Zr, Y, Nb, Sc) elements were determined on air-dried samples,digested with HNO3 in PTFE bombs at 120 �C for 9 h. The digestedmaterial was then analyzed by the ICP-ES (Inductively CoupledPlasma-Emission Spectrometry). International reference sampleswere used to check the accuracy and precision of the analyses.

3.3. Micropaleontological analysis

A total of 88 samples has been prepared for micropaleontolog-ical investigations.

All samples were weighted and washed through a sieve with asquare grid of 63 lm of net aperture in order to remove the silt andclay fraction of the sediment. They were air dried before dry siev-ing. In order to concentrate foraminiferal tests from sandy samples,residues were repeatedly floated in CCl4 (Carbon tetrachloride).

The foraminifera assemblage representative of a certain tempo-ral interval must contain all the fauna variations caused by thevariations of the physical–chemical parameters that occur duringthat given temporal interval. Because any change of the biotic orabiotic parameters modifies the foraminifera assemblage composi-tion (Scott and Medioli, 1980; Culver and Buzas, 1995), the totalassociation of all foraminifera, dead and alive, must be analyzed

S. Donnici et al. / Marine Pollution Bulletin 64 (2012) 2015–2028 2017

in order to cover the productivity peaks and the seasonal variationsas indicated by Scott and Medioli (1980) and Hallock et al. (2003).

In previous papers on Guanabara Bay, Eichler et al. (2003b) andVilela et al. (2004) analyzed the foraminifera alive and dead sepa-rately. During the analysis, however, they added the two fractions(dead and alive organisms) in order to balance for the seasonalblooming.

The total assemblage analyzed in this study, resulting from thesum of different living assemblages due to changes such as sea-sonal variations, indicates the environmental evolution and in par-ticular the relationship with the geochemical data which are notaffected by seasonal variations. More than 100 counts per sampleare needed in order to obtain the minimum standard deviation va-lue (Buzas, 1990; Serandrei-Barbero et al., 1997). However, in pol-luted environments, a sub-sample of 100 individual elements isconsidered sufficient for the statistical interpretation (Martins

7450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

675000 680000 685000 690000 695000 700000 705000

% Silt plus Clay

0

5

10

20

30

40

50

60

70

80

90

95

7450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

675000 680000 685000 690

Fig. 2. Map of spatial distribution of silt + clay

et al., 2010). A total of 100 individuals per sample (or all thosepresent in the sample if they numbered less than 100) was consid-ered to be representative of the sample analyzed and allowed acomparison with data previously obtained for the Guanabara Bayusing the same total value (Vilela et al., 2003, 2004). Foraminiferawere classified according to the taxonomic order of Loeblich andTappan (1987).

3.4. Statistical analyses

In order to quantify the taxonomical diversity in the samples,the diversity indices were determined by means of the paleonto-logic statistical software PAST version 2.10 (Hammer et al., 2001).

Detrended correspondence analysis was also applied to thematrices using the software PAST. This type of multivariate statis-tical analysis is the most suitable way of treating enumerative data

7450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

675000 680000 685000 690000 695000 700000 705000

% Sand

0

5

10

20

30

40

50

60

70

80

90

95

000 695000 700000 705000

% Organic Matter

0

2.5

5

7.5

10

12.5

15

17.5

20

22.5

25

, sand and of organic matter percentages.


in which the number of variables (species) is greater than the num-ber of observations (samples), without any a priori reduction inspecies number.

Correlation between foraminifera percentages, heavy metals(HM) content, sand and clay percentages, Organic Matter (OM)content and diversity statistical indexes were calculated usingthe Pearson’s correlation coefficient r, which varies between +1and �1 and yields a measure of the strength of the linear relationbetween two variables. For this dataset, r values equal to or greaterthan |0.397| are significant with 95% probability.

The Kriging algorithm was applied to elaborate the contourmaps of grain size, organic matter, mayor and trace elements,and foraminiferal content.

4. Results

4.1. Sediment characteristics

Grain-size analysis indicates that silt is the prevailing texturaltype of the bottom sediments in the Guanabara Bay, whereas sand,silty sand and sandy silt are subordinate. In the northern andinnermost sector of the bay, bottom is characterized by fine sedi-ments: poorly sorted silt is almost always present at the bottom.Silty sediments are also present in the central area of the bay. Sandsediments are found near the entrance of the bay and along thecentral channel. Areas with relict sands and submerged sand banksare also present in the bay.

The highest level (16.6) of OM occurs in the north-western partof the bay while the lowest level (0.3) is found at the entrance and

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0102030405060708090100

Cu ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

50

100

150

200

250

300

325

400

Zn ppm

Fig. 3. Map of spatial distribu

in the central part of the bay. Areal variations in the bay of organicmatter, sand and mud (silt plus clay) are reported in Fig. 2.

4.2. Geochemical content

Areal distribution of heavy metal in the Guanabara Bay bottomsediments is in general related to the grain size which in turn is re-lated to the hydrodynamics of the bay. Anthropogenic activitieshave also influenced the concentration of the heavy metal, as rec-ognized in the area adjacent to the harbor of Rio de Janeiro and inthe north-western area of the bay where the untreated city sew-age, the oil refinery and the polluted sediment discharge of severalrivers have had a negative environmental impact.

Low concentration of heavy metals is found in the area near theentrance of the bay.

The highest concentrations of Cu, Cr, Zn, and Ti were found inthe north-western part of the bay, near the mouths of Iguaçu andSaracuruna rivers (Fig. 3). Al, Mg, Fe, Ni reach the greatest valuesalong the central and eastern areas of the northern GuanabaraBay (Fig. 4). The distribution of these elements follows those of fineparticles deposited by rivers into the bay. Among these Al, Mg andFe come from ferromagnesian aluminum silicates and are of litho-genetic origin. Cu, Zn, Ni and Cr show higher concentrations inlocations close to the dockyard, generally characterized by low cir-culation of sediments and high anthropogenic activities such asantifouling coating and general ship painting. Cu and Zn are oftenassociated with sewage contamination.

Mn, Cd, Pb and Ag reach their maximum values in the centralGuanabara Bay (Fig. 5), with a very high level for Pb in R1, near

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

020406080100120140160180200220

Cr ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Ti %

tion of Cu, Cr, Zn and Ti.

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

2

4

6

7

8

9

10

Al %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

4

10

15

20

25

27.5

30

35

40

Ni ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

11.522.533.544.555.56

Fe %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

Mg %

Fig. 4. Map of spatial distribution of Al, Fe, Mg and Ni.


the terminal of an oil refinery, where Pb reaches 1391 ppm, an or-der of magnitude higher than the other stations. High levels of Pbdue to the combustion in cars of leaded gasoline are also foundnear the Niteroi Bridge.

Ca and Sr prevail at the bay inlet and are linked to the distribu-tion of coarse sediments (Fig. 5). Concentrations of major and min-or elements are summarized in Table 1.

4.3. Benthic foraminifera

Foraminifera were not found in 54 of the 88 total samples ana-lyzed, and nine samples contain very few benthic foraminiferatests, too scarce to perform statistical analyses, with a numberper gram of foraminifera specimens of sediment between 0.04and 0.4. The remaining 25 samples contained crushed molluscshells mixed with benthic foraminifer tests. The test area samplescontain also gypsum, vegetal remains, siliceous diatom frustules,ocraceus silty agglomerates.

In the 25 samples containing benthic fauna (Fig. 1), a total of 68taxa were found, with a minimum of 4 and a maximum of 31 taxaper sample (Tables 2 and 3). Number of taxa (S), total number ofindividuals (n), Shannon index (H) and Fisher’s alpha (a) weredetermined for each sample (Table 3). Samples from the most inte-rior area show low diversity indexes whereas samples with highervalues are found in the southern area and relate respectively to la-goonal brackish environments and to normal marine environments(Murray, 2006, p.20).

On average, fauna accounted for 14 taxa per sample. Eight taxaare present in more than 50% of the 25 sites: Brizalina spathulata

(Williamson, 1858), Bulimina gibba Fornasini, 1902, Bulimina mar-ginata d’Orbigny, 1826, Buliminella elegantissima d’Orbigny, 1839,Nonion politum (d’Orbigny, 1826), Ammonia beccarii (Linnè, 1758)(=A. beccarii + A. beccarii var. tepida Cushman, 1926), Cribrononiongranosum (d’Orbigny, 1846) (=Elphidium gunteri Cole, 1931) andCribrononion translucens (Natland, 1938).

Among these taxa, A. beccarii has mean content around 45% andis present in all 25 non sterile stations; the mean content of B. ele-gantissima is around 18%, and the other six species are comprisebetween 3% and 5%. The spatial distribution of the taxa (Fig. 6) isindicative of an estuarine environment.

4.4. Statistical analysis

Distribution of samples characterized by similar association offoraminifera was obtained using data from 25 non-sterile samplesfrom the Guanabara Bay (22 samples) and test area (3 samples).Detrended Correspondence Analysis on the counted species in eachsample identified groups of similar samples represented by neigh-boring dots. The first three transformations from CorrespondenceAnalysis explained respectively for 22%, 13% and 10% of total vari-ability. C-means Cluster Analysis was applied to these three com-ponents to better define groups of samples with similarforaminifera associations. Samples are plotted in different posi-tions on the diagram and they are grouped in five clusters (Fig. 7).

The five clusters fall along axis 1 on the basis of residence timewhich is higher for the samples located in the inner part of the bay.Samples of Cluster 1 have few species (average 11) and high con-tents of B. elegantissima (22–54%) and of genera Bulimina, Bolivina,

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

50

75

100

200

500

750

1000

1125

Pb ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0.2

1

1.5

2

3

4

6

8

Ag ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

100

120

140

160

180

200

300

Sr ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

0.5

1

1.5

2

3

4

6

Ca %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

200

400

600

800

1000

1200

1400

Mn ppm

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0

0.2

0.4

0.6

0.8

1

1.2

1.4

Cd ppm

Fig. 5. Map of spatial distribution of Pb, Ag, Mn, Cd, Ca and Sr.


Brizalina. The samples of Cluster 3 also have a high content ofBuliminella (lower than Cluster 1) together with Bulimina and Epis-tominella vitrea and a number of species between 15 and 20. InCluster 3, the selective characters of Cluster 1 appear mitigated,being close to the bay mouth.

In Cluster 4, the dominant species is A. beccarii (>40%) togetherwith other typical lagoonal taxa. Within Cluster 4, sample R23shows high content (29%) of C. granosum if compared to the othersamples.

The two samples of Cluster 2 contain Quinqueloculina seminulmassociated with other taxa like Cribrononion venetum and Elphidiumdepressulum, indicative of a lagoon environment with a good ex-change with sea water.

Samples of Cluster 5 are characterized by a high content ofMiliolids and a high number of species (ca. 30), indicative ofthe vicinity of the sea entrance. They are species that live onthe continental shelf, like Textularia, Neoconorbina, Cibicidella,Buccella.

Table 1Average (±std), minimum, maximum values for the geochemical data obtained for surficial sediments of Guanabara Bay.

Fe Ca P Mg Ti Al Na K Mo Cu% % % % % % % % ppm ppm

Test area samples Average 4.35 0.80 0.19 1.31 0.46 6.67 3.52 0.98 4 66Min 3.72 0.39 0.12 0.65 0.36 5.38 2.14 0.74 2 45Max 5.41 1.35 0.44 1.71 0.67 8.42 6.33 1.20 7 101St dev 0.33 0.24 0.05 0.24 0.06 0.63 0.97 0.12 1 10

Regional area samples Average 3.64 1.27 0.11 1.09 0.41 6.53 2.26 1.35 4 43Min 0.56 0.30 0.01 0.11 0.12 1.37 0.48 0.70 2 4Max 5.90 6.91 0.22 1.72 0.71 9.87 4.15 1.95 13 112St dev 1.35 1.03 0.04 0.43 0.11 2.18 0.88 0.34 3 23

Total area samples Average 4.00 1.03 0.15 1.21 0.43 6.60 2.90 1.16 4 55Min 0.56 0.30 0.01 0.11 0.12 1.37 0.48 0.70 2 4Max 5.90 6.91 0.44 1.72 0.71 9.87 6.33 1.95 13 112St dev 1.03 0.77 0.06 0.36 0.09 1.58 1.12 0.31 2 21

Pb Zn Ag Ni Co Mn As Th Sr Cdppm ppm ppm ppm ppm ppm ppm ppm ppm ppm

Test area samples Average 68 261 1.7 27 7 748 10 8 90 0.5Min 42 169 0.7 20 4 368 2 5 62 0.2Max 92 335 2.5 35 9 1577 20 11 148 1.1St dev 11 35 0.4 3 1 247 4 2 18 0.3

Regional area samples Average 128 190 1.7 24 8 601 14 13 137 0.6Min 43 11 0.2 5 2 82 2 4 61 0.2Max 1391 394 8.6 39 11 1265 23 28 537 1.4St dev 204 81 1.4 8 3 343 6 5 71 0.3

Total area samples Average 97 226 1.7 25 8 676 12 10 113 0.6Min 42 11 0.2 5 2 82 2 4 61 0.2Max 1391 394 8.6 39 11 1577 23 28 537 1.4St dev 145 71 1.0 6 2 305 5 4 56 0.3

V La Cr Ba Zr Sn Y Nb Be Scppm ppm ppm ppm ppm ppm ppm ppm ppm ppm

Test area samples Average 78 19 156 176 53 6 8 22 1.9 8Min 51 12 89 142 44 2 5 14 1.0 6Max 91 35 258 256 70 10 14 38 3.0 11St dev 7 5 41 23 6 2 2 6 0.3 1

Regional area samples Average 64 38 80 269 48 5 13 15 1.9 9Min 7 15 3 159 19 2 4 5 1.0 1Max 92 86 253 436 80 11 26 48 3.0 14St dev 22 14 54 65 11 2 5 8 0.7 3

Total area samples Average 71 28 119 222 51 5 11 19 1.9 9Min 7 12 3 142 19 2 4 5 1.0 1Max 92 86 258 436 80 11 26 48 3.0 14St dev 18 14 61 67 9 2 4 8 0.5 3


Table 4 and Fig. 8 illustrate the cluster composition and distri-bution.

4.5. Correlation between foraminifera, heavy metals andenvironmental characteristics

A. beccarii is the prevailing species in all clusters and shows thehighest values in Cluster 4. It correlates positively with some tracemetals like Ni, Mn, Be, Fe, Al and Na and with the mud and organicmatter contents, and negatively with the number of taxa and theFisher a index (Table 5).

B. elegantissima is present in all clusters except for Cluster 5 andshows the highest values in Clusters 1 and 3. As for the otherBuliminidae, (Bulimina, Brizalina and Bolivina), it has a positivecorrelation with mud content and with most of the heavy metalssuch as Cu, Zn, Pb, Ag and Cd (Table 5).

Textularia agglutinans, Quinqueloculina seminulum, C. translucensand venetum are the major taxa in Clusters 2 and 5, both located atthe entrance of the bay. They have a negative correlation with Cu,Zn, Ni, Co, V, Cr, Zr, Sc, Fe, Mg, Al and with mud and organic mattercontent and a positive correlation with sand content in the sedi-ment. Moreover, Q. seminulum and C. translucens correlate posi-tively with the number of taxa S present in the sample and withthe a index of Fisher, which is a measure of species abundance. Dis-corbis mirus, Rosalina globularis and Nonionella auris show correla-

tions very similar to the above mentioned Q. seminulum-T.agglutinans group (Table 5) but with a positive correlation withSr and Ca.

5. Discussion

In the northern part of the Guanabara Bay, characterized by lowhydrodynamic energy, bottom sediments are mainly mud and clay.The southern sector of the bay, where the hydrodynamic action isintense being affected by waves and by tidal currents, shows coar-ser grain-size in bottom sediments along the central channel. Asexpected, grain-size distribution is closely related to the bottommorphology, to the hydrodynamic characteristics and to the shore-line contour of the Guanabara Bay estuarine system.

The highest values of organic matter are found in the north-western area of the bay where water circulation is low and a greatamount of untreated sewage discharges is present. In addition,intensive sunlight and high temperature throughout the year favorthe high productivity of the area (Rebello et al., 1988). According toBaptista Neto et al. (2006), the highest values of organic mattercorrespond to the highest values of heavy metals (Fig. 2), as the or-ganic matter is a geochemical carrier of metals due to its capacityof absorbing metals of both terrestrial and marine origins(Salomons and Forstner, 1984; Warren and Haack, 2001).

Table 2Foraminiferal taxa in 25 samples of Guanabara Bay surficial sediments: percent average, maximum and minimum content per taxon, number of samples in which the taxon ispresent. Taxa follow the taxonomic order of Loeblich and Tappan (1987).

Taxa Average Max Min N

Acostata mariae (Acosta, 1940) 4.59 8.7 0.55 8Haplophragmoides canariensis (d’Orbigny, 1839) 3.81 3.81 3.81 1Ammobaculites agglutinans (d’Orbigny, 1846) 1.9 1.9 1.9 1Trochammina inflata (Montagu, 1808) 1.74 4.81 0.81 7Atlantiella atlantica (F.L. Parker, 1952) 6.9 6.9 6.9 1Gaudryina silvestrii (Bronniman, Whittaker and Valleri, 1992) 4.28 10.34 0.96 8Textularia agglutinans (d’Orbigny, 1839) 11.03 32.12 0.43 3Textularia conica (d’Orbigny, 1839) 3.03 3.03 3.03 1Spirillina vivipara (Ehremberg, 1843) 0.86 0.86 0.86 1Spiroloculina excavata (d’Orbigny, 1846) 0.43 0.43 0.43 1Massilina disciformis (Williamson, 1858) 0.52 0.61 0.43 2Quinqueloculina agglutinata (Cushman, 1917) 0.43 0.43 0.43 1Quinqueloculina bicornis (Walker and Jacob, 1798) 0.43 0.43 0.43 1Quinqueloculina candeiana (d’Orbigny, 1839) 0.61 0.61 0.61 1Quinqueloculina laevigata (d’Orbigny, 1826) 1.21 1.21 1.21 1Quinqueloculina seminulum (Linnè, 1758) 6.98 15.76 2.88 5Quinqueloculina undulata (d’Orbigny, 1826) 0.61 0.61 0.61 1Miliolinella subrotunda (Montagu, 1803) 1.64 2.42 0.86 2Pyrgo oblonga (d’Orbigny, 1839) 0.61 0.61 0.61 1Triloculina trigonula (Lamarck, 1804) 1.29 1.29 1.29 1Amphicorina scalaris (Batsch, 1791) 2.38 2.38 2.38 1Lagena clavata (d’Orbigny, 1846) 0.55 0.55 0.55 1Lagena laevis (Montagu, 1803) 0.68 0.81 0.55 2Lagena striata (d’Orbigny, 1839) 2.42 2.42 2.42 1Guttulina problema (d’Orbigny, 1826) 0.95 0.95 0.95 1Oolina exagona (Williamson, 1858) 0.61 0.61 0.61 1Fissurina laevigata (Reuss, 1850) 1.29 2.17 0.55 5Fissurina lucida (Williamson, 1848) 1.33 2.73 0.58 6Bolivina laevigata (Williamson, 1858) 3.23 9.26 0.95 8Bolivina psudoplicata (Heron-Allen and Earland, 1930) 0.75 0.93 0.58 2Brizalina spathulata (Williamson, 1858) 2.85 5.83 0.61 13Brizalina striatula (Cushman, 1922) 3.94 11.11 0.55 10Cassidulina laevigata (d’Orbigny, 1826) 0.99 1.02 0.95 2Globocassidulina subglobosa (Bradyi, 1881) 6.03 6.03 6.03 1Bulimina elongata (d’Obigny, 1846) 2.98 10.19 0.91 10Bulimina gibba (Fornasini, 1902) (=B. elegans d’Orbigny, 1826) 3.16 6.9 0.61 20Bulimina marginata (d’Orbigny, 1826) 5.04 11.9 0.81 18Buliminella elegantissima (d’Orbigny, 1839) 17.57 54.1 0.86 23Uvigerina peregrina (Cushman, 1923) 1.02 1.41 0.61 7Trifarina angulosa (Williamson, 1858) 2.19 3.57 0.81 2Valvulineria perlucida (Heron-Allen & Earland, 1913) 3.49 15 0.55 7Eponides repandus (Fichtel and Moll, 1798) 3.06 4.31 1.82 2Poroeponides lateralis (Terquem, 1878) 2.2 2.59 1.82 2Discorbis mirus (Cushman, 1922) 3 6.03 0.93 10Neoconorbina terquemi (Rzehak, 1888) 0.71 0.81 0.61 2Rosalina bradyi (Cushman, 1915) 0.7 0.86 0.55 2Rosalina candeiana (d’Orbigny, 1839) 0.65 0.86 0.43 2Rosalina globularis (d’Orbigny, 1826) 3.15 3.88 2.42 2Epistominella vitrea (Parker, 1953) 4.38 21.43 0.86 12Discorbinella bertheloti (d’Orbigny, 1839) 3.27 7.76 0.86 3Cibicides lobatulus (Walker & Jacob, 1798) 1.29 1.29 1.29 1Cibicides pachydermus (Rzehak, 1886) 3.28 6.52 0.61 8Cibicidella variabilis (d’Orbigny, 1826) 1.21 1.21 1.21 1Asterigerinerata sp. 13.1 13.1 13.1 1Haynesina paucilocula (Cushman, 1944) 2.5 15 0.43 12Nonion politum (d’Orbigny, 1826) syn. N. citai (di Napoli) 3.48 17.39 0.58 14Nonionella auris (d’Orbigny, 1839) 4.59 10.34 1.61 6Nonionella opima (Cushman, 1947) 1.42 3.85 0.43 7Buccella frigida granulata (Di Napoli Alliata, 1952) 1.14 1.29 0.96 4Buccella pustulosa (Albani e Serandrei Barbero, 1982) 0.73 0.86 0.61 2Ammonia beccarii (Linnè, 1758) 45.38 96.43 6.12 25Cribrononion advenum (Cushman, 1922) 3.61 3.88 3.33 2Cribrononion granosum (d’Orbigny, 1846) 4.17 29.52 0.86 13Cribrononion simplex (Cushman, 1933) 1.95 3.81 0.58 5Cribrononion translucens (Natland, 1938) 3.83 11.96 1.09 14Cribrononion venetum (Albani, Favero, Serandrei Barbero, 1991) 5.55 14.52 1.09 4Elphidium depressulum (Cushman, 1933) 2.04 6.8 0.43 11Elphidium discoidale multiloculum (Cushman e Ellisor, 1945) 2.42 2.42 2.42 1


To compensate for grain size and mineralogy effects on traceelement concentrations and to evaluate contamination in the sed-iment samples with respect to regional values, normalization pro-

cedure to a reference element and enrichment factor (EF)determination (the ratio between normalized and baseline value)are usually performed. As in previous work on Guanabara Bay

Table 3Diversity indexes of total foraminiferal assemblage in the 25 non-sterile samples.

Sample R1 R2 R3 R5 R6 R13 R14 R16 R18 R23 R27 R28 R29

Taxa_S 11 11 6 13 6 14 20 8 7 8 28 21 31Individuals 108 114 70 173 28 90 105 110 76 105 165 115 232Shannon_H 1.69 1.43 0.53 1.22 1.28 1.58 2.18 0.95 0.97 1.18 2.32 2.59 2.82Fisher_alpha 3.06 3.00 1.57 3.26 2.34 4.64 7.33 1.98 1.88 2.01 9.68 7.53 9.61

R30 R31 R32 R33 R34 R35 R36 R38 R39 T11 T36 TCC

Taxa_S 19 16 24 16 15 20 12 20 11 4 8 8Individuals 103 92 116 103 84 98 71 183 103 20 58 23Shannon_H 2.33 2.27 2.52 2.01 2.06 2.39 1.82 1.45 1.22 1.00 1.73 1.41Fisher_alpha 6.85 5.60 9.19 5.30 5.32 7.6 4.14 5.72 3.12 1.50 2.51 4.35

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

6

20

40

60

80

A. beccarii %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0.8

10

20

30

40

50

B. elegantissima %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

2

4

8

12

Q. seminulum %

675000 685000 695000 7050007450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

0.4

5

10

20

30

T. agglutinans %

Fig. 6. Map of spatial distribution of relative frequency of Ammonia beccarii, Buliminella elegantissima, Quinqueloculina seminulum and Textularia agglutinans.


(Baptista Neto et al., 2005), also for the samples of this study the EFvalues have been normalized with respect to Fe (Covelli, 2007). TheEF provided a useful assessment of the distribution of anthropo-genic sediment pollution, confirming the high values in thenorth-western areas, just north of Governador Island, and moregenerally in front of local industrial and urban sources. Even inthe presence of high values of EF, however, only a part of metalmay actually be bioavailable and thus threaten marine organisms.

Although the bio-availability of heavy metals in the GuanabaraBay is generally low (Perin et al., 1997), the distribution of benthicforaminifera is affected because the majority of the taxa shows anegative correlation with the heavy metal content. In fact heavymetals, although essential for enzyme activities, in high concentra-tions hinder the growth of organisms by preventing the formationof enzymes (Kennish, 1992).

Along the coasts of the northern sector of the bay, the bottomsediments do not contain foraminifera. In these areas anthropo-genic discharges from the highly urbanized surrounding area arepresent and the concentrations of Cu, Cr, Zn are very high. Zn, inparticular, together with Cd and Pb, is related to pollution due totraffic of vehicles.

In the more interior sectors of the bay (Fig. 8), Clusters 4 and 1are characterized by A. beccarii and B. elegantissima, respectively.

A. beccarii correlates positively with some heavy metals like Fe,Mn and Ni (Table 5), which in small amounts are essential to per-form biological functions. In particular Ni is essential to the growthof the diatoms and the dinoflagellates (Munsel et al., 2010) onwhich A. beccarii feeds. In fact, in the nearby Ubatuba Bay, A. bec-carii is correlated to the chlorophyll (Burone et al., 2007), as alsoobserved in the Lagoon of Venice (Donnici et al., 1997). In general

detrended correspondence analysis

R39R23

3.5

R6R16

R28R3

3

R1R2 R5

R16R18

R3

R13 R30

T11

TCCR27

2.5

R2

R36R38

T36 R31R33

TCC R291.5

2

Axi

s 2

cluster 1

R14 R32

R33

R34

cluster 2

R14R35

1cluster 3

0.5 cluster 4

cluster 5

-0.5

0

-1 0 1 2 3 4 5

Axis 1

Fig. 7. Output of Detrended Correspondence Analysis: plot of first two lineartransformations. Samples are grouped in 5 cluster distributed along axis 1according to residence time.


this species has an opportunistic behavior and a high potential tosurvive with high input of nutrients and trace metal concentrations(Nikulina et al., 2008). It can survive even in environments withhigh physico-chemical variations and occasional high concentra-tion of Cu, as already observed in the Guanabara Bay (Perin et al.,1997), without reporting any deformities of the shell (de Nooijeret al., 2007). In the samples of Cluster 4, A. beccarii is the dominanttaxon as a consequence of the environmental stress and reducedsalinity (intermediate between normal marine and brackish condi-tions) in the inner part of Guanabara Bay. Also the high content ofC. granosum in Cluster 4 (29% in site R23) is interpreted as due tothe nearby fluvial discharge, as this taxon can tolerate very low lev-els of salinity (Donnici and Serandrei-Barbero, 2005; Murray, 2006,p. 78).

Maximum abundance values for B. elegantissima are found insamples of Cluster 1 located in the central area of the bay, east ofthe Governador Island, where the concentration of Pb reaches itsmaximum value. B. elegantissima is an infaunal species of estuarine,lagoonal and continental shelf environments. It is common in pol-luted areas (Bandy et al., 1964a,b; Stott et al., 1996) and also inareas close to hydrocarbon seeps (Bernhard and Bowser, 1999).According to the above, B. elegantissima is very abundant in siteR35 which is located close to an oil refinery, whose facing area is

Table 4Sample composition, mean abundance of main taxa and diversity (expressed as number o

Cluster Samples Representative foraminifera

Main taxa

1 R1, R2, 5R, R6, R16, R18, R36, R38, T36 Ammonia beccariiBuliminella elegantissimaBulimina gen.Bolivina levigata?

2 R18, R39 Ammonia beccariiCribrononion venetumQuinqueloculina seminulumElphidium depressulum

3 R14, R31, R32, R33, R34, R35 Ammonia beccariiBuliminella elegantissimaBulimina gen.Brizalina gen.

4 3R, R13, R23, R30, T11, TCC Ammonia beccariiBuliminella elegantissima

5 R27, R29 Ammonia beccariiTextularia agglutinansQuinqueloculina seminulumNonionella aurisCribrononion translucens

characterized by a high content of Polycyclic Aromatic Hydrocar-bons (Mao, 2007) and Hg (Covelli et al., 2012).

In general, the Buliminidae (Bulimina, Buliminella, Brizalina andBolivina) are typical of coastal zones with muddy sediments suchas along the mud belt of the western Adriatic Sea (Jorissen, 1987;Donnici and Serandrei-Barbero, 2002). In these anoxic environ-ments with a high content of organic matter as in the GuanabaraBay (Pereira et al., 2006; Sobrinho da Silva et al., 2008), the Buli-minidae modify their habitat from epifaunal to infaunal accordingto the oxygen content.

As shown by the geochemical speciation of metals in order toevaluate their biodisponibility (Mao, 2007), Zn and Cd are the mostbioavailable metals in the sediments of Guanabara Bay. Here, theBuliminidae show a positive correlation with Zn, whose metal ionsare essential for biological systems. In addition, the Buliminidaehave a positive correlation with metals ‘‘non-essential’’, such asCd, Pb and Ag (Table 5), suggesting that they can withstand themost polluting elements.

In the southern sector of the bay, toward the sea inlet, theforaminifera assemblages of Clusters 3, 2 and 5 (Fig. 8), more di-rectly connected to the sea, show a progressively increase of diver-sity index values, varying from brackish lagoon to normal marine(Murray, 2006, p. 18).

In the sediment samples of Cluster 3 the foraminiferal assem-blage is similar to the one in Cluster 1. A. beccarii + B. elegantissima,however, represent only 45% of the total compared to the 80% inCluster 1. The taxa number S is 18 compared to 11 in Cluster 1.

Along the western section of the bay, the increased effect ofmarine water dilution can be observed in samples of Cluster 2. Inthis foraminiferal assemblage, stress-tolerant species typical ofestuarine environments such as A. beccarii are associated with taxaof hypersaline and normal marine coastal environments (Murray,1991) like Quinqueloculina which badly tolerates high heavy metalcontents (Ferraro et al., 2006).

Finally, samples of Cluster 5 (Fig. 8) located near the entrance ofthe bay contain the highest number of taxa (30) due to the pres-ence of a great number of continental shelf species. Cluster 5 showsa positive correlation with Sr and Ca, elements that are found in theabundant carbonate bioclasts of the bottom sands. T. agglutinansand Q. seminulum, characterizing Cluster 5, show a negative corre-lation with heavy metals. The latter are scarce in Cluster 5 because

f taxa) of the 5 clusters.

Mean abundance (%) Other taxa >2% Total number of taxa S

51 11 (6–9)2911

4

47 Buliminella elegantissimaBulimina gibbaCribrononion translucensBrizalina spathulata

16 (11–21)10

75

27 Epistominella vitreaNonion politumCribrononion translucensDiscorbis mirus

18 (15–24)1811

8

62 Bulimina gibba 10 (4–19)5

21 Rosalina globularisDiscorbis mirusBulimina gibbaEponides repandus

29 (28–31)16

966

2

3

54

4

1R1

R2R3

R5R6

R13

R14

R16

R18

R23

R27R28

R29

R30R31

R32R33R34

R35R36

R38R39

T11T36TC

675000 680000 685000 690000 695000 700000 705000

7450000

7455000

7460000

7465000

7470000

7475000

7480000

7485000

7490000

Fig. 8. Spatial distribution of foraminiferal clusters in Guanabara Bay according to the content of different taxa.


they tend to accumulate into the mud fraction here removed by themarine currents.

A. beccarii and B. elegantissima are dominant species in theGuanabara Bay and correlate positively with the high mud content.The latter is becoming a factor of environmental stress due to itshigh deposition rate inside of the bay, as a result of the channeli-zation of the rivers and deforestation of the basin (Kjerfve et al.,1997). However, the positive correlation of A. beccarii and B. elegan-tissima with different chemical elements indicates that these twotaxa can be used to differentiate areas under environmental stressof different origin: natural origin for A. beccarii, which tolerateshigh index of confinement (=index of environmental stress, accord-ing to Murray, 2006, p. 20) and is well correlated to mud and tomainly lithogenic elements; anthropogenic origin for B. elegantiss-ima, which correlates positively with the majority of the heavymetals (Table 5).

Because the heavy metals concentrate preferably in the mudfraction of the sediments (Siegel, 2002), it becomes difficult to dis-tinguish if the foraminiferal assemblages are more influenced bythe content of heavy metals or rather by the textural characteris-tics of the sediments (Debenay et al., 2001): the presence of areaswith sterile sediments seems to be mostly relevant for the moni-toring of Guanabara Bay.

The Guanabara Bay is a marine ecosystem with high productiv-ity due to heavy untreated urban and agricultural discharges, highwater temperature and long daily solar illumination (Carreira et al.,2002; Baptista Neto et al., 2006). The lack of foraminifera in certainareas of the bay becomes therefore significant.

The colonization of a marine area depends on several factors:the length of the life cycle of the colonizing organisms is certainlythe most important factor (Boesch and Rabalais, 1991). For theforaminifera, the time required for the colonization of low energyenvironments varies from few months (Debenay et al., 2009; Rath-burn et al., 2008) to few years (Alve, 1999). Although in environ-ments affected by human activities colonization could require alonger time (Stachowitsch, 1991; Serandrei-Barbero et al., 2011),in the Guanabara Bay the absence of foraminifera in the test areaand the great number of sterile samples found even outside ofthe test area indicate that the pollution effects are still active andprevent the colonization of the interior areas of the bay.

Hydrodynamic investigations of Guanabara Bay using a numer-ical model showed that the water residence time in the bay is al-ways high comprised between 15 and 50 days, depending on thetide and different wind scenarios (Cucco, 2007). This high resi-dence time and the high productivity lead to anoxic conditionswhich, along with the high content of heavy metals, may explain

Table 5Pearson’s correlation coefficient r among representative foraminiferal taxa, sediment characteristics and heavy metals.

%Sand

%Fine

Organicmatter

TaxaS

Fisheralpha

Mo Cu Pb Zn Ag Ni Co Mn As Th Sr Cd

Ammonia beccarii (Linnè, 1758) 0.41 �0.73 �0.76 0.42 0.52Buliminella elegantissima

(d’Orbigny, 1839)0.40 0.49 0.52 0.59 0.40 0.54 0.52 0.49

Bulimina elongata (d’Obigny,1846)

0.43 0.87 0.44 0.87 0.41 0.43 0.5

Bolivina laevigata(Williamson, 1858)

0.79 0.80 0.53

Brizalina striatula (Cushman,1922)

0.72 0.57

Epistominella vitrea (Parker,1953)

0.54

Quinqueloculina seminulum(Linné, 1758)

0.47 �0.54 0.49 0.47 �0.65 �0.69 �0.67 �0.66 �0.44 �0.49 �0.4

Cribrononion venetum(Albani, Favero e SerandreiBarbero, 1991)

0.46 �0.45 �0.47 �0.49 �0.49 0.54

Cribrononion translucens(Natland, 1938)

�0.65 �0.53 0.56 0.55 �0.57 �0.58 �0.56 �0.52 �0.57 �0.43

Elphidium depressulum(Cushman, 1933)

�0.41

Textularia agglutinans(d’Orbigny, 1839)

�0.41 �0.42 �0.43 �0.41

Discorbis mirus (Cushman, 1922) �0.66 �0.59 0.77 0.79 �0.59 �0.55 �0.61 �0.51 �0.54 0.5 �0.42Rosalina globularis (d’Orbigny,

1826)�0.77 �0.87 0.64 0.55 �0.54 �0.50 �0.58 �0.57 �0.46 0.82

Nonionella auris (d’Orbigny,1839)

�0.72 �0.81 0.74 �0.52 �0.46 �0.55 �0.47 �0.4 0.74

V Cr Ba Zr Sn Y Nb Be Sc Fe Ca P Mg Ti Al Na K

Ammonia beccarii (Linnè, 1758) 0.5 0.4 0.4 0.42Buliminella elegantissima

(d’Orbigny, 1839)0.49 0.43 0 0.8 0.5 0.46 0.5 0.57 0.45

Bulimina elongata (d’Obigny,1846)

0.51 0.43

Bolivina laevigata (Williamson,1858)

0.4

Brizalina striatula (Cushman,1922)

Epistominella vitrea (Parker,1953)

Quinqueloculina seminulum(Linné, 1758)

�0.75 �0.62 �0.52 �0.47 �0.6 �0.4 �0.7 �0.7 �0.57 �0.67 �0.64 �0.7 �0.7 �0.51

Cribrononion venetum(Albani, Favero e SerandreiBarbero, 1991)

�0.48 �0.42 �0.5 �0.5 �0.47 �0.5 �0.5

Cribrononion translucens(Natland, 1938)

�0.52 �0.57 0.41 �0.52 �0.4 �0.5 �0.6 �0.6 �0.6 �0.55 �0.56 �0.52 �0.5 �0.5

Elphidium depressulum(Cushman, 1933)

Textularia agglutinans(d’Orbigny, 1839)

�0.49 �0.4 �0.4 �0.41 �0.5

Discorbis mirus (Cushman, 1922) �0.53 �0.58 �0.48 �0.42 �0.4 �0.6 �0.5 �0.6 0.52 �0.53 �0.54 �0.57 �0.6 �0.5Rosalina globularis (d’Orbigny,

1826)�0.6 �0.48 �0.63 �0.4 �0.5 �0.6 �0.5 0.81 �0.43 �0.46 �0.63 �0.6 �0.5

Nonionella auris(d’Orbigny, 1839)

�0.48 �0.48 �0.59 �0.4 �0.4 �0.5 �0.5 0.75 �0.44 �0.44 �0.59 �0.5 �0.5


the absence of the benthic fauna in certain areas and the presenceof the Buliminidae in others.

Several years after the study of Perin et al. (1997) and fromother investigations based on samples collected before our sam-pling (Vilela et al., 2003; Baptista Neto et al., 2006; Eichler et al.,2003b; Pereira et al., 2006), it appears that the environmental con-ditions of Guanabara Bay are not improving. In fact, an on goingworsening is evidenced by the identification of not previously re-ported areas of the bay which are unsuitable to living organisms.

6. Conclusions

This study contributes to a better understanding of the Guana-bara Bay ecosystem and of the several processes that concur to its

complexity. The multidisciplinary approach adopted leads to thefollowing conclusions:

(1) Despite the expected reduction in pollution due to the sew-age treating facilities adopted several years ago, the contam-ination of the Guanabara Bay sediments continues to behigh, in particular with regard to Cu, Pb, Zn, Cr, Ag and Cd.

(2) The highest concentration of heavy metals due to severalpollution sources (industrial sectors, river discharges, urbansettlements, etc.) is found in the north-western part of thebay.

(3) The southern part of the bay, directly connected to the opensea, is in part naturally purified by the tide currents and thewave forcing.


(4) The foraminifera assemblages, although characterized bystress-tolerant taxa, act as environmental indicators distin-guishing areas with a natural ecosystem from those areassubjected to different kinds of pollutants.

(5) A. beccarii correlates positively with lithogenetic and essen-tial elements (Fe, Mn and Ni), highlighting areas subjected to‘‘natural’’ environmental stress.

(6) B. elegantissima can be used as indicator of those areas withpollutants of anthropogenic origin, including heavy metalsnon-essential to the life like Cd and Ag.

(7) The content of foraminifera in sediment samples, comparedwith previously collected samples, shows that the factors,both natural and anthropogenic, that control the environ-mental conditions of the bay, are persistent.

(8) The lack of foraminifera colonization of the test area and thepresence of sterile sediments not previously reported, indi-cate the existence of unlivable conditions in the internalareas of the bay.

(9) The results suggest a worsening trend of the ecological stressconditions of the bay and indicate those areas in need ofaccurate monitoring for a future recovery plan.

Acknowledgements

This research was carried out as part of TAGUBAR (TAngentialGUanabara Bay Aeration Recovery) interdisciplinary cooperationproject between the University Ca’ Foscari of Venice, Italy (resp.G. Perin) and the UERJ, Universidade do Estado Rio de Janeiro, Bra-zil (resp. L. Verçosa Carvalheira).The authors kindly acknowledgethe financial support of the Ministry for Foreign Affairs of Italy.Thanks are given to Stefano Covelli, Andrea Mao, Giancarlo Arcari,Silvia De Pieri, Sabrina Manente and to the personnel of the Insti-tute of Oceanography of the UERJ for their assistance during fieldand lab work.

References

Albani, A., Serandrei-Barbero, R., Donnici, S., 2007. Foraminifera as ecologicalindicators in the Lagoon of Venice, Italy. Ecological Indicators 7, 239–253.

Alve, E., 1995. Benthic foraminiferal responses to estuarine pollution: a review.Journal of Foraminiferal Research 25, 190–204.

Alve, E., 1999. Colonization of new habitats by benthic foraminifera: a review.Earth-Science Reviews 46, 167–185.

Armynot du Châtelet, E., Debenay, J.-P., Soulard, R., 2004. Foraminiferal proxies forpollution monitoring in moderately polluted harbors. Environmental Pollution127, 27–40.

Bandy, O., Ingle Jr., J.C., Resig, J.M., 1964a. Foraminiferal trends, Laguna Beach outfallarea, California. Limnology and Oceanography 9, 112–123.

Bandy, O., Ingle Jr., J.C., Resig, J.M., 1964b. Foraminifera, Los Angeles county outfallarea, California. Limnology and Oceanography 9, 124–137.

Baptista Neto, J.A., Crapez, M., McAlister, J.J., Vilela, C., G, G., 2005. Concentrationand bioavailability of heavy metals in sediments from Niteroi Harbour(Guanabara Bay/S.E. Brazil). Journal of Coastal Research 21, 811–817.

Baptista Neto, J.A., Gingele, F.X., Leipe, T., Breme, I., 2006. Spatial distribution ofheavy metals in surficial sediments from Guanabara Bay: Rio de Janeiro, Brazil.Environmental Geology 49, 1051–1063.

Baptista Neto, J.A., Smith, B.J., Mcalliste, J.J., 1999. Concentrações de matais pesadosem sedimentos de escoamento superficial urbano: implicações quanto aqualidade ambiental de Niterói, RJ, Brasil. Anais da Academia Brasileira deCiências 4, 981–995.

Bernhard, J.M., Bowser, S.S., 1999. Benthic foraminifera of dysoxic sediments:chloroplast sequestration and functional morphology. Earth-Science Reviews46, 149–165.

Boesch, D.F., Rabalais, N.N., 1991. Effects of hypoxia on continental shelf benthos:comparison between the New York Bight and the Northern Gulf of Mexico. In:Tyson, R.V., Pearson, T.H. (Eds.), Modern and Ancient Continental Shelf Anoxia.Geol. Soc. Spec. Publ. 58, London, pp. 27–34.

Burone, L., Valente, P., Pires-Vanin, A.M.S., Sousa de Mello, S.H., Mahiques, M.M.,Braga, E., 2007. Benthic foraminiferal variability on a monthly scale in asubtropical bay moderately affected by urban sewage. Scientia Marina 71, 775–792.

Buzas, M., 1990. Another look at confidence limits for species proportions. Journal ofPalaeontology 64, 842–843.

Carnahan, E.A., 2005. Foraminiferal assemblages as bioindicators of potentially toxicelements in Biscayne Bay, Florida. Thesis, Master of Science, College of MarineScience. University of South Florida, Tampa, FL (US), 228 pp.

Carreira, R.S., Wagener, A.L.R., Readman, J.W., Fileman, T.W., Macko, S.A., Veiga, Ã.l.,2002. Changes in the sedimentary organic carbon pool of a fertilized tropicalestuary, Guanabara Bay, Brazil: an elemental, isotopic and molecular markerapproach. Marine Chemistry 79, 207–227.

Cearreta, A., Irabien, M.J., Leorri, E., Yusta, I., Quintanilla, A., Zabaleta, A., 2002.Environmental transformation of the Bilbao estuary, N. Spain: microfaunal andgeochemical proxies in the sedimentary record. Marine Pollution Bulletin 44,487–503.

Coccioni, R., Frontalini, F., Marsili, A., Mana, D., 2009. Benthic foraminifera and traceelement distribution: a case-study from the heavily polluted lagoon of Venice(Italy). Marine Pollution Bulletin 59, 257–267.

Covelli, S., 2007. Marine sediment geochemistry. In: Perin, G. (Ed.), Tagubar Project,Final Reports, Data & Documents 2003–2007. Ca’ Foscari University of Venice,Italy.

Covelli, S., Protopsalti, I., Acquavita, A., Sperle, M., Bonardi, M., Emili, A., 2012.Spatial variation, speciation and sedimentary records of mercury in theGuanabara Bay (Rio de Janeiro, Brazil). Continental Shelf Research 35, 29–42.

Cucco, A., 2007. Hydrodynamic numerical model of the Guanabara Bay. In: Perin, G.(Ed.), Tagubar Project, Final Reports, Data & Documents 2003–2007. Ca’ FoscariUniversity of Venice, Italy.

Culver, S.J., Buzas, M.A., 1995. The effects of anthropogenic habitat disturbance,habitat destruction, and global warming on shallow marine benthicforaminifera. Journal of Foraminiferal Research 25, 204–211.

Debenay, J.-P., Tsakiridis, E., Soulard, R., Grossel, H., 2001. Factors determining thedistribution of foraminiferal assembleges in Port Joinville Harbor (Ile d’Yeu,France): the influence of pollution. Marine Micropaleontology 43, 75–118.

Debenay, J.-P., Della Patrona, L., Goguenheim, H., 2009. Colonization of coastalenvironments by foraminifera: insight from shrimp ponds in New Caledonia(SW Pacific). Journal of Foraminiferal Research 39, 249–266.

Donnici, S., Serandrei-Barbero, R., 2002. The benthic foraminiferal communities ofthe northern Adriatic continental shelf. Marine Micropaleontology 44, 93–123.

Donnici, S., Serandrei-Barbero, R., 2005. I foraminiferi di ambiente vallivo dellaLaguna di Venezia. Lavori della Soc. Ven. Scienze Naturali 30, 25–36.

Donnici, S., Serandrei-Barbero, R., Taroni, G., 1997. Living benthic foraminifera in theLagoon of Venice (italy). Populations dynamics and its significance.Micropaleontology 43, 440–454.

Eichler, P.P.B., Eichler, B.B., Pimenta, F.P., Cardoso, P.B.P.K., da Rocha Mendes Pereira,E., 2003a. Avaliação dos Efeitos Ambientais e Ecológicos Referentes ao AcidenteOcorrido no Oleoduto Pe-II (Reduc – Petrobrás) na Baía de Guanabara. Anuáriodo Instituto de Geociências – UFRJ 26, 139–151.

Eichler, P.P.B., Eichler, B.B., de Miranda, L.B., Pereira, E.M., Kfouri, P.B.P., Pimenta,F.M., Bergamo, A.L., Vilela, C.G., 2003b. Benthic foraminiferal response tovariations in temperature, salinity, dissolved oxygen and organic carbon, in theGuanabara Bay, Rio de Janeiro, Brazil. Anuario do Instituto de Geociências –UFRJ 26, 36–51.

Eichler, P.P.B., Eichler, B.B., Sen Gupta, B., Rösch Rodrigues, A., 2012. Foraminifera asindicators of marine pollutant contamination on inner continental shelf ofsouthern Brazil. Marine Pollution Bulletin 64, 22–30.

Faria de Melo, M., Sanchez, B.A., 2001. Geochemistry and mineralogy of recentsediments of Guanabara Bay (NE sector) and its major rivers – Rio de JaneiroState – Brazil. Anais da Academia Brasileira de Ciências 73, 121–133.

Ferraro, L., Sprovieri, M., Alberico, I., Lirer, F., Prevedello, L., Marsella, E., 2006.Benthic foraminifera and heavy metals distribution: a case study from theNaples Harbour (Tyrrhenian Sea, Southern Italy). Environmental Pollution 142,274–287.

Geslin, E., Stouff, V., Debenay, J.P., Lesourd, M., 2000. Environmental variation andforaminiferal test abnormalities. In: Martin, R.E. (Ed.), EnvironmentalMicropaleontology – The Application of Microfossils to EnvironmentalGeology. Kluwer, New York, pp. 191–215.

Hallock, P., Lidz, B.H., Cockey-Burkhard, E.M., Donnelly, K.B., 2003. Foraminifera asbioindicators in coral reef assessment and monitoring: the FORAM index.Environmental Monitoring and Assessment 81, 221–238.

Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Palaeontological statisticssoftware package for education and data analyisis. Palaeontologia Electronica 4,9.

Jorissen, F.J., 1987. The distribution of benthic foraminifera in the Adriatic Sea.Marine Micropaleontology 12, 21–48.

Kennish, M.J., 1992. Ecology of Estuaries: Anthropogenic Effects. CRC Press.Kjerfve, B.R., Ribeiro, C.H.A., Dias, G.T.M., Filippo, A.M., Da Silva Quaresma, V.R.,

1997. Oceanographic characteristics of an impacted coastal bay: Baya deGuanabara, Rio de Janeiro, Brazil. Continental Shelf Research 17, 1609–1643.

Kjerfve, B., Lacerda, L.D., Dias, G.M.T., 2001. Baía de Guanabara, Rio de Janeiro,Brazil. In: Seeliger, U., Kjerfve, B. (Eds.), Coastal Marine Ecosystems of LatinAmerica, vol. 144. Springer Verlag, Heidelberg, pp. 107–117.

Loeblich, A.R., Tappan, H., 1987. Foraminiferal Genera and their Classification, v. 1–2. Van Nostrand Reinhold Company, New York, 970 pp.

Mao, A., 2007. Guanabara Bay sediment chemistry. In: Perin, G. (Ed.), TagubarProject Final Reports, Data & Documents 2002–2007. Ca’ Foscari University ofVenice, Italy.

Martins, V., Ferreira da Silva, E., Sequeira, C., Rocha, F., Duarte, A.C., 2010. Evaluationof the ecological effects of heavy metals on the assemblages of benthicforaminifera of the canals of Aveiro (Portugal). Estuarine, Coastal and ShelfScience 87, 293–304.


Morvan, J., Le Cadre, V., Jorissen, F., Debenay, J.-P., 2004. Foraminifera as potentialbio-indicators of the Erika’’ oil spill in the Bay of Bourgneuf: field andexperimental studies. Aquatic Living Resources 17, 317–322.

Munsel, D., Kramar, U., Dissard, D., Nehrke, G., Berner, Z., Bijma, J., 2010. Heavymetal incorporation in foraminiferal calcite: results from multi-elementenrichment culture experiments with Ammonia tepida. Biogeosciences 7,2339–2350.

Murray, J.W., 1991. Ecology and Palaeoecology of Benthic Foraminifera. LongmanGroup Ltd., London, 397 pp.

Murray, J.W., 2006. Ecology and Applications of Benthic Foraminifera. CambridgeUniversity Press, 426 pp.

Nooijer de, L.J., Reichart, G.J., Duenas-Bohorquez, A., Wolthers, M., Ernst, S.R., Mason,P.R.D., van der Zwaan, G.J., 2007. Copper incorporation in foraminiferal calcite:results from culturing experiments. Biogeosciences 4, 493–504.

Nikulina, A., Polovodova, I., Schönfeld, J., 2008. Foraminiferal response toenvironmental changes in Kiel Fjord, SW Baltic Sea. eEarth 3, 13.

Pereira, E.R.M., Eichler, P.P.B., Eichler, B.B., 2006. Foraminifera as proxies inenvironmental diagnostic in Guanabara Bay, RJ. Journal of Coastal Research39, 1395–1398, Special Issue.

Perin, G., Fabris, R., Manente, S., Rebello Wagener, A., Hamacher, C., Scotto, S., 1997.A five-year study on the heavy metal pollution of Guanabara Bay sediments (Riode Janeiro, Brazil) and evaluation of the metal bioavailability by means ofgeochemical speciation. Water Research 31, 3017–3028.

Rathburn, A., Perez, E., Giestes, J.M., 2008. SIOSED Line b: foraminiferal studies.Ministry for Infrastructure and Transport – Venice Water Autority, CD finalSIOSED Project, Venezia 22 settembre 2008.

Rebello, A.L., Ponciano, C.R., Melges, L.H., 1988. Availaçao da Produtividade Primáriae da Disponibilidade de Nutrientes na Baia de Guanabara. Anais da AcademiaBrasileira de Ciências 60, 419–430.

Romano, E., Bergamin, L., Finoia, M.G., Carboni, M.G., Ausili, A., Gabellini, M., 2008.Industrial pollution at Bagnoli (Naples, Italy): benthic foraminifera as a tool inintegrated programs of environmental characterisation. Marine PollutionBulletin 56, 439–457.

Romano, E., Bergamin, L., Ausili, A., Pierfranceschi, G., Maggi, C., Sesta, G., Gabellini,M., 2009. The impact of the Bagnoli industrial site (Naples, Italy) on sea-bottomenvironment. Chemical and textural features of sediments and the relatedresponse of benthic foraminifera. Marine Pollution Bulletin 59, 245–256.

Salomons, W., Forstner, U., 1984. Metals in the Hydrocycle. Springer-Verlag, Berlin,349 pp.

Samir, A.M., 2000. The response of benthic foraminifera and ostracods to variouspollution sources: a study from two lagoons in Egypt. Journal of ForaminiferalResearch 30, 83–98.

Saraswat, R., Kurtarbar, S.R., Mazumder, A., Nigam, R., 2004. Foraminifers asindicators of marine pollution: a culture experiment with Rosalina leei. MarinePollution Bulletin 48, 91–96.

Scott, D.B., Medioli, F.S., 1980. Living vs. total foraminiferal populations:their relative usefulness in paleoecology. Journal of Paleontology 54,814–831.

Serandrei-Barbero, R., Albani, A.D., Zecchetto, S., 1997. Palaeoenvironmentalsignificance of a benthic foraminifera fauna from an archaeological excavationin the Lagoon of Venice, Italy. Palaeogeography, Palaeoclimatology,Palaeoecology 136, 41–52.

Serandrei-Barbero, R., Donnici, S., Madricardo, F., 2011. Supratidal foraminifera asecological indicators in anthropically modified wetlands (Lagoon of Venice,Italy). Ecological Engineering 37, 1140–1148.

Siegel, F.R., 2002. Environmental Geochemistry of Potentially Toxic Metals.Springer, New York.

Sobrinho da Silva, F., Costa (da) Pereira, D., Sanchez Nuñez, L., Krepsk, N., FontanaI,L.F., Baptista NetoI, J.A., Araújo Carlos CrapezII, M., 2008. Bacteriological study ofthe superficial sediments of Guanabara Bay, RJ, Brazil. Brazilian Journal ofOceanography 56, 13–22.

Stachowitsch, M., 1991. Anoxia in the Northern Adriatic Sea: Rapid Death, SlowRecovery, vol. 58. Geological Society, London, pp. 119–129 (SpecialPublications).

Stott, L.D., Hayden, T.P., Griffith, J., 1996. Benthic foraminifera at the Los Angelescounty whites point outfall revisited. Journal of Foraminiferal Research 26, 357–368.

Vilela, C.G., Sanjinés, A.E.S., Ghiselli Jr., R.O., Filho, J.G.M., Baptista Neto, J.A., Barbosa,C.F., 2003. Search for Bioindicators of pollution in the Guanabara Bay:integrations of ecologic patterns. Anuario do Instituto de Geociências – UFRJ26, 25–34.

Vilela, C.G., Batista, D.S., Baptista-Neto, J.A., Crapez, M., Mcallister, J.J., 2004. Benthicforaminifera distribution in high polluted sediments from Niteroi Harbor(Guanabara Bay), Rio de Janeiro, Brazil. Anais da Academia Brasileira de Ciências76, 161–171.

Warren, L.A., Haack, E.A., 2001. Biogeochemical controls on metal behaviour infreshwater environments. Earth-Science Reviews 54, 261–320.

Yanko, V., Ahmad, M., Kaminski, M., 1998. Morphological deformities of benthicforaminiferal tests in response to pollution by heavy metals: implications forpollution monitoring. Journal of Foraminiferal Research 28, 177–200.

Yanko, V., Arnold, A.J., Parker, W.C., 1999. Effects of marine pollution on benthicforaminifera. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer Ac. Publ.,New York, pp. 217–235.