Marine Pollution Bulletin 79 (2014) 175–187

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Marine Pollution Bulletin

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Late Holocene evolution and increasing pollution in Guanabara Bay, Riode Janeiro, SE Brazil

0025-326X/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.marpolbul.2013.12.020

⇑ Corresponding author. Tel.: +55 21 2598 9484; fax: +55 21 2598 9465.E-mail addresses: vilela@geologia.ufrj.br (C.G. Vilela), bidaorioli@gmail.com (B.O.

Figueira), ncardosomariana@yahoo.com.br (M.C. Macedo), jabneto@id.uff.br (J.A.Baptista Neto).

1 Present address: School of Environment, University of Auckland, Auckland 1142,New Zealand.

Claudia Gutterres Vilela a,⇑, Brígida Orioli Figueira a,1, Mariana Cardoso Macedo a,José Antonio Baptista Neto b

a Depto de Geologia, IGEO, CCMN/Universidade Federal do Rio de Janeiro, Av. Athos da Silveira Ramos 274, Cidade Universitária, 21941-916 Rio de Janeiro, RJ, Brazilb Instituto de Geociências, Lagemar/Universidade Federal Fluminense, Av. Litorânea s/n, Gragoatá, 24210-340 Niterói, RJ, Brazil

a r t i c l e i n f o

Keywords:Foraminiferal bioindicatorPollutionCoresRadiocarbon dates

a b s t r a c t

To detect changes during the Late Holocene and historical periods in Guanabara Bay, the paleoecological andecological parameters from nine cores were analysed using foraminiferal assemblages and bioindicators.Usingradiocarbon dates and sedimentation rates in the cores, it was possible to detect the firstEuropeans’ arri-val in the 16th century. Foraminiferal bioindicators of organic matter and human pollution were correlatedwith radiocarbon dates from the bottom and middle of the cores in each region and revealed an increase inpollution along the cores. The foraminiferal results were compared with total organic carbon (TOC) valuesbefore, during and after European settlement and showed a historical increase in organic matter.

Pristine mangrove ecosystems are characterised by agglutinated species such as Ammotium salsum, and thepresence of this organism also confirmed the extent of historical mangrove forests. Ammonia tepida, Buliminel-la elegantissima and Elphidium excavatum were the dominant species, but they presented distinct patterns overtime. B. elegantissima was dominant before the European influence in older sediments with high organic mat-ter content that were found at deeper intervals. A. tepida is dominant in younger sediments at upper intervals,as a bioindicator of human pollution.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Correctly interpreting environmental changes in Guanabara Bayduring different historical periods relies on interpretations of itsecology before and after its discovery by Europeans. The arrivalof the first Europeans in America in the 15th and 16th centuriesbrought the advances of other countries to people who still livedin balance with nature. The increasing human influence since theEuropean settlement and in the following centuries can be mea-sured by records deposited in old sediments below the GuanabaraBay sediment–water interface. Microfossils, such as the benthicforaminifera, can be useful in those reconstructions. They respondto changes in salinity, organic matter, pH, and heavy metals, andprovide a measure of the level of human influence (Alve, 1991; Bol-tovskoy et al., 1980; Culver and Buzas, 1995; Debenay et al., 2000;Geslin et al., 2002; Murray, 2006).

Guanabara Bay is located in south eastern Brazil, surrounded bythe Rio de Janeiro City, which is one of the largest cities of Brazil,

and three other large cities (Niterói, São Gonçalo and Duque deCaxias) in addition to other districts and municipalities of Rio deJaneiro State. This important tourist and economic centre includestwo harbours, two oil refineries and thousands of industries. Itserves as recipient of untreated domestic and industrial sewage,and products of runoff from urban streets. There is a tourist tradein sightseeing around the bay, though the serious problems of pol-lution and degradation remain hidden.

The Guanabara estuarine system was covered by rising seawater during the Holocene by the marine post-glacial transgres-sion. Its hydrographic bay comprises tens of small and mediumsized degraded rivers. It is surrounded by beaches and mangroveforests, which have nearly all been destroyed by infill, land recla-mation and garbage (Amador, 1997; Kjerfve et al., 1997, 2000). Inthe northern region, there is a protected area that includes an in-tact mangrove forest.

This study analyses some paeleoecological and ecologicalparameters in Guanabara Bay by the use of foraminiferal assem-blages and bioindicators that responded to changes during theHolocene and historical periods. Foraminiferal bioindicators oforganic matter and human pollution were used to determine thelevels of pollution in nine cores collected from different regionsof Guanabara Bay. The results were correlated with radiocarbonages, and increase our understanding of the evolution of

176 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

paleoenvironmental features during the Holocene and historicalperiod. Foraminiferal results were compared to total organic car-bon (TOC) values before, during and after the colonisation period.Those results should be used for future studies about pollutionand pollution reduction monitoring.

2. Methods

Nine cores, varying from 130 to 280 cm in length, were col-lected in four distinct areas of Guanabara Bay and analysed for

Fig. 1. Location of the cores from Guanabar

microfauna contents and TOC. The areas include the mangrove sys-tem APA (under protection area) de Guapimirim to the north; SãoGonçalo municipality to the north–northeast, where the mangroveforest is nearly completely destroyed; Paquetá Island, also north–north eastern; and Jurujuba Sound, in the south eastern area(Fig. 1; Table 1). We selected locations for the core that were likelyto be less disturbed based on high resolution seismic (3.5–7.0 kHz)reflection patterns (Quaresma et al., 2000; Catanzaro et al., 2004).

Those results were correlated to sediment features, and the fourcores from the distinct areas were radiocarbon (C14) dated at thebottom and middle intervals.

a Bay, Rio de Janeiro, Southeast Brazil.

Table 1Core coordinates, sea-water depths, core lengths, studied regions and dates of collection in Guanabara Bay.

Cores Lat. (S) Long. (W) Sea-water depth (m) Core length (cm) Region Date of collection

T3 22�4100600 43�0402900 1 169 APA de Guapimirim July 2005T4 22�4100600 43�0404700 1 130 November 2001

T2 22�4501500 43�03450 1.5 135 São Gonçalo November 2001T14 22�5004000 43�0700000 3 220 July 2005T15 22�4700200 43�0504000 4 200 July 2005

T8 22�4402800 43�0604600 7 242 Paquetá November 2001T10 22�4403000 43�0703800 5 222 November 2001T11 22�4500600 43�0901600 5 283 November 2001

T13 22�5502500 43�0603400 3 223 Jurujuba July 2005

Table 2Radiocarbon dates at cores (T) in Guanabara Bay. *T4, 122 cm – dating after Barthet al. (2006); *T8 – dating after Barth et al. (2004).

Depth (cm) C14 date (yrs BP)

APA of Guapimirim*T4 90 530 ± 25

*122 1760 ± 50

Paquetá island*T8 222 4210 ± 40

São GonçaloT14 (south site) 70 550 ± 40

200 5700 ± 40

Jurujuba SoundT13 202 3520 ± 50

Table 3Shannon (H0) diversity index and TOC values in the Guanabara Bay core intervals.

T2 T3 T4 T8 T

(cm) (H) TOC(%)

(cm) (H) TOC(%)

(cm) (H) TOC(%)

(cm) (H) TOC(%)

(

0 1.19 4.75 0 1.74 5.70 0 1.12 6.30 0 0.00 4.56�2 1.44 5.01 �2 1.24 5.79 �2 1.63 5.69 �2 1.48 5.38�4 1.33 5.91 �4 1.44 4.78 �4 1.33 6.00 �4 1.82 4.93�6 1.25 5.40 �6 1.43 4.79 �6 1.04 5.75 �6 1.50 4.28�8 1.41 4.61 �8 1.91 4.52 �8 1.47 6.46 �8 1.63 5.41�10 0.83 4.58 �15 1.61 4.79 �10 1.36 6.31 �15 0.94 5.08�15 1.42 4.63 �20 1.80 4.35 �15 0.00 6.23 �20 1.81 5.05�20 0.79 4.60 �25 2.29 4.15 �20 1.77 4.79 �25 1.31 4.45�25 1.65 4.65 �30 1.08 4.86 �25 0.00 4.98 �30 1.16 4.40�30 1.04 4.89 �35 1.34 4.40 �30 0.00 5.88 �35 1.10 3.88�35 0.64 4.19 �40 1.84 4.52 �35 1.86 5.45 �40 1.06 3.58�40 0.88 4.89 �45 1.49 3.77 �40 1.63 4.91 �45 0.49 3.88�45 0.90 4.58 �50 1.72 3.94 �45 1.60 4.74 �50 1.15 4.24�50 0.90 4.81 �60 2.00 3.03 �50 1.45 5.67 �60 0.55 3.48�60 1.30 4.97 �70 1.84 3.66 �60 0.92 3.31 �70 0.55 3.02�70 0.59 3.68 �80 2.00 1.79 �70 1.91 4.10 �80 0.71 2.44�80 0.96 3.86 �90 1.53 1.52 �80 1.87 2.56 �90 0.67 2.53�90 0.80 3.65 �100 1.21 1.59 �90 1.90 1.89 �100 1.19 2.58 ��100 0.88 4.13 �110 0.38 1.56 �100 2.06 2.02 �110 1.50 1.37 ��110 1.53 4.15 �120 2.05 1.32 �110 1.91 0.88 �120 1.24 2.72 ��120 1.28 4.21 �130 1.95 1.20 �120 1.80 0.58 �130 1.41 2.55 ��130 0.51 4.12 �140 2.12 1.00 �130 0.00 0.66 �140 0.87 2.10 ��135 0.00 �150 2.07 1.25 �150 0.77 2.16 �

�160 1.30 1.50 �160 1.48 2.27 ��169 1.98 1.13 �170 1.52 2.15 �

�180 1.13 2.16 ��190 1.73 2.18 ��200 0.93 2.00 ��210 0.93 2.05 ��222 0.71 1.63 ��232 0.00 1.45�239 0.00 1.02

C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187 177

Radiocarbon dates were determined by the Beta AnalyticsRadiocarbon Laboratory (Miami, USA) in organic clay and shellsamples from the cores located at APA de Guapimirim (T4),Paquetá Island (T8), São Gonçalo (T14) and Jurujuba Sound (T13).The measurements were taken with AMS radiometric methods,and the dates are reported as radiocarbon years before present(present = AD 1950). Calendar-calibrated results (Table 2) werecalculated from the Conventional Radiocarbon Age (Talma andVogel, 1993; Stuiver et al., 1998; INTCAL04, 2004) using a twosigma calibration (Variables used: C13/C12 = �3.1; 1R = �8 ± 69;Glob. Res = �200–500).

Sediment sub-samples were taken at centimetre intervals from thetop to the bottom for sediment and microfaunal analyses. They werestandardised for 30 ml each. The treatment of sub-samples for

10 T11 T13 T14 T15

cm) (H) TOC(%)

(cm) (H) TOC(%)

(cm) (H) (cm) (H) (cm) (H)

0 0.00 6.24 �0 1.49 5.60 0 1.51 �6 1.18 �2 2.35�2 1.66 6.36 �2 1.30 �4 2.25 �18 0.88 �10 1.51�4 1.79 5.79 �4 1.75 �8 1.86 �26 0.67 �15 2.18�6 1.81 5.74 �6 0.00 5.31 �20 1.09 �30 0.72 �20 2.67�8 2.00 5.60 �8 1.40 �25 1.85 �34 0.94 �25 2.33�15 1.42 5.39 �10 1.49 4.84 �35 1.99 �42 0.00 �30 2.27�20 1.79 5.33 �15 1.69 4.10 �40 1.84 �50 0.00 �35 1.82�25 1.24 5.64 �20 0.69 3.92 �45 1.87 �58 0.00 �40 1.68�30 1.88 5.26 �25 0.00 3.87 �50 1.87 �66 0.00 �45 1.90�35 1.86 5.29 �30 1.88 3.77 �60 1.42 �74 1.34 �50 2.18�40 1.82 4.96 �35 1.79 2.68 �70 2.02 �82 1.00 �60 2.19�45 0.64 5.37 �40 1.38 2.63 �90 1.66 �90 1.63 �70 0.72�50 1.08 4.85 �45 1.29 2.39 �100 1.95 �110 1.21 �80 1.96�60 0.69 4.45 �50 1.38 2.67 �110 1.99 �134 1.40 �90 2.28�70 1.07 3.50 �60 1.56 2.57 �120 1.37 �142 1.24 �100 2.18�80 1.14 2.70 �70 1.52 2.35 �130 1.30 �170 1.47 �110 2.21�90 1.17 2.29 �80 1.81 2.53 �140 1.82 �194 1.42 �120 2.28100 0.90 2.31 �90 1.62 2.24 �150 1.93 �210 1.78 �130 2.24110 1.08 2.41 �100 1.79 1.96 �160 1.59 �140 2.28120 1.41 2.26 �110 2.13 1.70 �170 1.80 �150 2.33130 2.01 1.65 �120 1.54 1.79 �190 1.27 �160 1.69140 1.66 1.95 �130 1.67 1.48 �200 1.11 �170 1.67150 0.78 2.00 �140 1.44 1.53 �180 1.83160 1.65 2.02 �150 0.96 1.48 �190 1.67170 1.24 1.83 �160 1.64 1.38 �200 1.62180 0.78 1.87 �170 1.52 1.59190 1.70 1.63 �180 1.34 1.86200 1.83 1.43 �190 1.08 1.60210 1.15 1.56 �200 1.08 1.42220 0.00 1.13 �210 1.35 1.39

�220 1.50 1.41�230 1.13 1.01�240 1.49 0.84�250 1.51 0.96�260 1.83 0.67�270 1.48 0.81�280 1.56 0.33

Table 4Shannon H0 diversity and TOC values in the upper, middle and bottom intervals from the Guanabara Bay cores.

T3 T4 T8 T10 T11 T2 T14 T15 T13

(cm) (H) TOC (%) (cm) (H) TOC (%) (cm) (H) TOC (%) (cm) (H) TOC (%) (cm) (H) TOC (%) (cm) (H) TOC (%) (cm) (H) (cm) (H) (cm) (H)

0 1.74 5.70 0 1.12 6.30 0 0.00 4.56 0 0.00 6.24 �0 1.49 5.60 0 1.19 4.75 �6 1.18 �2 2.35 0 1.51�80 2.00 1.79 �70 1.91 4.10 �80 0.71 2.44 �80 1.14 2.70 �70 1.52 2.35 �70 0.59 3.68 �170 1.47 �110 2.21 �130 1.30�140 2.12 1.00 �130 0.00 0.66 �140 0.87 2.10 �140 1.66 1.95 �130 1.67 1.48 �130 0.51 4.12 �170 1.67 �200 1.11

�210 0.93 2.05 �210 1.15 1.56 �200 1.08 1.42

178 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

microfaunal studies consisted of washing, wet sieving with a0.063 mm-mesh sieve and drying in an oven at 50 �C. After treatment,the samples were picked, counted and the benthic foraminifera wereclassified to the species level. A minimum count of 100 specimens persub-sample (interval) was used for statistical analyses, according toFatela and Taborda (2002). The determination of genera followedLoeblich and Tappan (1988), and the species classification were basedon classic works, including the catalogue of Ellis and Messina (1940-etseq) and several specific studies, such as Cushman (1931, 1939),Tinoco (1971), Barker (1960) and Debenay et al. (2000).

Absolute and relative abundance indices were evaluated alongwith ecological parameters of dominance and diversity. Absoluteabundance values were recorded in Excel tables. Species with10% or higher relative abundance in the samples were consideredto be dominant (Boltovskoy and Totah, 1985). The species diversitywas calculated using the Shannon H0 diversity index (Shannon,1949), which considers the number of species and their relative

Fig. 2. The relative abundance of dominant species per interval in the APA de Guapimirim2006).

abundance in the assemblage. The dominant species distributionsalong the cores were presented with Panplot graphics using Pan-gaea software.

Particle size was analysed using a Malvern 2000 hydroG laseranalyser after the removal of organic matter by digesting in 30%H2O2 (Folk, 1974). The total organic carbon and inorganic carboncontents were determined using a CS infrared analyser model EltraMetalyt 1000CS. The geochemical methods consisted of pulverisa-tion, acidification, washing and drying of the samples. Then, theywere placed in an oven for burning with O2, and the organic carbonwas measured. The TOC analyses expressed the percentage of or-ganic carbon in core sub-samples.

3. Results

The sediment analyses in the cores showed colours varyingfrom black to dark or olive grey. Muddy sediments with silt

T3 and T4 cores. Radiocarbon dates in core T4 are shown (modified from Figueira,

Table 5Absolute abundances of species in core T3, APA de Guapimirim, Guanabara Bay.

Table 6Absolute abundances of species in core T4, APA de Guapimirim, Guanabara Bay.

C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187 179

Fig. 3. The relative abundance of dominant species per interval in the São Gonçalo T2, T14 and T15 cores. Radiocarbon dates in core T14 are shown (modified from Figueira,2006).

180 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

laminations and a lens of organic matter were dominant in the topintervals. Near Paquetá Island, in core T8, there was an abrupt con-tact or an erosive surface at the bottom, with coarse particles in a

hard mottled and brownish clay. The deposits near that contact, at222 cm, were radiocarbon dated to 4210 ± 40 yrs BP (Barth et al.,2004; Barreto et al., 2005).

C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187 181

TOC values increased many fold from the bottom to the top inthe most of cores. They increased more than threefold above90 cm of depth (Recent) and more slowly in the deeper sectionsof the cores (Tables 3 and 4). Considering the micropaleontologicalanalyses, the Shannon H’ diversity index presented low values (e.g.,Tables 3 and 4).

The dominant species that characterised the various depthintervals may indicate levels of pollution or organic matter and re-flect the region of the bay from which the core was collected.

In APA de Guapimirim (cores T3 and T4), agglutinated speciessuch as Ammotium salsum, Haplophragmoides wilberti and Textulariaearlandi are more abundant in the upper intervals. Ammonia tepida,Elphidium excavatum and Elphidium discoidale have distinct abun-dance values along the cores (Fig. 2, Tables 5 and 6).

In the São Gonçalo area, which contains a nearly destroyedmangrove, the agglutinated H. wilberti and Trochammina inflatawere dominant only in core T2, from the north. The cores T14and T15 presented rare agglutinated species. A. tepida was domi-nant in the shallow intervals, and Buliminella elegantissima wasdominant at the deepest intervals (Fig. 3, Tables 7–9).

Near the Paquetá Island, in cores T8, T10 and T11, B. elegantiss-ima and A. tepida distributions are inversely proportional. A. tepidatended to be abundant and dominant at shallow intervals, and B.elegantissima at deep intervals (Fig. 4, Tables 10–12).

The results from Jurujuba Sound, in core T13, clearly showedthe distinct occurrence of A. tepida at shallow intervals and B. ele-gantissima at deep intervals (Fig. 5, Table 13).

Table 7Absolute abundances of species in core T2, São Gonçalo, Guanabara Bay.

Radiocarbon ages in the cores of each region in Guanabara Bayconfirm an increase in the sedimentation rates in the upper sec-tions. In the APA de Guapimirim and São Gonçalo, dates in the mid-dle of the cores were approximately 500 yrs BP and marked theEuropeans’ discovery of and arrival in South America.

4. Discussion

Several authors have already discussed the causes and the eco-system effects of pollution, and in particular the effects on micro-fauna. The use of benthic foraminifera in environmentalmonitoring of polluted areas has already yielded good results.The responses of benthic foraminifera to organic and inorganic pol-lution have been evaluated in many marginal marine regions at alllatitudes and have proven their utility for pollution monitoring(Bates and Spencer, 1979; Alve, 1991; Culver and Buzas, 1995;Debenay et al., 2000; Samir, 2000; Vilela et al., 2011).

In foraminiferal assemblages, high levels of contamination canresult in extreme stress and cause local extinction of some species,the dominance of few species, and abnormalities in tests for thelevels of environmental pollutants (Culver and Buzas, 1995; Yankoet al., 1994; Alve and Olsgard, 1999; Geslin et al., 2002; Vilela et al.,2004). Nevertheless, certain species are tolerant to contaminants,and they have been used as pollution bioindicators in different re-gions of the world. A. tepida and Triloculina marioni in the Carib-bean and Mediterranean, along with E. excavatum and Eggerellaadvena in northern seas (Schafer, 1973; Seiglie, 1975; Culver and

Table 8Absolute abundances of species in core T14, São Gonçalo, Guanabara Bay.

Table 9Absolute abundances of species in core T15, São Gonçalo, Guanabara Bay.

182 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

Fig. 4. The relative abundance of Ammonia tepida and Buliminella elegantissima per interval in the cores T8, T10 and T11, near Paquetá Island. Radiocarbon dates in the core T8are shown (modified from Figueira, 2006).

Table 10Absolute abundances of species in core T8, Paquetá Island, Guanabara Bay.

C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187 183

Buzas, 1995; Yanko et al., 1994, 1999; Le Cadre and Debenay,2006), have been cited as pollution bioindicators. E. excavatumand Elphidium gunteri are common in stressed bays and estuaries(Sen Gupta et al., 1996; Duleba and Debenay, 2003; Vilela et al.,2003; Lançone et al., 2005). Benthic foraminifera have been usedas proxies for various parameters of pollution (Murray, 2002,2006). Areas affected by sewage outfalls are dominated by organ-ic-tolerant species such as B. elegantissima and Bulimina marginata(Bandy et al., 1965; Collins et al., 1995). A. tepida and B. elegantiss-ima are used as proxies in bays and lagoons with high organic mat-ter content, but coastal areas such as estuaries are complex and

each has its own environmental characteristics. Consequently, aspointed out by Murray and Alve (2002), understanding the pre-pol-lution baseline through the sedimentary record and microfossilcontent is important to the analysis of recent environmentalchanges and anthropogenic impacts.

The microfossil record can provide information on changes indistinct specific region over historical time scales (Cearreta et al.,2002). In Guanabara Bay, the radiocarbon ages of core subsamplesin distinct regions such as APA de Guapimirim, São Gonçalo, Pa-quetá and Jurujuba were correlated with different sedimentationrates. Godoy et al. (1998) estimated increased sedimentation rates

Table 11Absolute abundances of species in core T10, Paquetá Island, Guanabara Bay.

Table 12Absolute abundances of species in core T11, Paquetá Island, Guanabara Bay.

184 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

from approximately 50 cm of depth to the top of sediment cores inthe APA the Guapimirim and São Gonçalo regions by applyingmethods of 210Pb analysis and the constant rate of supply (CRS).Baptista Neto et al. (1999, 2013) found higher sediment rates inthe upper core in the Jurujuba Sound region.

Radiocarbon dates, sediment rates and foraminiferal resultswere correlated with TOC values from before, during and afterthe colonisation period.

The values of the Shannon H0 diversity index were relativelyconsistent along the cores (e.g., Table 3), but they were in line withvalues from bays, estuaries and shallow continental shelves in

many regions and latitudes. However, the differences among spe-cies assemblages may aid the paleoecological interpretations forGuanabara Bay. Species such as A. tepida, B. elegantissima, E. excav-atum and E. gunteri were differently distributed according to theage of the sediments. Previous works have pointed out that A. tep-ida is an opportunistic species and can resist to damage fromdomestic sewage, chemical effluents and heavy metals even asother species disappear. Elphidium spp. and B. elegantissima are ci-ted as common and dominant in impacted coastal areas (Yankoet al., 1994, 1999; Alve, 1995; Collins et al., 1995; Culver and Buzas,1995; Sen Gupta et al., 1996; Murray and Alve, 2002; Vilela et al.,

Fig. 5. The relative abundance of Ammonia tepida and Buliminella elegantissima perinterval in core T13, in Jurujuba Sound. The radiocarbon date is shown (modifiedfrom Figueira, 2006).

C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187 185

2003). These species are distributed differently along the studiedcores in Guanabara Bay.

4.1. APA de Guapimirim region

In the APA de Guapimirim, there is a protected mangrove sys-tem. Barth et al. (2006) confirmed that the mangrove forest wasalso present in the past by examining pollens characteristic ofmangrove vegetation in sediments in the region. Agglutinatedforaminifera such as A. salsum, H. wilberti and Ammobaculites spp.(Osarko et al., 1997; Barbosa et al., 2005), which are prevalent inmangroves, were found in several core intervals in the APA deGuapimirim, and confirmed Barth et al.’s (2004, 2006) results. A.salsum and other agglutinated species have been observed in la-goons and estuaries with variable in salinity, in tropical environ-ments (Scott and Medioli, 1980; Eichler et al., 1995).

Godoy et al. (1998) found that sediment rates increased fromapproximately 50 cm of depth to the top of sediment cores in theAPA the Guapimirim region, as stated above. At 54 cm depth, the

Table 13Absolute abundances of species in core T13, Jurujuba Sound, Guanabara Bay.

sediment rate was 0.19 cm/yrs and, at 39 cm it was 0.86 cm/yrs.In this study, the radiocarbon dates from the APA de Guapimirimindicated that there was an increase in sedimentation rates from90 cm of depth to the top, i.e., after the beginning of the colonialperiod in the 16th century, corresponding to the arrival of the firstEuropeans (1500 AD). Increasing sedimentation rates confirm theradiocarbon results (e.g., Table 2) that sediment at 90 cm had anage of 530 yrs BP and sediment at 122 cm had an age of 1760 yrsBP (Barth et al., 2006).

The foraminifera assemblage was dominated by A. tepida andElphidium spp. (e.g., Fig. 2), despite the presence of the agglutinatedspecies. Microfauna distribution and TOC values along the cores,along with the sedimentation rates in the APA de Guapimirim,showed two distinct periods along the cores: one from the bottomto 90–100 cm of depth, and another from this depth to the top. TOCvalues in cores T3 and T4 are low from the bottom to the middle ofthe core (Tables 3 and 4), and they increase into the present (top),and microfauna dominance and abundance also change along thissection. At 90–100 cm of depth, the estimated radiocarbon date isapproximately 500 yrs BP (approximately 1500 AD, 16th century,at the arrival of the first Europeans). After the beginning of the col-onisation period, foraminiferal abundance values fell, as did thepresence of Elphidium, but A. tepida abundance increased higherin the core, as a response to the colonisation and later, to the indus-trial period.

4.2. São Gonçalo region

Three analysed cores, T2, T15 and T14, were positioned fromnorth to south along the coastline in front of the municipality ofSão Gonçalo. To the north, nearer the APA de Guapimirim, theoccurrence of the agglutinated T. inflata and H. wilberti in core T2(e.g., Fig. 3) confirms that there was once a mangrove forest there,which could have extended from north to northeast.

In the southern region near Niterói, at depths of 70 and 200 cmin core T14, radiocarbon dates are 550 yrs BP and 5,700 yrs BP,respectively (e.g., Fig. 3). The sedimentation rates determined byGodoy et al. (1998) increased from 0.26 cm/yrs at 48 cm depth to0.5 cm/yrs at 36 cm. In this study, the radiocarbon dating agedthe 70 cm sediment at 550 yrs BP, marking the European settle-ment, which coincides with changes in the species assemblage.

In cores T14 and T15, there was little diversity; however, thereis higher diversity in core T15 than in T14 (near Niterói) at depthsof approximately 50–150 cm (e.g., Tables 3 and 4). No agglutinated

186 C.G. Vilela et al. / Marine Pollution Bulletin 79 (2014) 175–187

species were found, but A. tepida and B. elegantissima assemblagesare dominant in the upper and bottom intervals, respectively. B.elegantissima and Elphidium spp. are present in deeper sub-samplesbelow 50 cm; therefore their disappearance marks the Europeansettlement (e.g., Fig. 3). In both cores, A. tepida is dominant in theupper centimetres, as a response to the increase in the anthropo-genic impacts.

4.3. Paquetá region

Near Paquetá Island, in core T8, the radiocarbon date at thedepth of 222 cm is 4210 yrs BP (Barth et al., 2004). Benthic foram-inifera results near the unconformity show rare abraded tests, withinfilled sediment, and yellow–brownish tests. The microfaunal andsediment characteristics at this level could be explained by a per-iod of regression in the sea level during a high-frequency oscilla-tion period, as suggested by Martin (2003). Barreto et al. (2005)found disrupted and abraded pollen and spore exines there, sug-gesting that they were air-exposed and/or reworked.

The paleoecology of the Holocene is reflected in the dominanceof A. tepida and B. elegantissima in the three analysed cores, T8, T10and T11. Their distributions are inversely proportional and suggestan increase in anthropogenic impacts. A. tepida dominates the sed-iment of the upper intervals of the cores until a depth of 40 cm, andB. elegantissima dominates in the bottom intervals (e.g., Fig. 4). TheTOC of younger sediments was higher (e.g., Table 4), and the dom-inance of A. tepida may be a response to increased TOC. Barretoet al. (2005) observed two phases, before and during the Europeaninfluence, marked by the appearance of the exotic pollen grainssuch as Pinus and Casuarina and changes from tropical forest veg-etation to herbaceous field vegetation, beginning at approximately80 cm and extending upward. Their work is consistent with thebenthic foraminifera interpretations and the increase in humaninfluence to the ecosystem.

4.4. Jurujuba region

In Jurujuba Sound, the radiocarbon date at 202 cm in core T13 is3520 yrs BP (Baptista Neto et al., 2013). Baptista Neto et al. (1999)found higher sediment rates in the upper core, as was found in theAPA de Guapimirim, São Gonçalo and Paquetá regions by Godoyet al. (1998). Therefore, there are coherent results for date and sed-iment rates among the areas. Microfaunal results can also be com-pared, with A. tepida/B. elegantissima again inversely proportional.A. tepida is dominant in younger (upper) sediments, and B. elegan-tissima in older (deeper) sediments (e.g., Fig. 5).

The increase in anthropogenic impacts can also be confirmed bythe pollen results. In the upper part of the core, down to 70 cmdepth, a significant environmental change was observed in the pol-len record (Baptista Neto et al., 2013). Changes from tropical forestvegetation to herbaceous field vegetation were observed, as wereexotic genera of Casuarina, Eucalyptus and Pinus, which were thenrecorded for the first time in the palynological data.

Overall, the integrated results from cores in Guanabara Bay con-firm A. tepida as a bioindicator of human pollution, as asserted inVilela et al. (2003). B. elegantissima is found in sediment with highorganic matter content in confined environments (Culver and Bu-zas, 1995) but, with the increase in the anthropogenic impacts inGuanabara Bay, it became less dominant as A. tepida became moredominant.

5. Conclusions

Our study of the benthic foraminifera along cores from Guana-bara Bay confirmed an increase in pollution toward the present.

The sediment rates were assessed by radiocarbon ages in variousregions of the bay. From approximately 5700 yrs BP to the present,the microfauna has reflected a restrict environment, with lowdiversity and high dominance. B. elegantissima was dominant atdeeper intervals in older sediments, with high contents of organicmatter (TOC). These results reflected a native environment beforeEuropean influence. A. tepida was confirmed as a pollution bioindi-cator, with high values of dominance in younger sediments atupper intervals that were deposited after Europeans settlement.E. excavatum was present as common species at certain intervals.Agglutinated species confirmed the presence of mangrove systemsin the past, which could have extended from north to northeast.

Although pollutants have seriously affected areas in GuanabaraBay, the process is not irreversible in those areas, as indicated bythe benthic foraminifera assemblage. Change depends on a combi-nation of government actions and the conscience of people livingaround the bay, which could initiate an environmental reconstruc-tion period in a pollution reducing or post-pollution phase.

Acknowledgements

This work was developed at the MicroCentro, Laboratório deAnálise Micropaleontológica, Federal University of Rio de Janeiro.The research was supported by CNPq (Brazilian Research Council)and the Brazilian state oil company research centre, PETROBRAS/CENPES. Special thanks are given to the undergraduate students,Raquel Medeiros da Fonseca and Kelly Costa de Abreu, who helpedwith the benthic foraminifera laboratory analyses.

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