Environmental change in Guanabara Bay, SE Brazil, based in microfaunal, pollen and geochemical proxies in sedimentary cores

Ocean & Coastal Management xxx (2016) 1e12

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Environmental change in Guanabara Bay, SE Brazil, based in microfaunal, pollen and geochemical proxies in sedimentary cores
Anto ^ nio Baptista Neto a, *, Cintia Ferreira Barreto a, Claudia Gutterres Vilela b, Jose Estefan Monteiro da Fonseca a, Gustavo Vaz Melo a, Ortrud Monica Barth c ^nea s/n, 24210-340 Nitero
i, RJ, Departamento de Geologia e Geofísica/LAGEMAR, Instituto de Geoci^ encias, Universidade Federal Fluminense, Avenida Litora Brazil b
lise Micropaleontolo ~o, 21949
rio de Ana
gica e MicroCentro, Departamento de Geologia, Universidade Federal do Rio de Janeiro, Ilha do Funda Laborato 900 Rio de Janeiro, RJ, Brazil c ~o Oswaldo Cruz, Av. Brasil 4365, 21040-900 Rio de Janeiro, RJ, Brazil Instituto Oswaldo Cruz, Fundaça a

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 October 2015 Received in revised form 29 March 2016 Accepted 14 April 2016 Available online xxx

The exponential development of human activities during the last century has caused a negative impact on all environmental compartments, including coastal areas. Guanabara Bay-SE Brazil has been subjected to significant environmental pollution from increasing urban and industrial development in the last few decades. The major sources of pollution included municipal wastewater, deforestation, urban runoff and industrial effluents. A sediment deposit constitutes a continuous record of the history of a waterbody and its catchment in a chronological sequence, where the information contained in each sediment stratum provides a more or less clearly defined image of a period in the ecosystems history. In the present study, we have investigated the environmental change in the last decades using recent sediments cores along the coastal area of Guanabara Bay. Geochemical trends in coastal sediment depth profiles have been extensively used as indicators of historical pollution, especially when combined with the analysis of biological remains (foraminifera and pollen) in sediments have provided valuable information on respective contribution of terrestrial and anthropogenic inputs into coastal bays. Three sediment cores (~200 cm long) were taken from different areas inside Guanabara bay were interpreted based on sedimentological, foraminifera, pollen, geochemical and historical data for the last 5000 years. High concentrations of metals (Pb, Ni, Cu, Cr, Zn and Mn) were observed in the three sediment cores over approximately the last hundred years. This is also matched by an increase over time in the foraminifera species Ammonia tepida and a decline in the species Buliminella elegantissima. A. tepida is commonly found in restricted and highly polluted environments, whereas, B. elegantissima is more sensitive to environmental deterioration. Pollen analysis shows a gradual decrease in forest and mangrove vegetation since the European settlement and an increase in field vegetation that has accelerated in recently, together with the introduction of exotic species. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Guanabara bay Heavy metal Foraminifera Pollen Environment evolution

1. Introduction Contamination of the aquatic environment has become a serious problem in many coastal areas of the world (Cearreta et al., 2002). According to Goto and Wallace (2010) urban coastal habitats are often degraded from a variety of anthropogenic disturbances, which can be physical (e.g., trawling), chemical (e.g., chemical

* Corresponding author. E-mail addresses: [email protected] (J.A. Baptista Neto), cintiapalino@yahoo. com.br (C.F. Barreto).

discharges), and biological (e.g., invasive species) (Able and DuffyAnderson, 2006; Levin et al., 2001). Among these stressors, elevated levels of widespread chemical pollutants such as trace metals can have especially persistent effects on aquatic organisms (Lindegarth and Underwood, 2002; Savage et al., 2001). Metals are natural constituents of the marine environments which are generally found in low concentrations (Ansari et al., 2004). Metals introduced by human activities into the marine environment accumulate in sediments and are therefore useful indicators of anthropogenic inputs. Metals enter the marine environment through a variety of point and diffuse sources (Kramer and

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Please cite this article in press as: Baptista Neto, J.A., et al., Environmental change in Guanabara Bay, SE Brazil, based in microfaunal, pollen and geochemical proxies in sedimentary cores, Ocean & Coastal Management (2016), http://dx.doi.org/10.1016/j.ocecoaman.2016.04.010

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Botterweg, 1991; He and Morrison, 2001), most notably riverine influx (Forget et al., 2003), atmospheric deposition (Williams et al., 1998) and/or anthropogenic activities (Cheevaporn and Menasveta, 2003). According to Cukrov et al. (2011) a fundamental characteristic of trace metals is their lack of biodegradability. Once introduced into the aquatic environment, trace metals are redistributed throughout the water column, deposited or accumulated in sediments and consumed by biota. However, sediments are not only a sink but also a possible delayed source of these contaminants into the aquatic phase due to desorption and remobilization processes (Fichet et al., 1998; Long et al., 1996). Clearly, sediments constitute a long-term source of contamination to the food web (Burton, 2002). Sediment cores are environmental archives of past anthropogenic pollution, and the study of heavy metal profiles in undisturbed sediments can provide a complete record of temporal contamination history (e.g. Nriagu, 1979; Weiss et al., 1999; Smith, 2001; Cundy et al., 2003; Morelli et al., 2012). Although, at international level, studies mainly have focused on surface sediments, which are useful for monitoring changes in current environmental tendencies, core sediments allow to reconstruct the historical input of pollutants and their impact in the ecosystem (Rodríguez-Obeso et al., 2007). Furthermore, coring techniques can allow reaching unimpacted sediments, providing reference conditions based on environmental reconstructions as proposed by Andersen et al. (2004). According to Monteiro et al. (2012) in Guanabara Bay, the use of dated sediment profiles is scarce (Godoy et al., 1998; Baptista-Neto et al., 1999, 2013) and multi-proxy approaches have not been carried out to elucidate the historical environment changes in this coastal system. According to Coccioni et al. (2009) over the last few years, many studies of benthic foraminiferal assemblages have been carried out in different parts of the world, in areas exposed to different kinds of marine pollution. Through these studies, a considerable effort has been made to develop new methodologies for the biological monitoring of different contaminants. Moreover, because of increased knowledge of the biology of foraminifera, these studies have revealed that benthic foraminifera have great potential as indicators of pollution, thereby providing one of the most sensitive and inexpensive markers of environmental stress in both naturally and anthropogenically stressed locations (Murray and Alve, 2002). 1.1. Studied area Guanabara Bay is in Rio de Janeiro State - Southeast Brazil, between 22
400 S and 23
000 S of latitude and 043
000 e043
180 W longitude (Fig. 1). It is one of the largest bays on the Brazilian coastline and has an area of approximately 384 km2, including it islands, surrounded by industrial and densely populated areas in southeastern Brazil. According to Amador (2012) the coastline of the bay is 131 km long; the mean water volume is 1.87  109 m3. The bay measures 28 km from west to east and 30 km from south to north, but the narrow entrance to Guanabara Bay is only 1.6 km wide (Kjerfve et al., 1997). Guanabara Bay lies within the tropics of south eastern Brazil, but because of its coastal location a humid sub-tropical climate with 2500 mm (high altitudes) and 1500 mm (low altitudes) of rainfall prevails between December and April. The mean annual temperature is between 20
and 25
C (Nimer, 1989). Guanabara Bay has a complex bathymetry with a relatively flat central channel. The channel is 400 m wide, stretches from the mouth more than 5 km into the bay, and is defined by the 30 m isobath. The deepest point of the bay measures 58 m and is located within this channel (Kjerfve et al., 1997; Melo et al., 2014). Ac
i bridge, cording to the same authors, north of Rio de Janeiro-Nitero the channel loses its characteristics as the bay rapidly becomes shallower, with an average depth of 5.7 m, due to the high rates of

sedimentation, accelerated in the past century by anthropogenic activities in the catchment area. Nowadays, 11 million inhabitants live in the greater Rio de Janeiro metropolitan area, which discharges tons of untreated sewage directly into the bay. The second largest industrial site of Brazil is found in this area. There are more than 12,000 industries in the drainage basin which account for 25% of the organic pollution released to the Bay. The bay also hosts two oil refineries along its shore, which processes 7% of the national oil. At least 2000 commercial ships dock in the port of Rio de Janeiro every year, making it the second biggest harbour in Brazil. The bay is also the home port to two naval bases, a shipyard, and a large number of ferries, fishing boats, and yachts (Kjerfve et al., 1997). The hydrographic basin is drained by a total of 45 rivers, 6 of them responsible for the 85% of the mean annual fresh water discharge (Baptista Neto et al., 2006). The bay receives the untreated agricultural runoffs and the urban and industrial sewage from the rivers, from the Rio de Janeiro metropolitan area, from two harbors, from refineries, from the thousands of industries in the surrounding basin and from the atmospheric fallout (Kjerfve et al., 1997; Baptista Neto et al., 2006). 1.2. Methodology Three sediment cores, varying from 140 to 240 cm in length, were collected, using a PVC tube with the percussion method, in three distinct areas of Guanabara Bay (Fig. 1) and analyzed for microfauna contents, pollen, heavy metal, C and N. The areas include the mangrove system APA (under protection area) de ~o Gonçalo municipality to the northGuapimirim to the north; Sa enortheast, where the mangrove forest is nearly completely destroyed; and Paquet
a Island, also northe north eastern (Fig. 1). The selection of the locations for the sediment cores that were likely to be less disturbed based on high resolution seismic (3.5e7.0 kHz) reflection patterns (Catanzaro et al., 2004). Six samples were taken from the core for radiocarbon dating and submitted to the BETA Analytic Radiocarbon Dating Laboratory in Florida, United States of America. The dates were calibrated using CALIB 5 (Stuiver et al., 2005). Particle size analysis was carried out using a Malvern Mastersizer Microplus, MAF 5001. Sub-samples for chemical analysis were oven dried between 30 e 35
C since extractable metals were examined and passed through a 2 mm diameter nylon mesh sieve (Hesse, 1971). The <63 mm fraction was collected by further sieving a representative portion of the <2 mm fraction through a nylon mesh. This size fraction was analyzed as it is relatively undiluted by coarser sizes and allows a more accurate €rstner prediction of the threat to an ecosystem by heavy metals (Fo and Wittmann, 1983). Samples were digested in aqua regia under pressure using a Perkin Elmer microwave digestion system. Sample blanks and a reference sediment WQB-1 from the National Laboratory for Environmental Testing, Burlington, Canada was also analyzed at regular intervals to monitor quality control. Sample extracts were filtered into acid washed high-density polyethylene (HDPE) containers and diluted to a volume of 25 ml in deionizer water. Analytical standards were prepared by diluting a1000 mg/l BDH stock solution that is traceable to the NIST Certified Reference Institute. Elemental analysis (Pb, Zn, Ni, Cr, Cu, Mn & Fe) was carried out using a Perkin Elmer Model 200 atomic absorption spectrophotometer. Sediment sub-samples were collected at centimeter intervals from the bottom to the top of the core for microfaunal analyses. Sample pretreatment for microfaunal studies involved washing, wet sieving through a 0.063 mm-mesh sieve, drying in an oven and suspending in a dense liquid sodium tungstate (Na2WO4) solution. After the treatment the samples were picked, counted and classified at the benthic foraminifera species level. Genera determination

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Fig. 1. Location map with the position of the cores.

followed the method of Loeblich and Tappan (1988), and species

classification were based on classic works which including the

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catalogue of Ellis and Messina (1940), and several other specific articles. Benthic foraminifera occurrence was evaluated by considering the characteristic distribution per interval in the core. A minimum of 100 specimens per sub-sample were taken at intervals from the core and counted to achieve accurate statistical analysis of the results. Species with a relative abundance of 10% or higher were considered dominant (Boltovskoy and Totah, 1985). Samples were collected at intervals of 10 cm for pollen analysis and chemically treated following the standard methodology for Quaternary sediments proposed by Ybert et al. (1992). A minimum of three slides was prepared in a glycerin jelly medium and at least 300 pollen grains per sample were counted. Pollen identification used pollen catalogues, specific papers, and comparison to a reference pollen collection of the Palynology Laboratory, Federal University of Rio de Janeiro (UFRJ). The core T-4, was analyzed by Barth et al. (2006). 2. Results and discussions 2.1. Sediment core characteristics The sediment analyses in the cores showed colours varying from black to dark or olive grey. Muddy sediments with silt laminations and a lens of organic matter were dominant in the top intervals.
Island, in core T8, there was an abrupt contact or an Near Paqueta erosive surface at the bottom, with coarse particles in a hard mottled and brownish clay. The deposits near that contact, at 222 cm, were radiocarbon dated to 4210 ± 40 yrs BP (Barth et al., 2004). 2.2. Organic matter and C/N ratio Organic matter (OM) origins in coastal waters are highly diverse. They can come from autochthonous sources such as phytoplankton, micro algae and aquatic macrophytes and also from allochthonous sources such as terrestrial vegetation, freshwater marshes and organic pollution from the upper parts of the hydrological basin. The weight ratio of total organic carbon to total nitrogen (C/N ratio) is often used as an indicator of the source of organic matter (OM) in aquatic sediments (Sampei and Matsumoto, 2001). It has also been used for tracing mangrove OM transfer through estuarine food webs (Newell et al., 1995; Loneragan et al., 1997; Bouillon et al., 2000; Lee, 2000; Chong et al., 2001) and, in conjunction with other tracers, mangrove OM export to coastal sediments (Cifuentes et al., 1996; Dittmar et al., 2001). Some authors suggest different values of the C/N ratio according to the origin of the OM. Proteins, which are the primary nitrogen compounds of phytoplankton and zooplankton, have C/N ratios of 5e6 (Bordowskiy, 1965a,b). Freshly-deposited OM, derived mainly from planktonic organisms, has a C/N ratio of 6e9 (Bordowskiy, 1965a; Prahl et al., 1994; Biggs et al., 1983). In contrast Saito et al. (1989) suggested a ratio greater than 20 for a terrestrial origin. For example, the average C/N ratios for wood, leaf and macrophyte material in the watershed area of the Amazon River are 179, 24.1 and 39.4, respectively (Hedges et al., 1986). Higher plants are the main organic producers in the terrestrial environment, and consist mainly of cellulose and lignin, which contain few nitrogen compounds. Other important external inputs, such as those from agricultural activities associated with the geochemical transformations, can modify C:N:P ratios and biomarker C/N, masking the identification of the origin of organic matter, as happens in the coastal lagoon complex in the California Gulf of Northwest Mexico (Altata Bay and
n lagoon), where approximately 6279 tons of Ensenada del Pabello nitrogen and 7316 tons of phosphorus are used annually as

fertilizers on sugar cane fields (Lanza Espino et al., 2011). In the present study C/N ratio average values varied between 9.77 and 14.30. Stein (1991) demonstrated that values of approximately 10 indicate components of both marine and terrestrial origins in the sediment (Table 1). Studies using C/N ratios as tracers of different OM end member sources show that this ratio can be altered by many processes, including ammonification, nitrification and denitrification (Matson and Brinson, 1990; Thornton and McManus, 1994; Cifuentes et al., 1996; Andrews et al., 1998; Yamamuro, 2000; Graham et al., 2001). In the present study it wasn't found any clear tendency pattern of the C/N ratio variation along the cores (Table 1), although the results found in the deepest layers seemed to be lower than the others. Increases in C/N ratios of sedimentary OM, relative to the source, over time or with depth in a core, which are commonly observed, have been interpreted as indicative of preferential loss of nitrogen (N) (Andrews et al., 1998), while little change suggests that C and N are mineralized or preserved at the same rate. In the other hand, decrease of C/N ratio can be explained as a result of the absorption of organic or inorganic N onto silicate clay surfaces (Macko et al., 1993) or the incorporation of N by bacteria in decaying OM (Cifuentes et al., 1996). 2.3. Pollen The pollen analyses in dated sediment cores has been pointed out as one of the most reliable source for examining the changes in plant species diversity and abundance and thus reconstructing vegetation and climatic history. The pollen signal is particularly useful for analyzing the dynamic relations between land use and environmental change (Cao et al., 2010). Palynological analyses of Holocene sediments from Guanabara Bay meant an important step to characterize the vegetation that occupied the lands of the watershed of the bay. The accounts left by the landscape of the colonial period was a lush forest (Barreto et al., 2007, 2015). However, currently, the Atlantic Forest extremely fragmented, is reduced to discrete spots, mainly located in rugged topography, inadequate agricultural activities and preserved only in protected areas (Kurtz and Araújo, 2000). According to Veloso et al. (1991) and RADAMBRASIL (1983), the lands of the Serra do Mar was covered by a dense Ombrophylous forest (tropical rainforest) mainly in the mountain slopes. The Ombrophylous forest which is characterized by Drimys brasiliensis, Ocotea, Gordonia. Down the relief it is possible to observe that the Ombrophylous forest is characterized by the occurrence of Pordocarpus and some genera of Lauraceae (Ocotea and Nectandra) and the Ombrophylous Forest Submontane with the presence of Hieronyma, Didymopanax, Chrysophyllum, Pouteria and Alchornea. The coastal plain with Ombrophylous Forest of the Lowlands occurring mainly genres of Ficus, Alchornea, Tabebuia and Tapiria Guyanese. On the banks of the rivers that cross the coastal plain is the dense Ombrophylous alluvial Forest with Tapirira Guyanese, genera of Arecaceae (Mauritia and Euterpe) and Callophyllum Brasilienses occupying the flood plains temporarily by the flow of rivers. Upon reaching the bay is the mangrove vegetation, mainly preserved in the eastern sector of the bay, in the Environmental Protection Area of Guapimirim (Apa Guapimirim). Its vegetation is

Table 1 C/N ratio average values. Core

Core 4

Core 8

Core 14

C/N ratio average values

14.30

10.50

9.77

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mainly characterized by the presence of the species such as Rhizophora mangle, Avicennia nitida and Laguncularia racemosa. Other species also occur in the area, such as Hibicus, Acrostichum and Spartina (Araújo and Maciel, 1979; Amador, 2012). The significant presence of the pollen types which are representative of tropical rainforest were Observed in core T-4 located near the mangroves of the APA Guapimirim (22
410 1000 S and 43
040 5900 W) (Fig. 2). The high frequency of pollen types of mangrove the circa 1760 þ 50 yr BP, represented mainly by pollens of Rhizophora, followed by Avicennia and Laguncularia, it indicates the presence of a mangrove well developed in the inner area of the Guanabara Bay (Barth et al., 2006). The pollen analysis carried out in the sediment cores allowed the environmental fluctuations characterization of the last 6000 cal years BP. The pollen analytical results from a sediment ~o Gonçalo coastline (core T-14) record core collected near the Sa document the dominance of pollen types of the Ombhophylus florest (Fig. 3), with 116 pollen types identified, being 58 arboreal, suggested that the large part of the Guanabara Bay hydrographic basin and in its close neighbourhood were covered by rain forest during at 6486 cal yr BP (pollen zone base I). Probably, the climate conditions was wetter, indicated by high frequent spores associated with abundant arboreal components, low frequent herb and indicated also by the low frequency in charcoal records. The below deposition of the pollen and spores grains in 6486 cal yr BP (pollen zone base 1), may still be controlled by the Holocene transgressive maximum event. This event, submitted the central part of Brazil to a phase of submergence, elevating the line of coast to 4e5 m above ^ present (Martin, 2003, Angulo et al., 2006). During this period, the water surface of Guanabara Bay came to measuring approximately 800 km2 (Amador, 2012). This environmental change possibly altered and modified circulation patterns that may be difficult the deposition of pollen types of vegetation more dense forest located on the slopes of the mountain from the sea. In this period, the Rio de Janeiro coast was inhabited by people who occupied part of the Guanabara Bay during the Holocene transgressive event, evidenced by archaeological records revealed by the presence of sambaquis who witness the intense occupation of the region, including the sambaqui of Sernambetiba (Beltran et al., 1981/82) and Vale das Pedrinhas (Mendonça de Souza and Mendonça de Souza, 1981/82),
, in the coastline of Guanabara Bay, as well as the lower both in Mage levels of the sambaqui of Camboinhas (Kneip et al., 1981), on the
i. These people occupied part of Guanabara coast of Itaipu, Nitero Bay in the last 8000 years, throughout the Holocene transgressive event sea level (Beltran and Kneip, 1967; Mendonça de Souza and

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Mendonça de Souza, 1981/82). In circa 4210 þ 40 anos AP was an observed a major fall in palynomorph concentrations and the wide-ranging deposition of degraded pollen and spore grains, together with the occurrence of
Island, an erosive contact layer in this T8 core (near Paqueta 22
440 46600 S and 043
060 75700 W) (Fig. 3). This palymonorphs degradation can probably be related to the retreat of the sea level event after the maximum transgressive Holocene until about ^ 5300 cal yr BP (Martin, 2003; Angulo et al., 2006). This event caused erosion periods at river mouths that provide the high deposition of degraded palynomorphs. The predominance of the Ombrophilous forest, and the richness of the Alchornea, Banara, Cecropia, Celtis, Lecythis, Meliaceae, Piperaceae and Trichilia pollen types (Fig. 3), confirm the existence of an exuberant Atlantic forest in the region at this time (Barreto et al., 2007; Barth et al., 2004). The high concentrations of Alchornea, Celtis and Cecropia pollen grains indicate that these plants probably expanded and colonized the spaces opened up by the sea level regression (Barth et al., 2001; Luz et al., 1999). A second stage of human occupation occurred in the Guanabara region, evidenced by changes in the archaeological record and were related by Dias Jr. (1977) The Itaipu Phase A. These groups occupied a coastal area where the construction of coastal sand bars, lagoons isolation and development of mangrove due to the retreat of the sea level and coastal progradation (Amador, 2012). This sea level regression was documented in the northeast portion of Guanabara Bay around 4000 years BP. It is indicated by increase in the accumulation patterns of pollen and spore grains in the T-14 core (Fig. 4). This facilitated the transport of pollen and spore grains from the Guanabara Bay hydrographic basin to the study area. The sea level retreat can be observed in the reduction of the Ombrophilous forest vegetation and a small increase in the open vegetation. The small rise in pioneiros pollen types (open vegetation) such as Borreria, Diodia, Cyperaceae, Scoparia, and Apiaceae suggests an increase of open areas, which probably indicates the retreat of the shoreline (Souza and Lorenzi, 2005; Lorenzi, 2000). The intense human occupation can be clearly observed in the analyzed cores (T4, T8, and T14). This can be inferred from the significant reduction in the Ombrophilous forest pollen grains and the significant increase in the pollen grains of the herbaceous vegetation of the country. This vegetation is mainly represented by the pollen types Amaranthus/Chenopodiaceae, Borreria densiflora, Borreria latifolia, Brassicaceae, Chamaesyce, Diodia and Poaceae, which indicate an anthropized area and secondary vegetation (Figs. 2e4). The presence of exotic pollen types such as Eucalyptus

Fig. 2. The heavy metal concentration profiles and Vertical distribution of trace fossils (foraminifera and pollen) of the sediment core T-4.

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Fig. 3. The heavy metal concentration profiles and Vertical distribution of trace fossils (foraminifera and pollen) of the sediment core T-8.

Fig. 4. The heavy metal concentration profiles and Vertical distribution of trace fossils (foraminifera and pollen) of the sediment core T-14.

and Pinus indicates the reforestation of deforested areas and cultivation for the production of cellulose. Pinus was introduced into Brazil and expanded in the southeastern region during the period 1967e1982 (Ahrens, 1987). Deforestation in the Guanabara region, dating from the late 16th century with European colonization mainly around large monocultures, started with cane sugar, which expanded across almost all of the lowlands and was controlled by large landowners (Amador, 2012). 2.4. Heavy metal Sediment cores are environmental archives of past anthropogenic pollution, and the study of heavy metal profiles in undisturbed sediments can provide a complete record of temporal contamination history (e.g. Smith, 2001; Cundy et al., 2003). Most of our current knowledge on the history of metal pollution is based on studies of sediment cores from lakes and coastal areas (Morelli et al., 2012). Furthermore, coring techniques can allow reaching unimpacted sediments, providing reference conditions based on environmental reconstructions as proposed by Andersen et al. (2004). The advantage of this methodology is that it provides in

situ reference values, avoiding the great variability among different estuarine systems (Chapman and Wang, 2001). Guanabara Bay is considered one of the most polluted coastal bay in Brazil, fortunately, this contamination is receiving increasing attention from both the scientific community and governments at local and international levels. However, many studies mainly have focused on surface sediments (Fonseca et al., 2013; Donnici et al., 2012; Covelli et al., 2012; Baptista Neto et al., 2006, 2005; Rebello et al., 1986), which are useful for monitoring changes in current environmental tendencies. On the other hands, in the last few years some studies started to be carried out in differents sectors of Guanabara Bay, using dated sediments cores, for different purposes (Barreto et al., 2007, 2015; Barth et al., 2004; Godoy et al., 1998; Carreira et al., 2002; Baptista Neto et al., 1999, 2013; Figueiredo et al., 2014; Cordeiro et al., 2015, Vilela et al., 2014). Since most industrial and domestic discharges to Guanabara Bay are confined to the second half of the century, one would expect significant differences in the compositions of sediment at the top and bottom layers of the cores. The vertical distribution of all analyzed metals in the three sediment cores from Guanabara Bay is shown in Figs. 2e4. The temporal evolution of these elements is

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characterized by a strong variability. The total concentration of Cu, Pb, Zn, Cr and Ni of the sediment core 04 (Fig. 2) ranged from 16 to 192.5, 21 to 87.5, 50 to 187.5, 55 to 442.5 and 55 to 68.75, respectively, with an average of 100; 48, 122, 241 and 60, respectively. The total concentration of Cu, Pb, Zn, Cr and Ni of the sediment core 08 (Fig. 3) ranged from 7.5 to 50, 25 to 383.8, 37.5 to 200, 35 to 93.7 and 35 to 70, respectively, with an average of 23, 158.7, 117.5, 66 and 51, respectively. The total concentration of Cu, Pb, Zn, Cr and Ni of the sediment core 14 (Fig. 4) ranged from 18 to 190, 35 to 190, 50 to 190, 55 to 430 and 55 to 70, respectively, with an average of 104.6; 64.7, 125, 248 and 62, respectively. The heavy metals distribution was characterized by an increasing trend towards the surface with two distinct peaks, the first one slightly at the depth of 110e150 and the second one, strong 50e60 cm toward the surface. The metals also exhibited values gradually decreased from the depth of 150 cm towards to the base of the core until reaching the values as low as in the background. Highly concentrations of heavy metals in the upper part of the sediment cores are commonly reported as having a strong correlation with organic matter content and small sediment particle size (Salomons and Forster, 1984). Throughout the sediment core particle size distribution was very homogeneous and showed a predominance of very fine particles (silt and clay), it is possible to observed that the increasing concentrations of heavy metals in the middle part to the top of the cores coincides with the above mentioned change in pollen content. However, in the upper part of cores, the highest concentrations of metals are related with the beginning of the urbanization and industrialization in the Guanabara Bay catchment, this pattern was also observed in Jurujuba Sound, inside of Guanabara Bay, by Baptista Neto et al. (2013). The increase in the heavy metal concentration in the upper part of the sediment cores, are very similar to the pollen analyses, showing that the heavy metal enrichment followed the deforestation of the area.

influence. The element Ni was showed natural concentration throughout the entire core. For all metals in this core the concentrations were lower or equal to 1 at the depth of 100 cm to the base of the core, which indicates that the natural inputs prevailed up to this period. On the other hands, a very high Cu and Cr enrichment characterized the depth of 100 cm to the upper part of the core with maximum EF value up to 9.2 and 4.7, respectively. Cu is known for its high affinity for humic-substances, which represent a major part of organic matter in recent sediments and also this area is closed to the mangrove area. The sediment core 14 (Fig. 5), showed the same pattern of the core 4 (Fig. 5), where the elements Cu and Cr present a very high enrichment toward to the top of the core, with two phases of the enrichment, from 150 to 100 cm, where the concentrations stabilized between 100 and 50 cm, with the EF around 6, for Cu, and the upper part of the core where the EF for Cu reached > 8.1. The same pattern was observed for the element Cr, with lower values. The other elements such as Zn and Pb shows values around 1, however it is possible to observe a slightly enrichment toward to the top. The area where this core was collected is closed to the S~ ao Gonçalo coastline, which experienced in the last 70 year great land reclamation, it is probably affected the rates of sedimentation in this site, and also the majority of the rivers that flows to this area in reality act as a open sewage system, this municipality has more than 1 million inhabitants, without sewage treatment.

2.5. Normalization of the geochemical data

Igeo ¼

The heavy metal variability of sediments may be natural or influenced by anthropogenic sources. In order to reduce the mineralogical and grain-size variations of heavy metals, a common approach is to normalize the geochemical data using one element as a grain-size proxy, e.g., Al, Fe, Sc, Cs, and Li (Audry et al., 2004; Baptista Neto et al., 2006; Aloupi and Angelidis, 2001; RuizFernandez et al., 2004). Al, Li and Fe were already used in Guanabara Bay (Baptista Neto et al., 1999 and Baptista Neto et al., 2006) as a conservative element. For this study, Iron was chosen for this purpose due to the similarities in the geochemistry of Fe and many heavy metals in both oxic and anoxic conditions, which can compensate the diagenetic mobility of heavy metals to some extent (Schiff and Weisberg, 1999) and this metal has also been used by other authors as a normalization element (Tanner et al., 2000; Liu et al., 2002; Varol, 2011). The depth profiles of EF for Zn, Cu, Pb, Cr and Ni generally showed values above 1 from the depth of 150 cm to the upper part of the sediment cores (Fig. 5), which confirming the pollution of the Guanabara Bay sediments, in the recent decades. Over the last 70 years there has been an increase in the heavy metal contamination, which may be attributed to developing of urbanization, industries and increased untreated sewage discharge. It is possible to distinguish two phases of heavy Metal EF, where the greater Cu, Zn and Pb pollution, with EF values > 1.5, occurred at depth higher than 50 cm (Fig. 5). In the sediments core 4, it is possible to observe a slight enrichment of Zn and Pb (maximum 1.5- and 1.4-fold, respectively). Despite the EF values for Zn and Pb were lower than 1.5, their profiles showed a slight but consistently increasing trend from the upper part of the core, indicating some anthropogenic

2.6. Geoaccumulation indices In order to compare present day heavy metal concentration with pre-civilization background values, and for a quantitative measure of possible contamination in the studied sediments, an “index of geoaccumulation” (Igeo) is used, as introduced by Müller (1979). This index is defined as:

Log2 ðCnÞ 1:5Bn

where Cn is the measured concentration of the element n in the fine sediment fraction and Bn represents the geochemical background concentration of element n. Factor 1.5 is the background matrix correlation factor due to lithospheric effects. The geoaccumulation index consists of seven classes (Müller, 1979). Class 0 (practically unpolluted): Igeo  0; Class 1 (unpolluted to moderately polluted): 0 < Igeo < 1; Class 2 (moderately polluted): 1 < Igeo < 2; Class 3 (moderately to heavily polluted): 2 < Igeo < 3; Class 4 (heavily polluted): 3 < Igeo < 4; Class 5 (heavily to extremely polluted): 4 < Igeo < 5; Class 6 (extremely polluted): 5 > Igeo. Overrall, the Igeo values of the heavy metal reflected the general contamination tendency already observed in the EF values, and hence, the area can be considered moderated polluted to heavily polluted for the majority of the heavy metal, and heavily to extremely polluted mainly for Cu and Cr in the upper part of the three cores and heavily to extremely polluted for Pb in the core 8, located closer to an oil terminal (Fig. 5). 2.7. Adverse Effect Index (AEI) According to Hamdoun et al. (2015) calculated enrichment factors cannot be used to evaluate the probability of adverse effects on ~ oz-Barbosa et benthic biota. In the absence of toxicity studies, Mun at. (2012) suggest that element concentrations can be compared with Threshold Effect Level (TEL) sediment quality guidelines (SQG) developed by Long et al. (1996) in order to assess an Adverse Effect Index (AEI). Tel SQGs were developed in order to interpret metal concentrations in sediments in the context of their potential

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J.A. Baptista Neto et al. / Ocean & Coastal Management xxx (2016) 1e12

Fig. 5. Heavy metal normalization in cores from Guanabara Bay (Cores T-4, T-8 and T-14), together with Geoaccumulation indices and Adverse Effect Index in the cores.

biological effect. AEI values were calculated by the of the equation proposed by ~ oz-Barbosa et al. (2012) (AEI ¼ [X]/[TEL]). The Threshold Effect Mun Levels (TELs) used in the calculation of AEI values were derived by ~ oz-Barbosa et al. (2012), if Long et al. (1996). According to Mun AEI  1 the metal concentration in the sample is not high enough to produce adverse effects in biota, however if AEI  1 the metal concentration in the sample could produce adverse effects. These results shown in Figure suggest adverse biological effect for all the metals in the upper part of the core. However, core 4 and 14 (Fig. 5) shows the same pattern with the element Cu with an AEI values exceeding 10, and in core 8 (Fig. 5) only the element Pb reach an AEI values above 10. The AEI values are very similar to the pattern of the EF values and also to the Igeo values. The elements with the highest AIE values were Cu, Pb and Ni. It, is important to

highlight that the element Zn showed a very important enrichment in the upper part of the three cores (Fig. 5), however, its AEI values was not very important compared with the others elements.

2.8. Foraminifera in the sediment core According to Romano et al. (2013) foraminifera are protozoa constituting the most diverse group of shelled microorganisms in modern oceans (Sen Gupta, 1999). Due to their short life-cycle, abundance, wide distribution in marine and transitional environments, the ease with which they can be collected, and the fact that they leave a record of past conditions in sub-recent and fossil sediments, they may be considered as excellent ecological indicators. According to Barras et al. (2014) the main advantage of foraminifera is the conservation of a large part of their tests (Shells)

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J.A. Baptista Neto et al. / Ocean & Coastal Management xxx (2016) 1e12

in the sediment after their death. The study of dead faunas at different depths in the sediment can give important information about the natural conditions which existed before a site become polluted. Figs. 2e4 presented Zn, Cu and Pb indexes with increased values
Island and from the 50 cm to the top. In both cores, near Paqueta ~o Gonçalo area respectively, Ammonia tepida and Buliminella Sa elegantissima are inversely proportional. A. tepida tended to be abundant and dominant at shallow intervals until 40e50 cm, and B. elegantissima at deeper intervals. Radiocarbon dates in the middle of the S~ ao Gonçalo core, with the inversely proportional distribution of A. tepida and B. elegantissima, marks the European settlement (Vilela et al., 2014). A. tepida and B. elegantissima are used as proxies in bays and lagoons with high pollution levels, but coastal areas such as estuaries are complex and each has its own environmental characteristics. Consequently, as pointed out by Murray and Alve (2002), understanding the pre-pollution baseline through the sedimentary record and microfossil content is important to the analysis of recent environmental changes and anthropogenic impacts. These species are tolerant with the increase of pollution levels. Areas affected by sewage outfalls are dominated by organic-tolerant species such as Buliminella elegantissima (Bandy et al., 1965; Collins et al., 1995). With the increase of high indexes of heavy metals contents, foraminiferal microfauna respond with the dominance of opportunistic species such as A. tepida (Collins et al., 1995; Vilela et al., 2004). In the Rodrigo de Freitas Lagoon, high levels of heavy metals favored the presence of A. tepida as the most abundant species (Vilela et al., 2011). The inversely proportional distribution of A. tepida and B. elegantissima in the studied cores at the Guanabara Bay showed the presence of A. tepida as a response to anthropogenic impacts and high values of heavy metals. Buliminella elegantissima was dominant at deeper intervals in older sediments, with high contents of organic matter, but in a native environment before European influence (Vilela et al., 2014). The final interpretation of the environmental and depositional histories of the Guanabara Bay area are summarized in Table 2, which also shows the importance of the use of multiple proxies to observe the depositional differences between the periods and to highlights the human impact record in the depositional history of the bay. The Table 2 showed that the beginning of deforestation started before the input of heavy metals in this area. However, the

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foraminifera species showed the same pattern observed in the heavy metals concentrations, indicating a strong correlation between then. An increase in the A. tepida species along the enrichment of the heavy metals, highlighted the importance of these species as a proxy for studying the effects of human impact in a coastal area. Results would also indicate that association between these proxies is a very efficient means of highlighting the effects of human impact in the area. In terms of management and conservation value this study has shown that nearshore sedimentation can be a very useful tool in examining the growing impacts of urbanization in Rio de Janeiro. As with many third world countries, the lack of planning in the processes of occupation and urbanization of coastal areas, may generate or aggravate environmental problems. Such bay are experiencing rapid urbanization as the coastal hills of the hinterlands are already being cleared for cultivation. The impact of untreated sewage input and also several impact inside of the bay and in the catchment. Guanabara Bay has been on a worldwide spot due to its environmental conditions since the city of Rio de Janeiro has been chosen to host Olympic games, which will take place in 2016, and part of the games will take place inside of the Guanabara Bay. In anthropogenically modified systems, such as Guanabara Bay, an appropriate management are a very complex activity, coastal management requires a good knowledge of the natural and anthropic processes that affect the evolution of the bay, which is very difficult to achieve without a good database. The lack of baseline studies and insufficient understanding of coastal environmental evolution can brought misjudgment on the environmental impact of coastal development and also makes it difficult for the future coastal environmental management. Nowadays the appropriate management of coastal areas is an unavoidable task in order to develop a sustainable society. The current environmental problems of Guanabara Bay are well studied, however there are still very few studies related to sediment cores, which makes the understanding of their evolution and the human impacts in the area, since the arrival of the Europeans, too difficult to achieve. In this study, the combination of multiples proxies proved to be an efficient tool for the understanding of these environmental impact in the bay, and also it is represent a good baseline for an appropriate management project. Since observing past human activities and their influences on the coastal evolution is an important part of the research and an appropriate management project.

Table 2 Environmental history of Guanabara Bay and associated depositional history in relation to land-use changes. Main episodes Late 20th-century urbanization

Land use change

The intense human occupation can be clearly observed in the pollen analyses. Expressive increase in the herbaceous pollen from the grassland formations, which is associated with the appearance of exotic taxa that occupied the large deforested areas. The pollen record shows a significant reduction 16th-century, European arrival in the Ombrophilous forest pollen signature and a significant increase in the herbaceous pollen and selective signature. These changes suggest that the logging of catchment area Atlantic rainforest was strongly reduced during this period, attesting the influence of the European arrival Mid-Holocene, Significant presence of tropical rainforest pollen 5700 yrs BP types, suggesting that this vegetation occupied extensive regions of the Guanabara Bay hydrographic basin, covering the hillsides of the coastal mountain ranges, the alluvial plain and its countless islands.

Heavy metal pollution

Foraminifera

The B. elegantissima which is an organic-tolerant Rapid upward increase in heavy metal species disappeared with the great concentration in association with the rapid industrial and urbanization development in the concentrations of heavy metal and allowed the occurrence of A. tepida which is abundant and metropolitan area of Rio de Janeiro and dominant as an indication of human pollution. consequent anthropogenic metal input. The beginning of the input of heavy metal associated with the increase in sedimentation rates due to the topsoil erosion from the deforested slopes.

The dominance of B. elegantissima starts to decrease in association with the first occurrence of A. Tepida.

This period represents the baseline period, with low concentrations of heavy metal associated with slow accumulation of mud from background (Geological) erosion of forested catchment area.

B. elegantissima is the most abundant species in these sediments with high contents of organic matter, but in a native environment before European influence

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3. Conclusions The great human activities in the metropolitan area of Rio de Janeiro during the last century has caused a negative impact and changes on all environmental compartments, including the coastal areas. Guanabara Bay sediments clearly recorded all the environmental modification in its catchment. The pollution history from increasing urban and industrial development of the metropolitan area of Rio de Janeiro has been recorded by the sediments. Three sediment cores (~200 cm long) were taken from different areas inside Guanabara bay were interpreted based on sedimentological, foraminifera, pollen, geochemical and historical data for the last 5000 years. The use of multi-proxy geochemical indicators combined with biological remains (pollen and foraminifera) were a very good tool to understanding environmental change and increased pollution in the Guanabara bay. The present study showed that the core sediments collected from Guanabara Bay had similar texture and grain-size distribution, being dominated by clay and silt with high levels of organic matter content. The major changes occurred in the sediment sources in the last centuries. The environmental history of Guanabara can be classified into three main stages. The first one represents the baseline period, prior to the European arrival, with the predominance of Ombrophilous forest, the occurrence of Bulliminella elegantissima as the main foraminifera species and low concentrations of heavy metal. The second stage represent the beginning of the European colonization, with deforestation, decrease in the Ombrophilous forest, and increased in the grassland (herbaceous field vegetation), the occurrence of A. Tepida as indicator of human pollution, and also an increased in the levels of heavy metals. The third stage are related to the last century to nowadays, the pollen analyses revealed great changes in the vegetation, with the decreased in the Ombrophilous forest and increased in the grassland (herbaceous field vegetation) and the occurrence of exotic genera of Casuarina, Eucalyptus and Pinus. In this period it is also possible to observe a change in the dominance of B. elegantissima, which occur normally in sediments with high levels of organic matter content in confined environment, to the dominance of A. tepida, which confirmed to be tolerant to the increased values of heavy metal concentrations and can be used as a bioindicator of human pollution. Heavy metals concentrations in the upper part of the sediment core of Guanabara Bay exhibited considerable temporal variability as a result of various pollutant loadings over the past few decades. The upward increases in heavy metal concentration in the sediment cores were found to be correlated with the period of rapid industrial and urbanization development in the metropolitan area of Rio de Janeiro and consequent anthropogenic metal input. The use of normalization approach toward Fe, Igeo and Adverse Effect Index has been proven to be a good tool to investigated the degree of heavy metal contamination and it was possible to confirm the anthropogenic impact in Guanabara Bay in the last centuries. Acknowledgements ~o de Funding for this Project was provided by 1) Coordenaça Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and 2)
gico Conselho Nacional de Desenvolvimento Científico e Tecnolo (CNPq). The writers are also indebted to Departamento de Geologia e Geofísica/Universidade Federal Fluminense. J.A. Baptista Neto, C.G. Vilela and O.M. Barth are a Researchers from CNPq. References Able, K.W., Duffy-Anderson, J.T., 2006. Impacts of piers on juvenile fishes in the

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Please cite this article in press as: Baptista Neto, J.A., et al., Environmental change in Guanabara Bay, SE Brazil, based in microfaunal, pollen and geochemical proxies in sedimentary cores, Ocean & Coastal Management (2016), http://dx.doi.org/10.1016/j.ocecoaman.2016.04.010