Journal of Engineering and Applied Sciences Technology

Research Article Open Access

Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of : and Baixada Santista Patrícia Pinheiro Beck Eichler1,2*, Guido De Gregório Grimaldi2,3,4, Evelyn da Rocha Mendes Pereira2,5, Christofer Paul Barker2, Helenice Vital1

1Graduate Program in Geodynamics and Geophysics Laboratory of Marine Geology and Geophysics and Environmental Monitoring, Federal University of Rio Grande do Norte (PPGG, GGEMMA, UFRN), University Campos, Lagoa Nova, 59072-970 Natal, RN, Brazil.

2Post-Graduation in Ecology at the Federal University of Rio Grande do Norte (PPG / ECO). University Campus, Lagoa Nova, 59072-970, Natal, RN, Brazil.

3NGO, Oceânica - Research, Education and Conservation, Praça São Sebastião, s / n, annex 2, Pirangi do Norte, 59161-487, Parnamirim, RN, Brazil.

4Dynamic School, Rua Alves de Brito, nº 236, Centro, Florianópolis, SC, 88015-440, Brazil.

ABSTRACT The use of foraminifera as indicators is due to the sensitivity in response to environmental variations and in this paper, we present this correlation in two Brazilian coastal areas: Guanabara Bay and Baixada Santista. In Guanabara Bay, the species found show four sub-environments. A: marine influence, B: environmentally threatened, C: pollution by industrial waste and D: contamination by domestic sewage. In the Baixada Santista two sub-environments are highlighted: Sub-environment 1 presents typical associations of marine environment indicating greater water renewal, and in sub-environment 2 predominant species with continental input where water renewal is less efficient.

*Corresponding author Patrícia Pinheiro Beck Eichler, Graduate Program in Geodynamics and Geophysics Laboratory of Marine Geology and Geophysics and Environmental Monitoring, Federal University of Rio Grande do Norte (PPGG, GGEMMA, UFRN), University Campos, Lagoa Nova, 59072-970 Natal, RN, Brazil. E-mail: [email protected] Received: August 04, 2020; Accepted: August 10, 2020; Published: August 17, 2020

Keywords: Foraminifera, Sensitivity, Marine Sediment, Ph, a subdivision of the area in different ecological zones [1]. Acidification, Sub-Environment, Threatened, Renewal, Acute Based on the distribution of faunal associations, Zaninetti et al. conducted qualitative studies of the mangrove foraminifera from Introduction and Bay regions (RJ). Also noteworthy are Many studies currently developed in Brazilian coastal regions the works of Brönniman, Brönniman & Beurlen and Brönniman make it possible to know its hydrodynamic, chemical and & Dias-Brito, who emphasize the importance of foraminifera in biological characteristics. Despite the existence of numerous ecological studies of coastal regions [2-6]. More recently, Eichler, hydrological and geochemical parameters that can be used to Eichler et al., Pereira, Vilela et al., Kfouri et al., and Macedo et control environmental variations, the reproducibility of its analysis al. studying foraminiferal distribution in Guanabara Bay have and consequent interpretation is difficult to perform. Moreover, verified the potential of these organisms in environmental analysis analysis especially of the water column, provide no more than a and diagnosis studies [7-14]. Guanabara Bay is an unconfined snapshot of the environmental parameter. The value of this image environment due to the large penetration of marine waters within can be doubted if its extreme variability is taken into account, even the system. on a time scale equivalent to a tidal cycle. It is therefore appropriate to consider the use of a simple and inexpensive management In the Santos and São Vicente estuaries, water penetration is marker capable of synthesizing the general characteristics of the less efficient, creating mixohaline environments. The bays are environment, highlighting the environmental variations of short more influenced by the circulation processes of the adjacent periods. This marker needs to be sensitive enough to react quickly continental shelf, while the estuaries with elongated geometry to changes in the environment. In this sense, foraminifera react receive this influence less intensely. Despite the geomorphological very effectively. and oceanographic differences of the compared environments, it is possible through natural history and the distribution of The use of these organisms as environmental indicators in Brazilian foraminifera to make comparisons related to anthropogenic effects coastal areas began with Closs, who carried out quantitative work like warming and acidification of the ocean and of the marine in Lagoa dos Patos (RS) on foraminifera and the camoebians sediments in anoxic environment. The use of these organisms as and their relationships with different abiotic factors, elaborated biological indicators is an instrument that allows us to highlight

J Eng App Sci Technol, 2020 Volume 2(3): 1-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117. seriously and potentially compromised locations, for diagnosing population of 7.3 million people live around the region and dump the environments, and is the objective of this work. into its organic and inorganic pollution into it is waters. More than 6000 industries, 2 commercial ports, 16 marine terminals, We intend to present the behavior of foraminifera associations two naval bases, a shipyard and a large number of ferries, fishing occurring in two Brazilian impacted and restrict coastal areas prone boats and yachts, in addition to Brazil’s largest oil refinery, Duque to water stagnation with low oxygenated waters of: Guanabara de Caxias Refinery (REDUC) are installed in this region. Bay () and Baixada Santista, mainly the Santos and São Vicente (São Paulo) estuaries. Considering that these Forty-five rivers flow into Guanabara Bay act as drainage channels. estuarine zones are subject to different oceanographic regimes and The largest rivers are born in the Serra do Mar and when they the intensity of anthropogenic effects, it is intended to determine reach Baixada Santista it starts to meander. Among the rivers that the foraminiferal species as a function of environmental changes flow into the region, Iguaçú River, Estrela River (northwest of and to define the species that indicate marine, continental, polluted the bay, near REDUC) and Guapimirim Rivers (Environmental and contaminated sub-environments of these two coastal regions. Preservation Area-APA), Guaraí River, Macacu River and Guaxindiba River. The deepest locations are in the navigation Materials and Methods channel. The current average depth of Guanabara Bay is 7.6 Study area description m, being 3 m in the bottom of the Bay and 16.9 m in the outer This article presents foraminiferal species from two Brazilian portion of the Bay. coastal areas, the Baixada Santista (area that includes the cities of Santos, Guarujá, São Vicente, Cubatão and Bertioga) and Tidal movements and wind condition the circulation and salinity of the Santos-São Vicente Estuarine System (São Paulo, SP) and the waters of the bay and river discharges. The less saline waters Guanabara Bay (an oceanic bay located in Southeast Brazil in occur near the mouths of the rivers and mangroves in the northern the state of Rio de Janeiro. On its western shore lies the cities part of the Bay, reaching salinity values lower than 8. In the middle of Rio de Janeiro and Duque de Caxias, and on its eastern shore and southern portion of the Bay, the salinity ranges between 30 the cities of Niterói and São Gonçalo); some geomorphological and 34. Average temperatures vary between 22°C and 26°C. and oceanographic considerations will be contextualized below. Until the year of 1500, the mangroves of Guanabara Bay occupied Santos-São Vicente Estuarine System a large surface of the bay, from the mouth of the Berquó River in The Santos-São Vicente Estuarine System represents one of the to the Itaipu Lagoon in Niteroi. Currently, the mangroves most important Brazilian examples of environmental degradation are restricted to the Guapimirim Environmental Protection Area [15]. The Baixada Santista has approximately 1,200,000 (APA), and scattered portions along the coast of Duque de Caxias, inhabitants, a number that can double during the summer [16]. Governor’s Island, Canal da Maré and Fundão Island. In addition, the region has the country’s most important industrial complex, the Cubatão Complex, which in 1998 had about 1,100 The lagoons around the bay were about 39 at the time of discovery. industries including petrochemicals, steel and fertilizers, which They existed in Itaipu, Botafogo, Flamengo, Inhaúma Inlet, Saco discharged about 100,000 kg / month of various pollutants such de São Diogo, Saco de São Francisco, and Copacabana. Currently as metals and petrochemicals. The Port of Santos, located on there are only the lagoons of Itaipu and Piratininga, which are the estuary is the largest port in Brazil in terms of loading and greatly altered as natural ecosystems. The beaches of Guanabara unloading, and in 1995 handled 35 million tons of products, about Bay, also showing environmental degradation, number 118, and 50% of the country’s total. the most extensive are Copacabana, Piratininga and Itaipu. The samples collected in Guanabara Bay are represented in Figure 1. In addition to the discharge of industrial effluents and port The patterns recorded for the campaign are described in Table 2. activities, the Santos-São Vicente Estuarine Complex also receives Here we show foraminiferal species of two coastal environments sewage from the region through sewage systems, clandestine the Santos-São Vicente estuarine system (São Paulo, SP) and the sewage connections from the Cota neighborhoods and the riverine Guanabara Bay (Rio de Janeiro, RJ) and some geomorphologies population irregularly settled in slums along of the estuary. The and oceanographic considerations. Santos submarine outfall came into operation in 1979, and has a length of 4 km and an internal diameter of 1.75m and contributes a Laboratory work final drainage of 7,000 liters per second of sewage to Santos Bay. Sediment samples, hydrographic and current data were collected. Physical parameters measured were: salinity, temperature, speed The discharge of domestic and municipal sewage from Santos, São and direction of currents. Location of the stations was provided Vicente and Cubatão and the organic load from the entire resident via GPS, while the depth measurements through the echo sounder. and floating population in the summer period, in the municipalities Bottom sediment was collected for the analysis of foraminifera of Baixada Santista, contribute to the persistence of unfavorable species. conditions to the coastal environment of the region. Figure 1 shows sampling stations plotted on the map of the region. The samples collected in the Santos and São Vicente Estuarine The collection of these biological samples began at the entrance system are shown in Figure 1. The patterns recorded for the of the bays, followed by the collection in the middle parts and campaign are described in Table 1. finally at the bottom of the bay. Such sampling methodology aims to highlight the occurring gradients related to the different Guanabara’s Bay oceanographic parameters studied in the bay region. Guanabara Bay is a highly urbanized coastal area where a

J Eng App Sci Technol, 2020 Volume 2(3): 2-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

and oven dryed. After separation, the foraminifera were brush- transferred to special black-bottomed slides for further analysis and identification of species. Species identification was made using stereomicroscope and based on the works of the Catalogue of Foraminifera and on the Javaux & Scott studies on foraminiferal fauna [17,18].

From the identification of foraminifera species found in the Guanabara Bay region, the individuals were summed and the absolute frequency of individuals per sampled season was obtained. From the absolute frequency, the relative frequency of the species was calculated. Based on these data, contour maps were generated that facilitate the observation and discussion of the obtained data. The contour maps were made in the Surfer program from the digitization of nautical chart n.1501. Such methodology should be adopted with caution, as the program calculates the closest values and interpolates the results. These data should always be interpreted based on the absolute frequency table. This methodology was also applied to the hydrographic parameters measured at the time of collection and to the indices used in this study.

Results Figure 1: Location of the sampling stations in Santos –São Vicente Santos-São Vicente Estuarine System (A) and Guanabara Bay (B). Abiotic Parameters Spatial and seasonal variation of temperature is observed. The Biological material was collected at fixed and punctual collection highest spatial values are concentrated in the shallowest stations. stations, with sediment sample for foraminifera analysis. At the The lowest temperatures are between 21 and 22 °C and the highest time of these collections in winter and summer, the hydrographic around 24 ° C. In summer, there is a rise in temperature in all parameters of the water column were also measured. stations, especially at the mouth of the Porto Channel (Table 1). A gradient is observed where the highest bottom salinity was For the Guanabara Bay, the microfauna characterization consisted recorded at the entrance of the bay and Porto Channel, ranging of 26 samples of the surface of the sediment. For the estuarine from 32 to 37. The lowest value of this variable was found at system of Santos São Vicente, 17 samples were collected in the station 11 (27.69). Dissolved oxygen contents in the Santos bay and inner channels (S1 and S2). Estuary bottom water is low. This fact denotes the loss of water quality in the region. The bottom sediment pH did not vary The sediment sampling for foraminifera microfauna analysis was significantly and presented values between 7.53 and 8.25 between done with Petersen type bottom catcher. The sediment for the the collection stations. These values are considered normal for determination of foraminifera microfauna analyzes (50cc) was marine environments and /or with influence of saline water. separated using two successive sieves of 0.500 and 0.062mm Table 1: Positioning of sampling stations and abiotic parameters at the bottom water of the estuarine system of Santos-São Vicente (SP)

J Eng App Sci Technol, 2020 Volume 2(3): 3-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Biological Parameters high concentrations of Bolivina striatula, which may suggest Absolute numbers of individuals identified in S1 and S2 samplings organic enrichment. Species belonging to the genus Elphidium are are shown in Tables 2 and 3. According to these tables foraminiferal characteristic of mixohaline environments with lower salinities, hyaline tests were the most frequent, represented by 30 and 33 and in the stations adjacent to the mouth of the channel in winter/05 species in the sampled campaigns (S1, S2, respectively). The (S1). However, in summer/06, E. poeyanum does not seem to suborder Rotaliida dominated in the campaigns, with main genera tolerate the oxygen deficit that occurs in the region of station Ammonia, Bolivina, Buliminella and Elphidium among the most 15. Still, the relative high frequency of this species around the representative. The suborder Textulariida was represented mainly outfall in station 3 denotes that the increase in sewage volume by Gaudryina exilis and Siphotrochammina lobata, and the that occurs in summer directly affects the establishment of E. miliolids by the genus Quinqueloculina. The hyaline Ammonia poeyanum. Spatially, the Porto Canal is more populous than the tepida was observed in practically all stations in the analyzed other two biofacies studied. Most of the agglutinated species, in campaigns, indicating its cosmopolitan characteristic. However, turn, are concentrated in the Porto Channel. In winter (S1) high it is noted that although this species occurs in great abundance salinity seems to have favored the establishment of Pararotalia throughout the region, where there is greater influence of freshwater sp. in the Santos bay. In contrast, the decrease of this species can from rivers, there is a conspicuous increase in frequency of this also be observed in station 15 during campaign 2, following the species in S1 and S2 campaigns. same pattern of E. poeyanum.

In winter/05, the highest frequency of this species occurred Probably, the reduction of dissolved oxygen and the temperature in the São Vicente Canal. Pseudononion atlanticum presents rise resulted in the reduction of this species in the coastal region. high abundance at the entrance of the bay and in the Porto and Quinqueloculina seminulum presented low relative frequency, Barreiros channels, during winter/05 (S1) and summer/06 (S2). being limited to the station in the outfall in winter/05 (S1). This This species is characteristic of marine environments, and indicates species is recognized for surviving in low dissolved oxygen the penetration of currents to the sampled sub-environments, also environments, which explains its occurrence north of the Porto suggesting transport of the tests towards the outermost portions of channel in the subsequent sampling (S2). This hypothesis is the bay in summer. The highest abundance of Bolivina striatula corroborated by the high occurrence of Q. seminulum in Santos was observed in the central-eastern portion of Santos Bay in winter Bay during summer (S2). B. elegantissima is a typical species (S1). Bulimina elongata is probably more tolerant to temperature of environments that are poorly oxygenated and contaminated increase, since its frequency is positively correlated with the high with domestic sewage, and presents individuals both around the values of this variable. It is interesting to note the frequency of Santos Bay submarine outfall, and in the Porto channel (S1 and this species in station 15, when there seems to be a replacement S2), practically concentrated at the outlet of the Jurubatuba River of this species during the summer. Stations 3, 4, and 6 showed (Figure 3). Table 2: Absolute frequency of foraminifera in Santos (Winter, S1). (*) Significant species> 1%

J Eng App Sci Technol, 2020 Volume 2(3): 4-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

J Eng App Sci Technol, 2020 Volume 2(3): 5-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Table 3: Absolute frequency of foraminifera in Santos (Summer, S2). (*) Significant species> 1%

J Eng App Sci Technol, 2020 Volume 2(3): 6-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Figure 2: Distribution gradient of B. elegantissima in Santos São-Vicente region (S1 and S2).

Although the number of species with abundance greater than 1% was little representative in the Santos Estuarine System, the presence of smaller amount of species may be significant regarding the differentiation of natural or anthropogenic characteristics that act in the distribution of microfauna. The species Ammonia tepida, Bolivina striatula, Buliminella elegantissima, Discorbis williamsoni, Elphidium excavatum, E. poeyanum, Fissurina laevigata, Haynesina germanica, Pararotalia sp., Pseudononion atlanticum and Quinqueloculin seminulum were constant at both samplings. Interestingly, the species Gaudryina exilis and Trochammina inflata were frequent only in summer, indicating that the decrease in salinity caused by increased rainfall has benefited those species.

Guanabara Bay Abiotic Parameters Comparing the positioning of the stations (Figure 1) with the collection depths (Table 4), we observed that the highest depths occur in the southern part near the Bay entrance, while the lowest depths are found in the northern part (bottom of the bay). The spatial variation of abiotic surface and bottom parameters, measured simultaneously with the collection of bottom sediment, can be seen in the contour maps shown in Figures 4 and 5. In the northern region of the bay, higher values of bottom temperature were observed due to the great influence of the continental input, and intense heating of very shallow water column. The lowest bottom temperature values were found at the inlet of the bay, mainly related to the penetration of colder saline water from the adjacent continental shelf (Table 4). Figure 3 shows the distribution of surface and bottom salinity. The lowest values are found in the bottom regions of the bay, while the highest values can be observed at the inlet of the bay. In addition to temperature, the bottom salinity gradients from the bay inlet to the middle part also show the saline influence through the bottom.

Table 4: Positioning of collection stations and abiotic parameters at surface and bottom in Guanabara Bay

J Eng App Sci Technol, 2020 Volume 2(3): 7-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Figure 3: Surface and bottom salinity distribution for winter sampling stations

Biological parameters Indicator foraminiferal species The number of individuals collected during winter was higher than the number observed in summer. These individuals are distributed in 51 foraminiferal species, belonging to the suborder Rotaliina (great majority), Textulariina and Miliolina. The main species found in winter were: Ammonia tepida, Bolivina striatula, Bulimmina elongata, Buliminella elegantissima, Cassidulina subglobosa, and Quinqueloculin seminulum and in summer the dominant species were also A. tepida, B. striatula, and B. elegantissima. Our discussion was based in the total number of species and individuals, including living and dead, listed in tables 5 (winter) and 6 (summer) referring to the number of individuals per 50 cm3 of collected sediment. To understand biological patterns we have selected dominant species for the sub environments based on the absolute tables.

Table 5: Distribution of absolute frequency of species in Guanabara Bay in winter

J Eng App Sci Technol, 2020 Volume 2(3): 8-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Table 6: Absolute frequency of species in Guanabara Bay in summer

In both winter (Table 5) and summer (Table 6), the highest total absolute frequencies were found at stations 6, 7, 8, 9 located south of Governador Island, 13 and 14 located in the central portion of bay and at station 22 located in the northeast portion. The most frequent species found in these regions belong to the suborders Rotaliina, Ammonia tepida, Bolivina striatula, Buliminella elegantissima, Fursenkoina pontoni, Bulimmina elongata, all low oxygen bio indicators. Individuals of the suborder Textulariina (Gaudryina exillis) were also found, but in a smaller percentage and concentrated only in the middle part of the bay. In winter, the species Quinqueloculina seminulum (Miliolina) was very representative, having high frequency in the northern regions of the bay.

Maps of distribution of tolerant foraminiferal species found in the Bay were contouring just for illustration of the relative frequency data. Hyaline calcareous Ammonia tepida was dominant in all stations, indicating its cosmopolitan character (Figure 4). However, it is noted that the largest relative abundances of this species occur in the north and northeast of the bay, near the Guapimirim EPA. In the summer, 1 year after the accident, this species is absent near the fuel oil spill site. The dissolution of tests made of calcium carbonate (CaCO3) began at the time of the spill and continues to be gradually dissolved, demonstrating the ecological effects due to the acidity of the sediment. The acute anthropogenic effect like acidification in the marine sediments in anoxic environment are sensed by the Forams community, and their use as biological indicators is an instrument that allows us to highlight potencial areas with near future problems.

J Eng App Sci Technol, 2020 Volume 2(3): 9-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Figure 4: Relative frequency distribution of Ammonia tepida in winter and summer

Figure 5: Relative frequency distribution of Elphidium spp in Guanabara Bay in winter and summer

Species belonging to the genus Elphidium are characteristic of mixohaline environments with lower salinities. In figure 5, we observe the occurrence of this genus in stations 22 to 26. This genus showed relatively high abundance specifically in the REDUC region only in winter, while in summer this region was sterile, showing signals of shells dissolution because the acidity of the sediment. Specifically, in winter stations 26 near the REDUC region has very acidic sediment pH. This acidity negatively influences species diversity, limiting the occurrence of species with more fragile tests and thus increasing the dominance of Elphidium spp. This was the only barren season in the summer. This fact can be explained due to the continuous dissolution of these more resistant carapaces, which culminates in the total disappearance of these microorganisms one year after the accident.

In Figure 6, Buliminella elegantissima, also a typical species of low oxygenated environments and with high concentration of organic matter, presents individuals in practically all seasons with greater relative abundance in winter, in seasons 6 to 10 (south of Governador Island) and in summer at stations 13 and 14 (central part of the bay) in the azoic zone. The distribution maps of B. elegantissima show, therefore, the high occurrence of this species in the more anoxic regions of the bay, near the São João do Meriti river south of Governador Island and in the central region. In the region near REDUC, despite being an anoxic region, the absence of this species indicates the non-tolerance of their shells at low pH.

J Eng App Sci Technol, 2020 Volume 2(3): 10-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Figure 6: Relative frequency of Buliminella elegantissima in winter and summer. Discussion williamsoni as regards seasonal occurrence, where an east-west Periodic and occasional natural phenomena such as winds, storms, migration in the frequency gradient is also observed. This species meteorological and astronomical tides, and rainfall are forces is related to microenvironments where salinity exceeds 28 and that regulate the patterns of the physical properties of bays and sediment is coarse, with low carbon contents, corroborating our estuaries. Such properties depend on the magnitude and duration obtained data [10]. In the Guanabara Bay inlet region, gravitational of these events, which directly influence salt gradients, nutrients, currents are major forcing in exchanges with adjacent ocean current intensity, transport and sediment deposition. The benthic and result in a flow of bottom water into the estuary, favoring foraminifera species, highly controlled by the abiotic factors not only sedimentary transport but intrusion of marine species related to the environment, present geographic microdistribution [22]. According to Alve, most estuaries are characterized by high and can settle in different environments, and they help to locate levels of oxygen in the sediment, which allows the maintenance and to identify the polluting sources. of high level of biological activity [23]. However, large effluents from organic material (domestic sewage) can create areas where In the Baixada Santista, it was also possible to evidence the oxygen consumption exceeds supply, especially during summer presence of typical associations of marine environment indicating months, making the environment anoxic and atrophic. Regarding greater water renewal, and species with continental input where the results of dissolved oxygen in Santos, there is a gradient, water renewal is less efficient. Environmental characterization where lowest values were obtained in summer, corroborating studies involving Santos-São Vicente estuarine system also show literature, which emphasizes high rates of degradation in that low circulation in the surrounding channels around Cosipa, the São environment [24,25]. In addition, decrease in summer values Paulo Steel Company and this fact is directly related to temperature denotes increase in aerobic biological activity that is activated and salinity, since these restricted places tend to be stagnant, as temperature increases at this time of year. Severe hypoxia is resulting in higher temperature values [11]. The results obtained in defined as the threshold at which significant impacts are observed the present study corroborate this hypothesis, since the temperature on the biota and correspond to dissolved oxygen concentrations in the Santos estuary was higher in stations 1 to 3 and 13. In below 2 mg / L [26,27]. In addition, many authors have established marginal coastal areas such as bays and estuaries, the instability of relationships between dissolved oxygen content and foraminifera the water column because of the oscillation of astronomical tides associations corroborating our findings [28,29]. In summer, station provides greater evaporation increasing salinity, and increased 14 of Santos estuary was sterile, which may be related to low water temperature in summer. Bonetti studies of Santos Bay oxygen levels, which were often below the above threshold. It is shows that the vast majority of hyaline foraminiferal species is important to stress that there is a fundamental difference between in agreement with our study [19]. In Santos and Guanabara Bay, the eutrophic and opportunistic terms. Due to the dominance in the species Discorbis floridana, D. williamsoni and Cassidulina generally eutrophic environments, and the absence of oligotrophic subglobosa occurred only in the stations where salinity was higher sites, many bisserial species are characterized as eutrophic, but showing the preference of these species for sites like it. Eichler often have opportunistic behavior [30]. According to some authors, et al. and Cardoso, studying São Sebastião channel, consider Buliminella elegantissima is typical species of environments rich in the occurrence of these species as indicators of high density sea organic matter, which inhabits muddy and contaminated sediment currents that penetrate in the bottom water [20,21]. Eichler et al., by domestic sewage [20,31,32]. Environments with high organic studying Bertioga canal, also observed the presence of the genus contents are directly related to higher mud concentrations (Tyson, Discorbis as an indicator of marine influence [9]. The circulation 1995), since in this type of sediment the energy is low, contributing pattern of Santos Bay can be evidenced by D. williamsoni, appears to the deposition processes of organic matter. Environments with to have been transported east west. In addition to the presence of these characteristics have very low oxygen levels. In the Santos the genus Discorbis at the entrance stations of Guanabara Bay, Estuarine system, B. elegantissima estuary occurred in winter just the presence of Pseudononion atlanticum occurred in regions around the submarine outfall, which, according to Abessa et al.is with significant marine influence, indicated by the salinity value. a source of sedimentary changes to the central bay area [24]. In This species appears to have followed the same pattern as D. summer, however, the highest frequency was observed in the Porto

J Eng App Sci Technol, 2020 Volume 2(3): 11-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Channel, where a large amount of organic matter was observed, but the peak of this variable was obtained in the Casqueiro Human population of 7.3 million live around the region and dump channel, where this species did not occur, probably due to the a large amount of industrial and municipal waste daily, most of high temperature that restricted the occurrence of this species. which is untreated. The disposal of domestic sewage from the city This species was characterized by Burone et al. as a characteristic of Rio de Janeiro takes place mainly in the waters of the Rio S. of oxygen depleted environments [33]. The natural sources of J. de Meriti located to the west of Governador Island. Therefore, organic matter for coastal environments are the phytoplankton the region south of Governador Island is seriously compromised, production and the continental debris, which through the rivers because the stagnation of the net mass due to the low efficiency reach the receiving body and can be transported again. Therefore, of water renewal in this region which is unable to export from the determination of the elemental ratios between the organic the São João do Meriti River. sediment constituents can provide clues about the origin of organic matter. However, in places where there is a large river contribution, In addition, the S. J. do Meriti River influences the locations north the accumulation of organic matter occurs preferentially at the of the bay, because west of Governador Island, where the natural mouths, influencing the production of those sites [34]. In addition, passage of the water flow would previously be, communication the degradation of organic matter involves oxidation reactions is now practically closed due to silting and landfills carried out

(such as Fe3), which often result in the formation of azoic zones. in the region. As a result, water tends to Braga et al. demonstrated that water quality in the Santos Estuarine occur northwards, making its water renewal inefficient. System is strongly affected by continental drainage and industrial activities, with high values of nitrite, nitrate, phosphate and silicate More than 6000 industries, 2 commercial ports, 16 marine [35]. In recent decades, there has been increasing evidence that the terminals, two naval bases, a shipyard and a large number of relationship between the flow of organic matter and foraminifera ferries, fishing boats and yachts, as well as the largest oil refinery is intrinsic and this flow is directly related to primary production in Brazil, the Duque de Caxias Refinery (REDUC), pour 1.4 [28,36-40]. Ammonia tepida is characterized by being myxohaline, tons of oil and industrial waste into Guanabara Bay waters daily. infaunal, and develops well at temperatures between 0 and 30 °C According to Alve, most bays are characterized by high levels [41]. Its occurrence in the present work shows that this species is of oxygen in the sediment, which allows the maintenance of a cosmopolitan and tolerates practically all salinity variations in both high level of biological activity [24]. However, large effluents regions. In Santos, this species does not seem to correlate with from organic material (domestic sewage) can create localized the high levels of organic matter of the Casqueiro channel, maybe areas where oxygen consumption exceeds supply, especially because sediment is too acidic, being dominant in the bay and in during the summer months, making the environment anoxic and the Porto Channel. In studies by Eichler and Eichler, areas with atrophic. Due to the increased domestic sewage load in summer, mercury accumulation, which are the channels under the influence the central bay has the lowest bottom oxygen values. This fact is of the Cubatão industrial complex, the agglutinated species also related to the increase in temperature of this time of year and Arenoparrella mexicana, Gaudryina exilis, Haplophragmoides the phytoplankton bloom, which provides greater eutrophication wilberti and Ammotium salsum are dominant. In the Porto Channel, of the area, and consequent hypoxia. Periods of seasonal hypoxia the environments are characterized by high salinity and typical are widely observed in coastal areas, and are mainly related to species Ammonia spp., Elphidium spp., Bolivina striatula and eutrophication and oxygen uptake caused by phytoplankton Pseudononion atlanticum [8]. The total fauna (living and dead) blooms. Such periods were observed by Boesh and Rabalais in of foraminifera are reliable biological information through [42]. studies in Chesapeake Bay and the Gulf of Mexico [46].

In addition, Scott and Medioli demonstrated that the seasonally The regions south of Governador Island, near Fundão Island, need integrated total association better reflects prevailing environmental better study since they are regions where there is great organic conditions [43]. This fact confers important limitations regarding dumping through the S. J. de Meriti River. According to Cavalier the study of allochthonous (living) associations only. Morvan et et al., in an assessment of cell stress in mollusks, they observed al. indicate the exclusive use of living fauna only for correlation that animals from the southern regions of Governador Island were to specific factors [44]. more clearly affected by local pollution [47].

The distribution of foraminifera in Guanabara Bay is mainly It is also noteworthy that the levels of ammonia, chlorophyll and composed of opportunistic - tolerant species, and low diversity turbidity observed in the regions near Governador and Fundão with strong dominance of few species. It also shows marine Island are high in relation to the rest of the bay, and well above influence, pollution by industrial waste, and contamination by the standard set by CONAMA, proving to be worrying factors in domestic sewage. The alteration of the pH and oxygen contents the process of degradation of the bay [48]. demonstrated efficacy in the control of the establishment of foraminiferal species. Species that are abundant in polluted areas The influence of domestic pollution on the foraminiferal population are tolerant to pollutants to which they are subjected, however, has been widely studied. Recently, in a study conducted in the there are also sensitive species that express their sensitivity through Olaria River region (Cananéia, SP), Eichler et al. found that their absence. According to Alve, low or intermediate levels of essentially organic pollution, associated with the regular renewal dumping can cause hypertrophic zones related to foraminifera of its waters at each tide, favored the establishment of opportunistic productivity increase, while very high concentrations can result species [21]. The increase in A. tepida population is related to the in atrophic zones where productivity is lower [24,45]. decrease in bottom sediment oxygen levels (less than 3 mg / l), while the smallest populations are where the pH is acidic [49]. Due to its preference for anoxic environments Buliminella Whitcomb in experimental studies with A. becarii found that elegantissima was found in the area of the environmental oil inhibits the growth and reproduction of this species, and its preservation area in winter, but not in the region of REDUC, products cause foraminifera to die [50,51]. On the other hand, indicating that this species does not tolerate acidic pH environments in places near domestic sewage there is a proliferation of other due to the fragility of its carapace. species. This shows in the fact that this species degrades organic

J Eng App Sci Technol, 2020 Volume 2(3): 12-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117. matter in laboratory experiments and is omnivorous, and feeds on community, being low in polluted sites. However, the faunal phytodetrites that flourish in domestic sewage [52]. composition varies between different locations and may influence such values. B. elegantissima has a higher incidence in the southern region of Governador Island, near Fundão Island and the central part of This study revealed the applicability and efficiency of the use the bay, in the azoic region, exactly like the Santos Sao Vicente of foraminiferal population dynamics correlated to abiotic Estuary, in the enrichment zone. According to some authors , patterns in environmental assessments and diagnostics that can B. elegantissima is a typical species of environments rich in be used in coastal management plans, aiming at monitoring and organic matter, with low oxygen content, favoring its occurrence forecasting environmental impacts. Based on our data, it was in sediments contaminated by domestic sewage [21,32,53]. possible to verify where the regions most subject to pollution and Corroborating this data, Eichler points out that excessive nutrient contamination are located and to identify the polluting sources. enrichment favors the proliferation of opportunistic species with The four sub-environments in Guanabara Bay shows marine rapid growth rates, increasing local dominance [7]. Environments influence, environmentally threatened, pollution by industrial with high levels of organic matter are directly related to higher waste, and contamination by domestic sewage. In the Baixada concentrations of fine sediment, since in this type of sediment the Santista, however it was possible to evidence the presence of energy is low, contributing to the deposition of organic matter typical associations of marine environment indicating greater [54]. Also, in these regions, the oxygen content is very low. water renewal, and species with continental input where water It is noted that B. elegantissima presented its highest relative renewal is less efficient [57-67]. frequency just where hypoxia is accentuated, in the southern region of Governador Island, near Fundão Island in winter and Acknowledgments: We are thankful to CAPES (Coordenação de in the central region near the azoic zone. Azoic zones are usually Aperfeiçoamento de Pessoal de Nível Superior) for the Ciências located near places where the increase in bacteria from extreme do Mar II project 23038.004320/2014-11, and a post-doctoral pollutant concentrations causes a decrease in oxygen content [55]. fellowship (98/2017-05) for P.P.B. Eichler at Moss Landing Marine According to Kjerfve et al., the west bank and the inner parts of the Laboratories, San Jose State University, and at the Ocean Sciences, bay present high concentrations of nutrients (nitrogen, phosphate University of California, Santa Cruz and for the Special Visiting and sulfur) due to enrichment from domestic discharge and poor Professor (PVE 151-2012, AUXPE242/2013). efficiency in water renewal near Governador Island and Fundão Island [56]. These are the most seriously impacted locations for We are grateful to the ANP - PRH 22 and the CAPES Ciências water and sediment acidification. do Mar II 23038.004320/2014-11, Project “Oceanographic process in the breaking of the continental shelf of northeastern The analysis of hypoxia levels suggests that Guanabara Bay is Brazil: Scientific foundations for special marine planning” for the a highly eutrophic environment in the margins (low circulation financial assistance granted; which among other resources, enabled regions), reaching its maximum values close to APA. The lower a Pos Doc fellowship for P.P.B. Eichler (98/2017-05) at Moss hypoxia values obtained in the REDUC region also suggest that, Landing Marine Laboratories (MLML), San Jose State University despite the APA-like bottom oxygen content, this environment (SJSU), and Ocean Sciences at the University of California at presents lower eutrophication and consequent productivity Santa Cruz (UCSC). We are thankful to the crews of the vessels limitation compared to the preserved region. Dominance values used and to all colleagues of GGEMMA. This research was also are high in the REDUC region and in the azoic zone, reflecting sponsored by Capes Professor Visitante Special (PVE 151-2012, the establishment of few species adapted to those conditions. The AuxPe 242-2013) project. We are also thankful to CNPq for the results reaffirm the use of foraminiferal species in oil and sewage research grant (PQ 311413/2016-1) and for co-author Vital H. pollution studies, even where carbonate dissolution is active due to low pH values. References 1. Closs D (1964) Ecological distribution of Foraminifera and Conclusion Thecamoebina in the Patos Lagoon, Southern Brasil. Arch. The two regions have innumerable differences both in Oceanogr. E Limnolog., XIII (2). geomorphological terms and in the anthropogenic load, but 2. Brönnimann P (1978) Recent benthonic foraminifera when analyzing the sub-environment it is possible to make from Brazil-Morphology and Ecology: Part 3. Notes on considerations regarding the establishment of species in relation Asterothrochammina Bermuda and Seiglie. Notes from the to environmental factors. Paleontology laboratory, University of Gèneve 3:1-8. 3. Brönnimann P (1979) Recent benthonic foraminifera from The abundance and distribution of the main species of the Brazil-Morphology and Ecology: Part 4. Trochaminids from foraminifera population responds to salinity, temperature, decrease the Campos shelf with description of Paratrochammina n. of pH and dissolved oxygen. called paleontological Zeitscheiff, Stuttgart 63:5-25. 4. Brönnimann P (1980) Recent benthonic foraminifera Opportunist-tolerant species (Ammonia tepida and B. from Brazil-Morphology and Ecology: Part 5. Primitive elegantissima) have been found to benefit directly from certain agglutinated foraminifera from the Campos and Bahia shelf. types of contamination by increasing their relative abundance. Paleontologisch Zeitscheiff, Stuttgart 64: 67-89. The other type of benefit may be indirect, as forElphidium spp., 5. Brönnimann P, Beurlen G (1977b) Recent benthonic where its dominance is greatly increased due to the absence of foraminifera from Brazil-Morphology and Ecology. Part 2 and other species that had their tests first dissolved by acidification. 3. Cribostomoides Cushman and Haplophragmoides Cushman The present study emphasizes that Guanabara Bay is a highly from the Campos shelf. 4. Trochammina brasilienses. impacted environment, reflecting a little diverse fauna, dominated 6. Brönnimann P, Dias-Britto D (1982) New Lituolacea (Protista, by few species and Santos Bay presents agglutinating species Foraminiferida) from shallow waters of the Brazilian shelf. dominating in more contaminated places. Diversity can be assessed Jour. of foram. Research 12: 13-23. as a measure of environmental stress on the foraminiferal benthic 7. Eichler PPB (2001) Evaluation and Diagnosis of the Bertioga

J Eng App Sci Technol, 2020 Volume 2(3): 13-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

Canal (São Paulo, Brazil) through the use of indicators 24. Alve E (1995) Benthic foraminiferal responses to estuarine (foraminifera) associated with deposition and estuarine pollution: a review. J. Paleont 190-204. circulation patterns. Doctoral thesis. University of Sao Paulo. 25. Abessa DM, Carr RS, Rachid BR, Sousa EC, Hortelani MA Oceanographic Institute 240. et al. (2005) Influence of a Brazilian sewage outfall on the 8. Eichler PPB, Eichler BB (2003) Use of foraminifera in the toxicity and contamination of adjacent sediments. Marine environmental characterization of two coastal regions of Pollution Bulletin 50: 875-885. Brazil: Bai a de Guanabara (RJ) and Baixada Santista (SP): 26. Martins CC, Bícego MC, Mahiques MM, Figueira RC, Tessler Revista Episteme 28:291-299. MG (2011) Polycyclic aromatic hydrocarbons (PAHs) in a 9. Morvan J, Debenay JP, Jorissen F, Redois F, Bénéteau, et al. large South American industrial coastal area (Santos Estuary, (2006) Patchiness and life cycle of intertidal foraminifera: Southeastern Brazil): sources and depositional history. Marine implication for environmental and pale environmental pollution bulletin 63: 452-458. interpretation. Marine Micropaleontology 61: 131-154. 27. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a 10. Eichler PPB, Eichler B, Miranda LB, Rodrigues AR (2007) review of its ecological effects and the behavioural responses Modren foraminifera facies in a subtropical estuarine channel, of benthic macrofauna. Oceanography and marine biology. Bertioga, São Paulo, Brazil. Journal of Foraminifera Research An annual review 33 : 245-303. 37: 234-247. 28. Rabalais NN, Turner RE, Wiseman WJ (2001) Hypoxia in 11. Pereira ERM (2004) foraminifera response to stressors in the Gulf of Mexico. Journal of environmental quality 30: an impacted coastal bay - Guanabara Bay (RJ). Masters 320-329. dissertation. IOUSP. 29. Van der Zwaan GJ, Duijnstee IAP, Den Dulk M, Ernst 12. Pereira ERM (2009) Applicability of foraminifera as tracer SR, Jannink NT (1999) Benthic foraminifers: proxies or organisms - study applied in two distinct estuarine regions: problems?: a review of paleocological concepts. Earth- The Santos and Cananéia Systems - São Paulo (SP), Brazil. Science Reviews 46: 213-236. Doctoral thesis. IOUSP. 30. Thibodeau B, De Vernal A, Mucci A (2006) Recent 13. Vilela CG, Batista DS, Batista-Neto JA, Crapez M, Mcallister eutrophication and consequent hypoxia in the bottom waters JJ (2004) Benthic foraminifera distribution in high polluted of the Lower St. Lawrence Estuary: Micropaleontological and sediments from Niterói Harbor (Guanabara Bay), Rio de geochemical evidence. Marine Geology 231:37-50. Janeiro, Brazil. Anais da Academia Brasileira de Ciências 31. Abu-Zied RH, Rohling EJ, Jorissen FJ, Fontanier C, Casford 76:161-71. JS, et al. (2008) Benthic foraminiferal response to changes 14. Kfouri PB, Figueira RC, Figueiredo AM, Souza SH, Eichler in bottom-water oxygenation and organic carbon flux in the BB (2005) Metal levels and foraminifera occurrence in eastern Mediterranean during LGM to Recent times. Marine sediment cores from Guanabara Bay, Rio de Janeiro, Brazil. Micropaleontology 67:46-68. Journal of Radio analytical and Nuclear Chemistry 265: 32. Setty A, Nigam R (1982) Foraminiferal assemblages & 459-66. organic carbon relationship in benthic marine ecosystem 15. Macedo MC, Vilela CG, Baptista Neto JA (2013) Registration of western Indian continental shelf. Indian J. mar. Sci 11: of Marine Influence Through the Distribution of Benthic 225-232. Foraminifers in Guanabara Bay, State of Rio de Janeiro, 33. Sen Gupta B (1999) Modern foraminifera. Kluver Academic Brazil. Yearbook of the Geosciences Institute 36: 117-128. Publishers 371. 16. Lamparelli MC, Costa MP, Prosperi VA, Bevilacquaj E, 34. Burone L, Pires-Vanin AMS (2006) Foraminiferal assemblages Araújo RPA, et al. (2001) Santos and São Vicente estuarine in the Ubatuba Bay, south-eastern Brazilian Coast. Scientia system. Technical Report CETESB, São Paulo 183. Marina 70: 203-217. 17. MMA (2001) Brazilian national programme of action for the 35. Meyers PA (1997) Organic geochemical proxies of upper Southwest Atlantic Region. http://www.gpa.unep.org/ paleoceanographic, paleolimnologic, and paleoclimatic Documents/NPA/NPA_BRAZIL.pdf> processes. Organic geochemistry 27: 213-250. 18. Ellis BE, Messina AR (1940–1978) Catalogue of Foraminifera. 36. Braga ES, Bonetti CV, Burone L, Bonetti Filho J (2000) American Museum of Natural History, New York (ISBN Eutrophication and bacterial pollution caused by industrial 0-913424-34-X). and domestic wastes at the Baixada Santista Estuarine 19. Javaux EJ, Scott DB (2003) Illustration of modern benthic System–Brazil. Marine Pollution Bulletin 40:165-173. foraminifera from Bermuda and remarks on distribution in 37. Brönnimann P, Beurlen G (1977a) Recent benthonic other subtropical/tropical areas. Palaeontologia electronica foraminifera from Brazil-Morphology and Ecology. Part 1. 6: 29. Polystommininae, new subfamily. The Trochaminidae and 20. Bonetti CVHC (2000) Foraminifers as bioindicators of the description of Polystomamminina planulata (Mikhale Vitali), ecological stress gradient in polluted coastal environments. from the Campos shelf. Archives des Sciences. Genève 30: study applied to the Santos estuary system - São Vicente 77-90. (SP, Brazil). Doctoral thesis, Oceanographic Institute of São 38. Corliss BH, Chen C (1988) Morphotype patterns of Paulo 229. Norwegian Sea deep-sea benthic foraminifera and ecological 21. Eichler BB, Debenay JP, Bonetti C, Duleba W (1995) implications. Geology 16: 716-719. Distribution of benthic foraminifera in the southwest zone 39. Jorissen FJ, De Stigter HC, Widmark JG (1995) A conceptual of the lagoon-estuarine system of Iguape-Cananéia (Brazil). model explaining benthic foraminiferal microhabitats. Marine Bolm. Inst. Oceanogr 43: 1-17. micropaleontology 26: 3-15. 22. Cardoso PBPK (2000) Characterization of foraminifera in 40. Mackensen A, Schmiedl G, Harloff J, Giese M (1995) Deep- the São Sebastião channel (SP) and their use as indicators sea foraminifera in the South Atlantic Ocean; ecology and of water masses and some environmental variations. Masters assemblage generation. Micropaleontology 41: 342-358. dissertation. USP Oceanographic Institute 108. 41. Loubere P, Fariduddin M (1999) Benthic foraminifera and the 23. Kjerfve B (1986) Comparative oceanography of coastal flux of organic carbon to the seabed. In Modern foraminifera lagoons. In Estuarine variability Academic Press 63-81. Springer, Dordrecht 181-199.

J Eng App Sci Technol, 2020 Volume 2(3): 14-15 Citation: Patrícia Pinheiro Beck Eichler, et al (2020) Use of Foraminifera in the Environmental Characterization of Two Coastal Regions of Brazil: Guanabara Bay and Baixada Santista. Journal of Engineering and Applied Sciences Technology. SRC/JEAST-117.

42. Gooday AJ (2003) Benthic foraminifera (Protista) as tools 230. in deep-water palaeoceanography: environmental influences 55. Tyson RV (1995) Sedimentary Organic Matter. London, on faunal characteristics. Chapman & Hall 589. 43. Murray JW (1991) Ecology and Palaeoecology of Benthic 56. Schafer CT, ES Collins, JN Smith (1991) Relationship of Foraminifera. London, Logman Scientific & Technical 397. foraminifera and thecamoebian distributions to sediments 44. Kidwell SM (2002) Time-averaged molluscan death contaminated by pulp mill effluent. Saguenay Fjord, Quebec. assemblages: palimpsests of richness, snapshots of abundance. Canadá. Marine Micropaleontology 17: 255-283. Geology 30: 803-806. 57. Kjerfve B, Ribeiro CHA, Dias GTM, Filippo AME, 45. Scott DB, Medioli FS (1980) Quantitative studies of marsh Quaresma VS (1997) Oceanographic characteristics of an foraminiferal distributions in Nova Scotia: Their implications impacted coastal bay: Baía de Guanabara, Rio de Janeiro, for the study of sea-level changes. Cushman Foundation for Brazil. Continental Shelf Research 17: 1609-1643. Foraminiferal Research, Special Publication 17:58. 58. Adams CS (2006) Estuaries of the past and present: A 46. Yanko V, Kronfeld J, Flexer A (1994) Response of benthic biofacies perspective. Sedimentary Geology 190: 289-298. foraminifera to various pollution sources: implications for 59. Boltovskoy EE, Wright R (1976) Recent Foraminifera. Junk pollution monitoring: Journal of Foraminifera Research 24:1- , The Hague 515. 17. 60. Debenay JP, Eichler B Beck, Guillou J-J Eichler-Coelho P, 47. Boesh DF, Rabalais NN (1991) Effects of hipoxia on Coelho C, Porto-Filho E (1997) Behavior of foraminifera continental shelf benthos: Comparisons between the New populations and comparison with avifauna in a strongly York Bight and the northern Gulf of Mexico, In: Modern and stratified lagoon: Lagoa da Conceição (S.C., Brazil). Revue Ancient Continental Shelf Anoxia. Geol. Soc. of London. de Paléobiologie, Geneva 16 :55-75. Special publ 58: 27-34. 61. Kennish MJ (1997) Practical Handbook of Estuarine and 48. Cavalier BD, Amorim MA, Lima EFA,Wagener A (2000) The Marine Pollution. Marine Science Series. Boca Raton, Fl. use of the lysosomal assay for evaluation for rapid assessment MARGALEF, R. 1974. Ecologia. Omega, Barcelona 951. of cellular stress in Perna Perna mussel in Guanabara Bay, 62. Malone TC (1991) River flow, phytoplancton production and RJ. Anais Xiii National Week Of Oceanography 224-226. oxygen depletion in Chesapeak bay, in: Modern and Ancient 49. Amorim MA, Sabino C, Zee D (1995) Space-time monitoring Continental Shelf Anoxia. Geol. Soc. of London. Special of water quality in Guanabara Bay. Anais Xiii National Week publ 58: 83-93, Of Oceanography 308-310. 63. Odum EP (1988) Fundamentos da Ecologia, 4ª ed. Fun. 50. Bradshaw JS (1961) Laboratory experiments on the ecology Calouste Gulbenkian, Lisboa. 927. of foraminifera. Contributions from the Cushman Foundation 64. Rodrigues AR (2000) Response of foraminifera associations for Foraminifera Research 12: 87-106. to environmental variations occurring in the Bertioga channel 51. Whitcomb NJ (1977) Effects of Oil Pollution on selected (SP). Monograph (baccalaureate). Methodist University of species of benthic foraminifera from the Lower York River, São Paulo. Sao Paulo 74. Virginia. M.S. Thesis. Duke University, Durham, North 65. Sanders HL (1969) Benthic marine diversity and stability Carolina. time hypothesis. Brookhaven Symp Biol 22: 71-81. 52. Whitcomb NJ (1978) Effects of oil pollution upon selected 66. Seiglie GA (1967) Systmatics of the foraminifera from Araya- species of benthic foraminiferids from the lower York River. Los Testigos shelf and upper slope, Venezuela with special Virginia. Geological Society of America Annual Meeting. reference to suborder Rotaliina and its distribution. Carib, Abstracts with Programs A515. Jour. Sci 7: 95-133. 53. Thomas E, Varekamp JC (2000) Changes in environment 67. Zaninetti L, Brönnimann P, Beurlen G, Moura JA (1977) The biota in Long Island Sound: The last 40 years. mangroves of Guaratiba and the Bay of Sepetiba. State of 54. Sen Gupta BK, Turner RE, Rabalais NN (1996) Seasonal Rio de Janeiro, Brazil: Foraminifera and ecology. Arch. Sci. oxygen depletion in continental shelf waters of Louisiana: Geneva. 30:161-178. Historical record of benthic foraminifers. Geology 24; 227-

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