The environmental quality of the marine area close to the Landulpho Alves Oil Refinery situated in Todosos Santos Bay (Bahia, Brazil) was assessed by statistical methods on foraminiferal assemblages, with species tolerant to low continental influence such as Ammonia tepida, Elphidium excavatum, Pseudononion atlanticum and Quinqueloculina spp., and to high organic matter such as Buliminella elegantissima and Bulimina marginata. We have found that Bolivina pulchella, Pseudononion atlanticum, Fursenkoina pontoni, Buliminella elegantissima, Bolivina striatula, Bulimina marginata, Quinqueloculina spp., Ammonia tepida, and Elphidium excavatum are opportunistic and tolerant to high levels of accumulated organic matter, and are associated to stations 6, 17, 18, 19, 21, 22, 23, 24, and 25, located mainly in the southern, outermost part of the Bay.
The problems resulting from the pollution of coastal areas near urban and industrial centers in Brazil, as well as in several coastal countries, have been worsening rapidly. This has led to an ever-increasing number of environment protection entities, public health organizations and universities becoming involved in plans to assess and monitor pollutants in these areas. This is a subject to be tackled in a multidisciplinary way, taking into consideration the close interrelations linking the geological, physical, chemical and biological aspects inherent to the marine environment.
It is therefore worthwhile to consider the use of a proxy indicator that is simple to handle, inexpensive and reflects the environment’s general features variations. Such a proxy must be sensitive enough to react rapidly to environmental variation and to pollution effects. In this sense, foraminiferal patterns of dominance and diversity are widely used since they respond to environmental stress and are commonly used in areas of oceanography and environmental monitoring [
Several studies using foraminifera from confined coastal waters (lagoons, estuaries and mangroves) have been carried out in Brazil, however, most are limited to the species distribution. [
In relation to pollution, the use of benthic foraminifera as indicators was initiated by [
In this study, environmental quality of Todosos Santos Bay (TSB) was assessed quantitatively and qualitatively, through the distribution of foraminifera in the ecologically different environments of regions of Landulpho Alves Oil Refinery (RLAM) Sub-tidal area?stations 1 to 25 (
The study area is located between 12˚42'S - 12˚45'S and 38˚32'W - 38˚36'W in the northeast portion of TSB (
Studies have found temperature and salinity values indicated the presence of Coastal Water (CW) in TSB by [
BRAS Brazilian company “Refinaria Landulpho Alves-Mataripe” (RLAM) is situated adjacent to the study area and resultant effluents are discharged into it. Three rivers flow into the northeast portion of Todosos Santos Bay, the Caípe River, the Mataripe River and the São Paulo River. All of them flow through zones with mangrove vegetation and carry wastes from several industries and urban centers [
Silty sediments dominated in deep stations located in the center and in the east region of the TSB, whereas in shallow stations situated near the mouth of the three rivers, directly influenced by their inflow, sandy sediments were dominant. Highest content of total organic carbon, nitrogen and sulfur followed the distribution of silt and clay fractions [
Occurrence of petrogenic contamination with some pyrolytic input and the presence of degraded or weathered petroleum in sediments of TSB were presented by [
During the program’s first year, two samplings (winter and summer of 2003) were carried out, and 20 stations sampled (1 - 20) in the subtidal zone of the Landulpho Alves Oil Refinery (RLAM) area. No sampling was performed at the control stations located in the Caboto and Camamu mangrove. In the second year of sampling (winter and summer, 2005), five stations were added to the sampling network (21-25) of the RLAM subtidal area, and sediments were also collected at four stations situated in each one of the control regions (Camamu and Caboto) (
This material was washed in 0.500- and 0.062-mm sieves to remove silt and clay, and oven dried at 60˚C. Fractions were floated in trichloroethylene (C2HCL3), so as to facilitate the separation of foraminiferal tests from terrigenous grains [
Living foraminiferal species were counted per sampled station, then the species’ relative abundance was calculated.
Maps of foraminiferal spatial distribution were drawn up using a geographic information system (SURFER 8.0), which relates each datum to its geographic coordinates.
Diversity, dominance and evenness indices: Univariate techniques that encompass diversity, dominance and evenness indices are effective when used together to assess changes in community structure. The indices calculated in the present study were Shannon-Wiener diversity to the base e [
Multivariate analysis: To corroborate the descriptive statistics, Non-metric multi-dimensional scaling analysis (MDS) was applied using PRIMER program. In these analyses Bray-Curtis biological similarity matrices were used, with log (x + 1) transformed absolute data. Groups in non-metric multidimensional scaling (MDS), are formed based on foraminiferal data producing a “map” of samples in which the placement of samples reflects the similarity of their biological communities and environmental patterns, rather than their geographical location.
To assess the degree of environmental pollution the hypoxia index (A-E index) described by [
The A-E index is calculated by the formula:
where: A.B. = absolute abundance (number of individuals/50 cm3)
Values of the A-E index and the distribution of Ammonia tepida were plotted in Scatter plots correlating the percentage of organic carbon to the concentration of PAH to assess the patterns present in the samples. Analysis of tests fragmentation: Tests were observed in relation to the state of test preservation, due to acidity and transportation. These analyses were qualitatively estimated.
It can be visualized that Ammonia tepida presented highly expressive abundance (more than 30%) with a notable decrease at station 06 (
Elphidium excavatum, on the other hand, presented abundance increase at station 14, particularly in July 2004. This pattern was still more marked in the two summer samplings (
Buliminella elegantissima presented a similar pattern in July 2003, December 2003 and January 2005, with a peak of occurrence especially at station 15 (
In July 2003, Pseudononion atlanticum occurred at stations 13, 14, 17, 18, and in January 2005 the occurrence of this species at stations 2, 3, 4, 6, 14, 16, and 20 is very low (
Quinqueloculina spp. were dominante especially at stations 4 and 6, and had lower relative abundances at stations 16, 17, 18, 21 and 22. The patterns observed in the winter were quite similar to those found in the summer, and the pattern repeated itself from one year to the next with few variations (
In all samplings, Ammonia tepida predominated in the region, followed by species characteristic of marine environments under little influence from continental runoff such as Elphidium excavatum, Pseudononionatlanti-
Ammonia tepida
Elphidium excavatum
cum, Quinqueloculina spp. The presence of agglutinated forms (Gaudryinaexilis, Ammotium spp., Haplophragmoideswilberti, Arenoparrellamexicana, Trochammina sp.) was also found, indicating high influence from continental runoff in some stations. No anomalies in foraminiferal tests were detected.
Foraminiferal relative abundances from winter and summer samplings are given in supplementary data. Frag- mented tests of Ammonia tepida, Elphidium excavatum, Quinqueloculina spp. occurred more in the winter than in the summer. In the winter, the highest number of species with fragmented tests occurred at station 17, while in the highest number of fragmented tests was at station 25. These data can also be found in the supplementary data.
Diversity, dominance and evenness data are presented in
in
In all samplings it was observed decrease in diversity and increase in Ammonia tepidadominance in stations 1 to 4 of the RLAM subtidal area. An increase in diversitywas found at stations 21 to 25. Among the mangrove samples, stations Cab 2, Cab 3, Cam 1 and Cam 2 presented higher diversity and lower dominance and evenness.
In the MDS analysis using all the stations sampled in the winter of 2004 (
Jul-04 | Evenness | Diversity | Dominance | Jul-03 | Evenness | Diversity | Dominance |
---|---|---|---|---|---|---|---|
1 | 0.66 | 1.44 | 0.29 | 2 | 0.63 | 1.32 | 0.31 |
2 | 0.59 | 1.30 | 0.37 | 3 | 0.58 | 1.21 | 0.40 |
3 | 0.52 | 1.21 | 0.43 | 4 | 0.61 | 1.19 | 0.37 |
4 | 0.67 | 1.08 | 0.38 | 5 | 0.53 | 1.04 | 0.44 |
5 | 0.62 | 1.43 | 0.33 | 6 | 0.77 | 1.92 | 0.18 |
6 | 0.75 | 1.73 | 0.25 | 7 | 0.65 | 1.79 | 0.30 |
7 | 0.79 | 1.74 | 0.22 | 8 | 0.67 | 1.76 | 0.28 |
8 | 0.75 | 1.81 | 0.22 | 9 | 0.62 | 1.69 | 0.33 |
9 | 0.74 | 2.05 | 0.20 | 10 | 0.68 | 1.74 | 0.28 |
10 | 0.70 | 2.03 | 0.21 | 11 | 0.63 | 1.57 | 0.35 |
11 | 0.73 | 1.87 | 0.26 | 12 | 0.67 | 1.72 | 0.24 |
12 | 0.67 | 1.95 | 0.22 | 13 | 0.78 | 2.13 | 0.16 |
13 | 0.68 | 1.56 | 0.29 | 14 | 0.81 | 1.86 | 0.18 |
14 | 0.56 | 1.55 | 0.32 | 15 | 0.66 | 1.64 | 0.27 |
15 | 0.91 | 2.26 | 0.12 | 16 | 0.69 | 1.53 | 0.31 |
16 | 0.99 | 1.09 | 0.34 | 17 | 0.66 | 1.38 | 0.34 |
17 | 0.80 | 1.98 | 0.18 | 18 | 0.73 | 1.31 | 0.36 |
18 | 0.66 | 1.58 | 0.33 | 19 | 0.66 | 1.38 | 0.33 |
19 | 0.63 | 1.52 | 0.32 | 20 | 0.74 | 1.55 | 0.30 |
20 | 0.84 | 1.94 | 0.17 | ||||
21 | 0.67 | 1.66 | 0.27 | ||||
22 | 0.72 | 1.95 | 0.20 | ||||
23 | 0.96 | 2.11 | 0.13 | ||||
24 | 0.93 | 2.40 | 0.11 | ||||
25 | 0.94 | 2.73 | 0.08 | ||||
Cab 01 | 0.48 | 0.86 | 0.59 | ||||
Cab 02 | 0.76 | 1.48 | 0.28 | ||||
Cab 03 | 0.78 | 0.85 | 0.50 | ||||
Cab 04 | 0.54 | 0.75 | 0.61 | ||||
Cam 01 | 0.91 | 1.63 | 0.22 | ||||
Cam 02 | 0.66 | 1.69 | 0.27 | ||||
Cam 03 | 0.63 | 1.56 | 0.30 | ||||
Cam 04 | 0.81 | 1.12 | 0.37 |
Dec-03 | Evenness | Diversity | Dominance | Jan-05 | Evenness | Diversity | Dominance |
---|---|---|---|---|---|---|---|
2 | 0.61 | 1.19 | 0.37 | 1 | 0.60 | 1.82 | 0.30 |
3 | 0.53 | 1.17 | 0.37 | 2 | 0.69 | 1.43 | 0.32 |
4 | 0.71 | 0.98 | 0.42 | 3 | 0.36 | 0.71 | 0.67 |
5 | 0.69 | 1.23 | 0.35 | 4 | 0.56 | 1.09 | 0.47 |
6 | 0.75 | 1.91 | 0.19 | 5 | 0.75 | 1.66 | 0.25 |
7 | 0.59 | 1.36 | 0.38 | 6 | 0.65 | 1.72 | 0.24 |
8 | 0.60 | 1.43 | 0.32 | 7 | 0.71 | 1.15 | 0.40 |
9 | 0.68 | 1.64 | 0.28 | 8 | 0.72 | 1.67 | 0.26 |
10 | 0.68 | 1.48 | 0.30 | 9 | 0.48 | 1.19 | 0.51 |
11 | 0.77 | 1.84 | 0.20 | 10 | 0.71 | 2.34 | 0.18 |
12 | 0.70 | 1.67 | 0.24 | 11 | 0.69 | 1.95 | 0.26 |
13 | 0.82 | 1.96 | 0.18 | 12 | 0.65 | 2.04 | 0.21 |
14 | 0.58 | 1.12 | 0.43 | 13 | 0.70 | 2.14 | 0.18 |
15 | 0.94 | 1.83 | 0.18 | 14 | 0.56 | 1.16 | 0.46 |
16 | 0.84 | 1.84 | 0.19 | 15 | 0.73 | 1.43 | 0.30 |
17 | 0.76 | 1.59 | 0.27 | 16 | 0.58 | 0.93 | 0.47 |
18 | 0.91 | 1.26 | 0.31 | 17 | 0.80 | 2.25 | 0.14 |
19 | 0.95 | 1.32 | 0.28 | 18 | 0.83 | 2.54 | 0.10 |
20 | 0.45 | 0.94 | 0.56 | 19 | 0.77 | 2.04 | 0.16 |
20 | 0.76 | 1.05 | 0.40 | ||||
21 | 0.79 | 2.07 | 0.16 | ||||
22 | 0.97 | 2.90 | 0.06 | ||||
23 | 0.93 | 2.83 | 0.07 | ||||
24 | 0.94 | 2.49 | 0.09 | ||||
25 | 0.93 | 2.78 | 0.07 | ||||
Cab 01 | 0.81 | 0.89 | 0.47 | ||||
Cab 02 | 0.98 | 1.59 | 0.21 | ||||
Cab 03 | 0.88 | 1.23 | 0.33 | ||||
Cab 04 | 0.63 | 0.70 | 0.62 | ||||
Cam 01 | 0.64 | 1.54 | 0.30 | ||||
Cam 02 | 0.65 | 2.05 | 0.21 | ||||
Cam 03 | 0.59 | 1.42 | 0.37 | ||||
Cam 04 | 0.75 | 0.83 | 0.52 |
stations in terms of foraminifera species found stood out, however, it can be visualized that stations 20, Cab 1 to Cab 4, Cam 1 and Cam 4 presented differentiated fauna. A new MDS analysis disregarding the control stations (Caboto and Camamu) and station 20, was thus performed (
These samples were removed because they presented few individuals, low species numbers and the smallest diversities, suggesting that the station 20 and control areas are not environments once thought very similar to those in the RLAM area and, therefore, are not wholly comparable. Also, the lack of continual data from the control areas hampers comparison between the two consecutive years. By removing these stations from the MDS analysis, it was possible to see that in July 2004 the rest of the samples formed three groups with more similarity between stations. One group comprised stations 22, 23, 24, and 25; another one stations 1, 2, 3, 4, 5 and 6, and the last group, stations 9, 10, 11, 12, 14, 18, and 19. In December 2003, visualization of these groups was even clearer. In January 2005 (A2) it could be observed that the control stations were also less similar to those of
the RLAM subtidal area and were also removed from the analysis. In B2 the formation of main groups could be observed, similar to those groups found in July 2004 and December 2003.
In January 2005, high positive correlation was found between organic carbon and PAH (R2: 0.7603) and low positive correlation was found between the AE index and organic carbon (R2: 0.2173) (
The study of foraminifera in the RLAM subtidal area and in the control samples showed the occurrence of spe-
cies from marine environments under low continental runoff influence such as Ammonia tepida, Elphidium excavatum, Pseudononion atlanticum, Buliminella elegantissima and Quinqueloculina spp., and the presence of agglutinated forms, indicating higher continental runoff influence in certain areas. The type of fauna found in TSB indicates that the environment is dominated by marine waters. In Rehoboth Bay (Delaware, USA), [
The presence of morphological deformities in foraminifers as a response to heavy metal pollution is widely discussed in the literature ( [
The opportunistic species Buliminella elegantissima, known for its high tolerance to high organic matter content [
Our study showed that there is a slight positive correlation of AE index and organic carbon of 22%, in agreement with [
The number of species per sample increases when the environmental features are more typically marine [
The accumulation of pollutants in coastal areas does not rely entirely on the supply of these materials by rivers, but also on the chemical interaction between those elements and the sediment constituents, and are therefore reflected by the carbon and fine sediment contents, which more easily adsorb these types of particles [
Studies of foraminifera related to the pollution of Guanabara Bay [
Analysis of relative abundances suggests that the species Gaudryina exillis, Textularia earlandi, Arenoparrella mexicana, Haplophragmoides wilberti, Trochammina sp., Ammotium spp., Ammoastuta inepta, and Miliammina fusca, which occur in places more subjected to continental runoff, were grouped and are characteristic mainly of stations 1, 2, 3, 4, and 5. The marine species Uvigerina sp. is rarely found in the study region, since they are usually associated with colder water masses. Low abundance of the marine species Nonionella opima, Fissurina sp., Poreoponides lateralis, Oolina sp. Cibicides spp., Ammodiscus sp., Discorbis spp., and Triloculina sp. was also found. In January 2005 the influence of marine species was found mainly at stations 6, 12, 13, 19, 22, 23 and 25 where we can find Discorbis spp. [
High-diversity peaks were observed in the central and eastern regions of the RLAM subtidal area, while smaller values were found in the northern region close to the mouth of the Mataripe River and immediately offshore from the RLAM. That region displays a high dominance of Ammonia tepida.
In relation to evenness, there was an increase in the summer from stations 16 to 25, indicating greater environmental stability at those stations. This stability indicates that the low riverine runoff with consequent stratification break down creates environments that are healthier for foraminifera.
Our results show also that evenness is distributed along a gradient, where lower environmental stability values occur close to the RLAM and the Mataripe River continental runoff, and higher environmental stability occurs toward the ocean (stations 21 to 25) to the south. As environmental stress increases, species diversity falls, resulting in an increase of dominance [
The north-to-south diversity increase probably reflects local hydrodynamism, where the saline waters are responsible for water renovation in the southern portion of TSB. The data obtained in the present study reveal that the northern sector, including the regions close to the RLAM, are low-circulation zones, and are thus less subject to water renovation. The analysis carried out over two consecutive years shows a relative environmental stability in terms of foraminifera. The higher diversity found in the second monitoring year reflected the inclusion of stations with more marked euhaline characteristics in the RLAM subtidal area (stations 21 to 25) and therefore do not have an apparent relation to eventual interannual changes.
The region’s fluctuations in salinity and temperature established different tolerance limits for certain species, which indicate that species distribution was subject to natural environmental seasonal changes. In the present study, many marine species were observed, indicating a strong influence due to intrusion of marine waters from the adjacent continental shelf.
Given that opportunistic-tolerant species directly benefit from certain kinds of contamination (organic substances) or indirectly through the reduction of competition and predation, increasing in their occurrence, the present study reveals that the TSB study region is an environment where organic matter is easily deposited, and that the excess of nutrients results in a fauna with little diversity, dominated by Ammonia tepida in the areas closer to riverine runoff. The occurrences of Elphidium excavatum and Quinqueloculina spp. are limited to the eastern part of the area studied in TSB. Pseudononion atlanticum and Buliminella elegantissima occurred in the area under low continental runoff influence.
We thank PETROBRAS for the opportunity to sample and analyze the material discussed in the present text. We also thank FUNDESPA (Fundação de estudos e Pesquisa aquáticas) for their valuable work on the management of the project. The first author is grateful to Dr. Helenice Vital and the funding agency Capes (Coordenação de aperfeiçoamento de Pessoal de nivel superior) through the Edital Ciências do Mar 207/2010 for the Post Doc Fellowship at the Laboratório de Geologia e Geofísica Marinha e Monitoramento Ambiental da Universidade Federal do Rio Grande do Norte (GGEMMA-UFRN-Brazil) providing the means for this research to be published.
Patrícia P. B.Eichler,11,André RöschRodrigues,Evelyn da Rocha MendesPereira,Beatriz BeckEichler,AliciaKahn,HeleniceVital, (2015) Foraminifera as Environmental Condition Indicators in Todos os Santos Bay (Bahia, Brazil). Open Journal of Ecology,05,326-342. doi: 10.4236/oje.2015.57027