Foraminifera, Thecamoebians, and Bacterial Activity in ... - BioOne

Journal of Coastal Research

32

1

56–69

Coconut Creek, Florida

January 2016

Foraminifera, Thecamoebians, and Bacterial Activity in Polluted Intertropical and Subtropical Brazilian Estuarine Systems Lazaro L.M. Laut†*, Virg´ınia Martins‡, Frederico S. da Silva§, Mirian A.C. Crapez††, Luiz F. Fontana§, Sinda B.V. Carvalhal-Gomes§, and Rosa C.C.L. Souza†† †

Laboratório de Micropaleontologia, LabMicro Departamento de Ciências Naturais Universidade Federal do Estado do Rio de Janeiro, UNIRIO Rio de Janeiro, RJ 22290, Brazil

‡

Departamento de Estratigrafia e Paleontologia Universidade do Estado do Rio de Janeiro, UERJ Rio de Janeiro, RJ 20559, Brazil

§

Laboratório de Palinofaćies e Faćies ˆ Organica Departamento de Geologia Universidade Federal do Rio de Janeiro, UFRJ Rio de Janeiro, RJ 20559, Brazil

†† Departamento de Biologia Marinha Instituto de Biologia Universidade Federal Fluminense, UFF Niterói, RJ 24220, Brazil

ABSTRACT Laut, L.L.M.; Martins, V.; da Silva, F.S.; Crapez, M.A.C.; Fontana, L.F.; Carvalhal-Gomes, S.B.V., and Souza, R.C.C.L., 2016. Foraminifera, thecamoebians, and bacterial activity in polluted intertropical and subtropical Brazilian estuarine systems. Journal of Coastal Research, 32(1), 56–69. Coconut Creek (Florida), ISSN 0749-0208. This study aims to identify relationships between total organic matter (TOM), bacterial carbon (BC), and metabolic activity in the thecamoebian and foraminifera community of five estuarine regions on the Brazilian coast. Sediment samples were collected from the subtidal zone of five Brazilian estuaries: Potengi, Mataripe Sound, Para´ıba do Sul, Suru´ı, and Itacorub´ı. A total of 21 thecamoebian species, 29 species of agglutinated foraminifera, and 55 species of calcareous foraminifera were identified. In these estuaries the anaerobic process was dominant. In the Potengi Estuary, located in the NE coast of Brazil, the assemblages showed a decrease in diversity and richness as well as an increase in bacterial carbon concentrations. In the other estuaries the opposite pattern was observed, because they were dominated by agglutinated foraminifera and thecamoebians. Bacterial sulfate-reduction activity promotes acidification of the environment during organic matter degradation, and only calcareous species like Ammonia tepida, Elphidium fimbriatulum, Cribroelphidium poeyanum, Bolivina striatula, Bolivina inflata, and Nonionella opima increase their relative abundance with rising BC and TOM. Miliammina fusca, Haplophragmoides wilberti, and some species of trochamminids are associated positively with bacterial concentrations. Most of the thecamoebians species of genus Difflugia are positively related to BC, but Centropyxis aculeata is more clearly linked with total organic matter.

ADDITIONAL INDEX WORDS: Foraminifera, thecamoebians, bacteria, respiratory activities, polluted tropical estuaries.

INTRODUCTION Owing to the exponential urban growth in coastal zones, domestic sewage has become one of the main causes of pollution in marine environments. Input of sewage to the environment might occur indirectly, either by means of river systems or from point sources, such as submarine outfalls, and includes organic matter, metals, and organic pollutants (Lamparelli, 2007). Owing to the intense concern with the negative impact of pollution both for living beings in general and human health, the responses of foraminifera to pollutants are being heavily studied. Monitoring programs in coastal systems are being performed, which include not only the evaluation of pollution degree, but also the effects of pollutants in living beings. Foraminifera are, among all the benthic microfaunal organDOI: 10.2112/JCOASTRES-D-14-00042.1 received 7 February 2014; accepted in revision 2 July 2014; corrected proofs received 6 August 2014. *Corresponding author: [email protected] Ó Coastal Education and Research Foundation, Inc. 2016

isms, one of the most abundant protists in marine environments (Murray, 2000, 2001). Many studies dealing with benthic foraminifera as bioindicators of coastal pollution have recently been carried out (Boltovskoy, Scott, and Medioli, 1991; Scott, Medioli, and Schafer, 2001; Armynot du Châtelet and Debenay, 2010; Frontalini and Coccioni, 2011). These studies of pollution effects on benthic foraminifera and the possible use of these organisms as proxies to assess the environmental quality were initiated by Resig (1960) and Watkins (1961), although pollution effects on foraminifera were mentioned earlier (Zalesny, 1959). Foraminifera responses to coast pollution can include local extinctions, resulting in a barren zone where pollution levels are high, and assemblage modifications in terms of changes in composition density and diversity (Frontalini and Coccioni, 2008; Teodoro et al., 2010). However, trophic relations have been given little attention, and little is known about them regarding foraminifera and thecamoebians in coastal environments. Marine sediments are heavily colonized by microorganisms sized 150 lm.

Foraminifera, Thecamoebians, and Bacterial Activity in Polluted Estuaries

Most of them are organized in biofilms, which are complex associations of microbes also including extracellular polymeric substances secreted by cells. The organization in biofilms allows the microorganisms to create their own microhabitats and to use substrates and energy (Meyer-Reil, 1994). Bacteria represent a larger portion of the biomass in organic or inorganic substrates than any other benthic microorganisms and can be used to evaluate the degree of eutrophication. High eutrophic conditions, which are common phenomena in coastal systems, can be indicated, for instance, by the presence of strictly anaerobic sulfur bacteria (Guilizzoni, Ruggiu, and Bonomi, 1986). Degree of eutrophication may determine different choices of microhabitat by foraminifera and thecamoebians, with the development of different assemblage distribution (Van Lith, Langezaal, and Van der Zwaan, 2005). Microorganisms develop microhabitats depending on biological and physicochemical parameters that may interact positively or negatively with living beings that heavily colonize estuarine sediments (MeyerReil, 1994; Meyer-Reil and Köster, 2000). The factors that influence the distribution and abundance of benthic organisms include bathymetry, sediment texture, and physicochemical characteristics of the sediments, as well as water (Pati and Patra, 2012). However, foraminifera and thecamoebian variability-based food selection, which may include diatoms and other algae and bacteria, is still poorly understood. Murray (1963) suggested that food selectivity can vary widely between species, but this subject was seldom studied in the past and only very recently regained interest (Bernhard and Bowser 1992; Heinz et al., 2001; Moodley et al., 2002; Suhr et al., 2003; Ward, Pond, and Murray, 2003). In the case of estuarine foraminifera, it appears likely that these and many thecamoebians may feed on bacteria (Kota, Borden, and Barlaz, 1999) or on products resultant from bacterial activity. The occurrence of some thecamoebian taxa has been linked with sulfur bacteria (Asioli, Medioli, and Patterson, 1996). Souza et al. (2010) identified the influence of metabolic bacterial activity in foraminiferal assemblage distribution in estuarine systems. Arenoparrella mexicana shows high values of abundance favored by sulfate-reduction bacteria. On the other hand, the relative abundance of Ammonia tepida seems to be favored by a high percentage of total organic matter (TOM) and fermentative bacteria. Fontana et al. (2006) observed that mangrove foraminifera survive in oil-polluted sediment, because these assemblages are related to bacteria, which consume the polycyclic aromatic hydrocarbons (PAHs). Ammobaculites exiguus and Ammotium cassis showed the best response to bacterial abundance and esterase activity related to large molecular breakdown, like PAHs, whereas Quinqueloculina laevigata responds negatively to these parameters. Dissolved inorganic and organic substrates can be metabolized with high substrate affinity and specificity. Particulate organic matter can be decomposed in close contact with the substrate by microbial hydrolytic enzymes. In addition to oxygen, microbes may use alternative electron acceptors (nitrate, manganese, iron, sulfate, and carbon dioxide) for the oxidation of organic material (Meyer-Reil and Koster, 2000).

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The main goal of this study is to investigate the relationship between the distribution and composition of benthic foraminifera and thecamoebian assemblages, bacterial biomass, and respiratory activity and organic matter contents in five polluted estuaries along the Brazilian coast.

METHODS This study includes the analysis of foraminifera and thecamoebian assemblages in five estuaries along the Brazilian coast: Potengi Estuary (5840 0 S–35805 0 W, 5855 0 S–35825 0 W); Mataripe Sound (12841 00 S–38837 0 25 00 W, 12845 0 S–38830 0 30 00 W); Para´ıba do Sul Delta (21828 0 S–41802 0 W, 22801 0 S–40859 0 W); Suru´ı Estuary (22841 0 45 00 S, 43806 0 36 00 W); and Itacorub´ı Estuary (27834 0 S, 48832 0 W). Potengi River, Mataripe Sound, Paraiba do Sul, Surui Estuary, and Itacorub´ı Estuary are bordered by cities that discharge untreated sewage sludge directly into these areas. There are also many well-developed port and industrial activities nearby. Their water column and sediments are affected by a range of metals and petroleum hydrocarbons available to marine organisms (Soriano-Sierra and Ledo, 1998; Carreira, Wagener, and Readman, 2004; Fontana et al., 2006, 2010; L.L.M. Laut et al., 2007, 2011; V.M. Laut, 2011; Souza et al., 2010; Maioli et al., 2011). Potengi Estuary is bordered by three cities with a total population above 1,000,000 inhabitants. One of the cities, Natal, discharges more than 60% of its untreated sewage sludge directly into the Potengi River, and a number of port and industrial activities, including leather, textile, and paper industries, discharge effluent into the estuary (Silva, Smith, and Rainbow, 2006). Todos os Santos Bay, which includes Mataripe Sound, presents high concentrations of Al, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn. Cadmium and copper in seaweeds, oysters and seagrass, as well as Ni concentrations in oysters, were found in contaminated areas of that region. Cadmium and copper are available to the organisms through suspended particles, the dissolved fraction in the water column, and the bottom sediment interstitial water (Amado-Filho et al., 2008). Paraiba do Sul River, in SE Brazil, is affected by sugarcane monoculture practices and urbanization. A total of 16 PAHs were identified as principal pollutants by the U.S. Environmental Protection Agency (U.S. EPA) in this estuary (Maioli et al., 2011). On 17 January 2000, a 1300 m3 fuel spill affected Surui Mangrove River and several other ecosystems at Guanabara Bay. In addition, the mangrove is continuously affected by domestic sewage carried by Guanabara Bay waters and PAHs (Carreira, Wagener, and Readman, 2004). Itacorub´ı Mangrove has been seriously affected by anthropogenic activities as a result of its proximity to the city of Florianopolis. Part of the mangrove was cut to build a deposit for municipal waste, condominiums, and highways. The municipal government has also dredged artificial channels. Sewage treatment is insufficient in the area, and untreated waste is directly discharged into the creeks crossing the

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Figure 1. Estuarine polluted systems sampled for foraminiferal, thecamoebian, and bacterial studies in the tropical and intertropical Brazilian coast.

mangrove area (Soriano-Sierra and Ledo, 1998; Laut et al., 2007).

Sample Collection Forty-two sediment samples were collected with an Ekman Grab along the main channels, from the innermost to the outermost area of the mangrove forests, of five Brazilian estuarine systems (Figure 1): Potengi Estuary; Mataripe Estuary; Para´ıba do Sul Delta; Suru´ı Estuary; and Itacorub´ı Estuary. The distributional pattern of stations in the estuaries was established aiming to identify estuarine gradients (Figure 1).

The samples were collected in selected sites out of great erosion and allochthonous sediment deposition effects. In each station, a constant volume of sediment was collected in the superficial layer (0–3 cm): 50 ml for foraminiferal and thecamoebian analyses, 50 g of sediment for TOM analysis, and 10 ml for bacterial respiratory activity and bacterial carbon (BC). For foraminiferal and thecamoebian studies, sediments were stored in buffered ethanol stained with rose Bengal (2 g of Rose Bengal in 1000 ml of alcohol) to differentiate living foraminifera from dead ones (Walton, 1952).



Figure 2. Foraminifera and thecamoebian richness values (number of species) in the studied estuaries. Each estuary displayed specific faunal assemblages, which differ mainly in number of thecamoebian and foraminiferal species. The NE estuaries Pontengi and Mataripe show a great richness of calcareous foraminifera. On the other hand, the SE estuaries, Para´ıba do Sul and Surui, show a great richness of thecamoebian species.

Total Organic Matter, Bacterial Carbon Biomass, and Respiratory Activity TOM was determined through the calcination of 50 g of dry sediment at 5008C for 4 hours (Byers, Mills, and Stewart, 1978). Bacterial respiratory activity, such as aerobic activity, fermentation, denitrification, and sulfate reduction, was analyzed using the methodology described by Alef and Nannipieri (1995). Aerobic, fermentation, and denitrification growth media and sulfate-reduction growth medium contained peptone (0.2 g L1) and sodium lactate (0.2 g L1). Methylene blue solution (0.03% final concentration) and resazurin solution (0.0003% final concentration) were used as redox indicators in fermentation and sulfate-reducing growth media. Durham vials and NaNO2 (0.687 g L1) were used in denitrification growth medium. Heterotrophic bacteria were quantified by epifluorescent microscopy (Axiosp 1, Zeiss, triple filter Texas Red, 4 0 ,6diamidino-2-phenylindole, fluorescein isothiocyanate, 10003 magnification) and using fluorochrome fluorescein diacetate and ultraviolet radiation (Kepner and Pratt, 1994). Bacterial carbon biomass (lg C g1) data were obtained using the method described by Carlucci et al. (1986).

At stations PT01 (Potengi Estuary), PB05, PB06, PB10, PB11 (Para´ıba do Sul Delta), and SU02 (Suru´ı Estuary) no foraminiferal and thecamoebian tests were found. Thus, only the biotic and abiotic data results of 36 sediment samples are being analyzed in those areas. Systematic classification of foraminifera at the phylum level was based on Margulis, Schwarts, and Dolan (1999); at class and order level on Sen Gupta (1999); at genus level on Loeblich and Tappan (1987); and at the species level on several authors (Cushman and Brönniman, 1948; Todd and Brönniman, 1957; Boltovskoy et al., 1980). The thecamoebian classification was based on Kumar and Dalby (1998) and Scott, Medioli, and Schafer (2001). Considering the small number of specimens of thecamoebians (testate rhizopod), which would prevent an individualized statistical analysis, and considering the importance of this group of protozoans, they were analyzed together with foraminifera (also Rhizopoda). The species richness represents the number of total species (foraminifera þ thecamoebian) identified in each station, and the constancy values account for the number of stations where one species occurred in each study area (Tinoco, 1980). The Shannon diversity index (H 0 ) was used, which is appropriate for random samples of a community’s or subcommunity’s species of interest, and is estimated by H 0 ¼ R pi ln pi, where pi represents the portion of ith species in the sample and ln is the natural (base e) logarithm (Shannon, 1948). The software MVSP 3.1 was used for calculating the diversity (H 0 ) index.

Statistical Analysis The relative abundance data of the species (foraminifera and thecamoebian) were submitted to detrended correspondence analysis (DCA) and used to show their relationship with BC and TOM. To make a DCA analysis and calculate the percentage of variance (relative Euclidean distance) in each test, we used the software PCord 5.0. The DCA’s results of not normalized data were selected to be used in this work, since they better represent what can be observed in the data sheet than the normalized data.

RESULTS

Benthic Foraminifera and Thecamoebians Processing the benthic foraminiferal and thecamoebian samples was done according to Boltovskoy (1965). The material was washed through 0.5 mm and 0.062 mm sieves, and the other fractions were discarded. After being dried in an oven at 508C, microorganisms were separated by flotation with carbon trichloroethylene (C2HCl3). Counting was carried out under a stereo microscope, and the total number of specimens per species found in each station was registered. Living and dead individuals were counted separately to provide information on living microfauna, but total assemblages were used for the study (Debenay et al., 2001b; Debenay, Guiral, and Parra, 2002). We chose this method because (1) using total assemblages smoothes small-scale variability and (2) it is a way to circumvent the problem of Rose Bengal staining. This method for recognizing living specimens is questionable because cytoplasm may be preserved in the test for several weeks after the organism’s death (Boltovskoy and Lena, 1970; Cann and Dekker, 1981; Murray and Bowser, 2000).

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Total organic matter values ranged from 0.2% to 14.3%: Potengi Estuary (0.5–3.6%), Mataripe Sound (1.1–1.7%), Paraiba do Sul River (0.2–7.5%), Surui Mangrove River (0.3–14.3%), and Itacorub´ı Mangrove (3.6–4.5%). At the Potengi Estuary, the highest TOM content was recorded at the PT02 station, located near the shrimp farms and harbor outflow, and PT03, which receives the untreated sewage of Natal city. At Mataripe Sound, the highest values of TOM were associated with the more confined region near the refinery (stations MT01, MT02, and MT03). A total of 19 species of thecamoebians and 75 of foraminifera (27 agglutinated and 48 calcareous, with hyaline and porcelanous tests species) were identified and are shown in the Appendix. Each estuary displayed specific faunal assemblages, which differ mainly in number of thecamoebian and foraminiferal species (Figure 2). The total (benthic foraminifera þ thecamoebian) average richness index is about 34 species per estuary and vary


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between stations and estuaries. Figure 2 shows that the highest species richness was found in the Surui Estuary (48 species). The estuaries of the NE coast, Potengi and Mataripe Sound, display the highest calcareous species richness. In the other estuaries (Itacorub´ı, Surui, and Para´ıba do Sul), agglutinated foraminifera dominated the assemblages. Foraminiferal assemblages in Potengi River are dominated by A. tepida in three sites (PT02, PT03, PT04) and by A. mexicana in PT05 (Appendix). The highest diversity indices were 1.8 and 1.3, found at sites located near the mouth (PT02, PT03), and the lowest diversity index is 0.4, at the innermost sampling point (PT05) (Appendix). In the Mataripe Sound, four sampling points (MT01, MT02, MT03, MT04) were dominated by calcareous foraminifera A. tepida and Elphidium excavatum (Appendix). Ammobaculites dilatatus and A. mexicana were the dominant species in MT05. The diversity index was higher at sampling point MT04 (2.0) and lower at MT06 (0.4) (Appendix). The agglutinated foraminifera Miliammina fusca was found in 75% of the 15 samples from the Paraiba do Sul River, comprising more than 80% of the assemblage in three sampling points (PB02, PB22, PB25). Cyclopyxis spp. was the most representative thecamoebian genus found in all stations, reaching more than 77.8% at the sampling point PB08. The largest number of species was found in two sampling points (PB13, PB14), both with 13 species (Appendix). The diversity index was higher at the sampling point PB14 (2.3), followed by PB09 and PB21 (2.1), and the lowest index was identified at PB02 (0.3) (Appendix). The most abundant agglutinated species in the Surui Estuary were Haplophragmoides wilberti (23.7–50.4%), followed by A. mexicana (12.6–27.9%) and Trochamminita salsa (1.6–12%). The highest number of species was identified in the innermost sampling points (16–31 species) and the lowest at the mouth (8–19 species). The species with calcareous tests, A. tepida, found at sampling points SU03 and SU08, accounted for only 8% and 3.9% of the species, respectively (Appendix). The most frequent thecamoebians species in this estuary were Cyclopyxis aculeata (0.9–3.6%), Difflugia capreolata (0.2–4%), Pontigulasia compressa (1.4– 3.8%), and Difflugia oblonga (1.4–3.4%). The diversity index was higher at station SU03 (2.4) and lower at SU08 (1.4) (Appendix). At Itacorub´ı Estuary, several species were found, with the dominant ones being A. tepida at sampling points IT01, IT02, and IT03; A. mexicana at IT03, IT04, and IT05; and Gaudryina exilis at IT07. Miliolids were identified only at IT01, IT05, and IT06, with Quinqueloculina seminula being the most common species (12–14%). The highest numbers of species were identified in sampling points IT01, IT03, and IT06, with 12, 13, and 14 species, respectively, with IT06 having highest diversity (2.3) (Appendix). BC values varied greatly in the five estuaries, from 0.0007 to 25.969 lg C g1. The highest value of BC was found in Surui Mangrove, which varied from 2.128 to 25.696 lg C g1 (Table 1). All bacterial respiratory activities were identified after growth in specific culture media. Aerobic activity was found in sites PB12, PB13, PB14, and PB17 (Para´ıba do Sul River) and in MT01 and MT02 (Mataripe Sound). Itacorub´ı Mangrove

still has bacteria that exhibit aerobic respiration. None of the sampling points at Potengi Estuary and Surui Mangrove had aerobic bacteria (Table 1). All sediment sampling points at Potengi Estuary, Mataripe Sound, Surui Mangrove, and Itacorub´ı Mangrove showed growth of fermentative bacteria that produce organic acids. At Paraiba do Sul River, sampling points PB01 and PB09 had fermentative bacteria, but this activity was not found in other stations (Table 1). All sediment sampling points at Mataripe Sound, Paraiba do Sul River, Surui Mangrove, and Itacorub´ı Mangrove showed growth of denitrifying bacteria. The Potengi Estuary had no denitrifying bacteria activity (Table 1). All stations at Potengi Estuary, Mataripe Sound, Paraiba do Sul River, and Surui Mangrove showed growth of sulfatereducing bacteria. But sulfate-reducing bacteria were found only at the IT05 station of the Itacorub´ı Mangrove (Table 1). The DCA analyses using the relative abundance of agglutinated foraminifera, calcareous foraminifera, thecamoebians, and the diversity index (H 0 ) show that BC was the most important factor in the distribution of these organisms in axis 1. The thecamoebian group was positively influenced by the BC, and calcareous foraminifera showed a negative answer to this parameter (Figure 3). According to this analysis, TOM has a lower influence on the organisms, but this analysis also shows that the agglutinated foraminifera group has a positive answer to TOM, while the diversity index is negatively influence by this factor (Figure 3). The DCA included in Figure 4 shows the relationship between of TOM and BC and thecamoebian species. Among the thecamoebian species, this analysis shows a clear division between D. capreolata, Centropyxis constricta, Difflugia urceolata, Difflugia viscidula, Cyclopyxis spp., and Cyclopyxis impressa that are positively related to BC, whereas Centropyxis aculeata, Difflugia globulus, Lesquereusa spp., and Plagiopyx spp. are negatively related. In axis 2, D. oblonga and P. compressa showed a positive link with TOM, while Cyclopyxis spp. and C. impressa showed a negative one (Figure 4). The agglutinated species of foraminifera, Jadammina macrescens, M. fusca, Lepidodeuterammina ochracea, T. salsa, and Polysaccammina ipohalina showed a positive connection with BC and TOM. On the other hand, G. exilis, Reophax nana, Ammotium salsum, and A. cassis are negatively associated with BC and TOM (Figure 5). Calcareous foraminifera such as A. tepida, Elphidium fimbriatulum, Bolivina striatula, Nonionella opima, Bolivina inflata, Cribroelphidium poeyanum, and Ammonia parkinsoniana showed a positive connection with BC and a negative one to TOM. Triloculina spp., Miliolinella subrotunda, Q. seminula, and Quinqueloculina angulata are negatively related to BC and positively with TOM (Figure 6).

DISCUSSION The distribution of foraminifera and thecamoebians was analyzed in this study as a function of the spatial distribution of organic matter in surface sediments, and also in terms of sediment bacterial carbon content.



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Table 1. Microbiological results and ecological indices of the studied estuaries on the Brazilian coast (BC ¼ bacterial carbon, TOM ¼ total organic matter, V ¼ variable growth, P ¼ growth, N ¼ absence of growth). Bacterial Respiratory Activity Stations Potengi PT 02 PT 03 PT 04 PT 05 Mataripe MT 01 MT 02 MT 03 MT 04 MT 05 Para´ıba do Sul PB 01 PB 02 PB 04 PB 08 PB 09 PB 12 PB 13 PB 14 PB 15 PB 17 PB 19 PB 20 PB 22 PB 25 Suru´ı SU 01 SU 03 SU 04 SU 05 SU 06 SU 07 SU 08 Itacorub´ı IT 01 IT 02 IT 03 IT 04 IT 05 IT 06

Aerobic

Fermentation

Denitrification

Sulfate Reduction

BC (lg C g1)

TOM (%)

N N N N

P P P P

V V V V

P V P P

0.383 0.382 0.011 0.007

2.6 3.6 1.8 0.5

P P N N N

P P P P P

P P P P P

P P P P P

0.019 0.018 0.021 0.015 0.009

1.7 1.3 1.1 1.2 1.1

V V V V N P P P V P V V V N

P V V V P V V V V V V V V V

P P P P P P P P P P P P P V

P V P P P V P V P V P V V V

3.070 1.990 2.980 3.530 4.140 3.360 3.990 2.480 3.160 3.930 1.310 3.220 4.780 1.670

0.7 1.1 3.4 5.3 2.5 0.5 3.6 0.2 5.3 7.5 5.2 1.4 3.0 1.2

N N N N N N N

P P P P N P P

P P P P P P P

P P P P P P P

11.309 21.173 17.716 25.969 24.673 3.932 2.128

1.9 9.5 11.1 7.5 14.3 10.3 0.3

P P P P P P

P P P P P P

P P P P P P

N N V V P N

0.011 0.009 0.018 0.008 0.031 0.014

3.6 3.9 4.0 4.0 4.5 3.6

Bacterial Carbon in Estuarine Systems The BC values found at the Suru´ı River and the Para´ıba do Sul Delta (from 1.31 to 25.97 lg C g1; Table 1) were higher than other affected estuarine regions in Brazil (Silva et al., 2011). Fontana et al. (2006, 2010) also found high BC values (from 0.248 to 10.241 lg C g1) in the Suru´ı Estuary mangrove, which were related to the presence of polyaromatic hydrocarbons (PAHs) and high total organic matter concentrations. Crapez et al. (2001) found bacterial carbon ranging from 1.962 to 2.640 lg C g1 at Boa Viagem Beach, and Silva et al. (2010) found in two cores from Jurujuba Sound a BC variation from 0.004 to 0.051 lg C g1.

Foraminifera, Thecamoebians, and Bacteria The highest bacterial biomass found in the sediments of the Surui Estuary may be associated with several factors, such as the proximity to the mangrove and the load of domestic and industrial discharges within a small estuary (3 km). This estuary also held the highest foraminifera and thecamoebian

richness, whose representative species were H. wilberti and Cyclopyxis aculeata, respectively. At the Para´ıba do Sul Delta, the highest BC values are a consequence of human activities, such as sugar cane agriculture, cattle raising, and domestic and industrial discharges (Silva et al., 2011; L.L.M. Laut et al., 2011). At the Potengi Estuary, the highest BC concentrations were recorded at the PT02 station located near the shrimp farms and harbor outflow, and the PT03 station (Figure 1), which receives the untreated sewage of the city of Natal. At Mataripe Sound, the highest BC values were matched to the most confined region near the refinery (stations MT01, MT02, and MT03). The BC values found at Itacorub´ı Estuary were the lowest. The highest concentration in this estuary was found only at the IT05 station on the sanitary landfill margin. In the Potengi Estuary and the Mataripe Sound, where the sediments have relatively low concentrations of organic matter, foraminiferal assemblages were dominated by calcareous foraminifera, with A. tepida being the main species. Our


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Figure 3. DCA analysis showing the importance of total organic matter (TOM) and bacterial carbon (BC) for the organisms. The BC was the most important factor in the distribution of organisms. The thecamoebian group was influenced positively by the BC, while calcareous foraminifera displayed an opposite trend. The diversity index shows the opposite trend in relation to TOM.

results based on total assemblage do not reflect what lives in the sediments as BC does; however, they showed a different relationship between A. tepida and sediment organic matter content than those found by Debenay et al. (2001a). These authors observed that a higher proportion of A. tepida can be found in the more impacted northern part of the lagoon of Araruama due to the input of nutrients by human activities. This species usually dominates in coastal systems where the

Figure 4. DCA analysis showing the total organic matter (TOM) and bacterial carbon influence on thecamoebian species. This analysis shows a clear division between Difflugia capreolata, Centropyxis constricta, Difflugia urceolata, Difflugia viscidula, and Cyclopyxis spp., which are related positively to BC, and Centropyxis aculeata, Difflugia globulus, Lesquereusa spp., and Plagiopyx spp., which are negatively related. In axis 2, Difflugia oblonga and Pontigulasia compressa showed a positive response to TOM, while Cyclopyxis spp. and Cyclopyxis impressa displayed a negative response.

Figure 5. DCA analysis showing the total organic matter (TOM) and bacterial carbon influence on agglutinated foraminifera species. The species Jadammina macrescens, Miliammina fusca, Lepidodeuterammina ochracea, Trochamminita salsa, and Polysaccammina ipohalina are positively related to BC and TOM. On the other hand, Gaudryina exilis, Reophax nana, Ammotium salsum, and Ammotium cassis are negatively connected with BC and TOM.

sediments are enriched by organic matter (Carnahan et al., 2009). However, Burone and Pires-Vanin (2006) consider A. tepida a generalist species. Languezaal et al. (2005) noted that Ammonia does not develop symbiosis with bacteria and that it performs extracellular digestion of the preyed cells. The increase of the relative abundance of A. tepida while BC also increase was observed in all the studied estuarine systems,

Figure 6. DCA analysis showing the total organic matter (TOM) and bacterial carbon influence on calcareous foraminifera species. The species Elphidium fimbriatulum, Bolivina striatula, Nonionella opima, Bolivina inflata, Cribroelphidium poeyanum, and Ammonia parkinsoniana are positively associated with BC and negatively with TOM. Triloculina spp., Miliolinella subrotunda, Quinqueloculina seminula, and Quinqueloculina angulata are connected negatively with BC and a positively with TOM.



which agrees with the observations of Languezaal et al. (2005). It is possible that Ammonia spp. have benefited from the abundance of small biomolecules resulting from the bacterial metabolic degradation of organic matter. The distribution of other calcareous species (E. fimbriatulum, B. striatula, B. inflata, C. poeyanum, and A. parkinsoniana) common in Brazilian estuaries, bays, and lagoons is always correlated to organic matter concentration (Burone and Pires-Vanin, 2006; Souza et al., 2010, Teodoro et al., 2010; L.L.M. Laut et al., 2011, Vilela et al., 2011; Donnici et al., 2012). This work shows for the first time the relationship between these species and bacterial carbon concentration. The DCA analysis included in Figure 6 suggests that these species display a positive response to the increase of this parameter. Agglutinated species like Trochammina macrescens, L. ochracea, T. salsa, and Trochammina squamata also increase their relative abundance where BC and TOC increase (according to the DCA analysis; Figure 5). These species are grazers (herbivorous) that respond positively to fermentative activities in aerobiosis (V.M. Laut et al., 2011). Miliammina fusca, a common species in brackish waters, also are present and become more abundant in sediments enriched in BC and TOM. L.L.M. Laut et al., (2011) also reported the link between this species and a high concentration of bacterial carbon. A symbiotic relationship between A. mexicana and sulfatereducing bacteria was suggested by Laut et al. (2007). However, this species tend to decrease as the amount of BC and TOM enhance, according to the DCA of Figure 5. The type of bacterial metabolism has been analyzed at each studied site, and the obtained data are presented in Table 1. Since these data are qualitative, they were not used in the DCA analysis. On the other hand, the BC values include all bacterial metabolic activity in the sediment, and for this reason it was not possible to identify any relationship between A. mexicana and this variable. Thus the results obtained in this work do not evidence the symbiotic relationship recognized by Laut et al. (2007). Organic matter content and bacterial metabolism are interconnected and are crucial in the process of diagenesis. Benthic bacteria have an anaerobic metabolism, such as fermentative, denitrifying, and sulfate-reducing, indicating reducing conditions in the five estuarine sediments. Aerobic bacteria, which are grown in specific culture medium in the laboratory, perform the fermentative metabolism in the sediments of these estuaries. In all the studied estuaries, living foraminifera were found in dysoxic conditions. A similar situation was also observed by several authors (Moraes et al., 1993; Bernhard and Sen Gupta, 1999; Souza et al., 2010; L.L.M. Laut et al., 2011). The results indicated the possibility that some species are able to live under dysoxic conditions, like Bernhard (2003) suggests, when they are associated with sulfate-reducing bacteria, although lack of oxygen is supposed to be a limiting factor for most species (Langezaal, van Bergen, and van Zwaan, 2004). Foraminifera probably feed on a wide range of food particles, which are part of complex microbial-based food webs that include dissolved organic matter, bacteria, and predation of

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small organisms. This helps to transfer and eventually dissipate most of the solar energy that is initially captured during photosynthesis (Karl, 2007). A complex microbial food web can be inferred analyzing DCA results in Figures 4, 5, and 6. In estuaries with higher concentrations of organic matter and bacterial carbon, such as in Surui Mangrove River and Para´ıba do Sul River, most of the species of agglutinated foraminifera and thecamoebians benefit from the food supply provided by heterotrophic and anaerobic bacterial biomass. In estuaries with lower concentrations of organic matter and bacterial carbon, such as Potengi Estuary, Mataripe Sound, and Mangrove Itacorub´ı, most of the calcareous foraminifera species seem to prefer the intake of anaerobic and heterotrophic bacterial biomass as source of carbon and energy. It is known that bacteria are often consumed by foraminifera (Goldstein and Corliss, 1994; Ernst et al., 2005; Langezaal et al., 2005; Mojtahid et al., 2011), and several littoral benthic foraminifera require bacteria to reproduce (Muller and Lee, 1969). Foraminifera are also able to feed actively on bacterial biofilms (Bernhard and Browser, 1992), and some epiphytic foraminifera have adopted a farming strategy, producing nutrient-rich substrata and then ingesting cultured bacteria (Langer and Gehring, 1993). This study represents a first attempt at recognizing the relationship between estuarine species of foraminifera, thecamoebians, and bacteria. The discussion established here is based on total assemblages that represent time-averaged assemblages that might have been altered by different processes, including transport specimens throughout the estuaries. The application of methodologies established by the foraminiferal bio-monitoring protocol (Schönfeld et al., 2012), which used only live specimens, will bring additional and more reliable contributions on the understanding of the relationships between these groups of protozoa and bacterial activity (Murray, 2000, 2001).

CONCLUSIONS The distribution pattern of thecamoebians and calcareous foraminifera demonstrates that they are able to live in reducing sediment colonized by heterotrophic anaerobic bacteria in stressed shallow marine environments. This work shows that the bacterial biomass, as well as their respiratory activities, played an important role on the distribution, richness, and diversity of the foraminiferal and thecamoebian assemblages. The estuaries composed of agglutinated foraminifera and thecamoebians presented an increasing tendency in ecological indexes when BC values were high. The NE Region estuaries, dominated by calcareous (hyaline and porcellaneous) foraminiferal assemblages, presented a decreasing tendency for these indices. This work is a first attempt at establishing some relationship between some foraminifera and thecamoebian species and bacterial respiratory activities in the estuarine regions of Brazil. More detailed studies are needed to investigate the possible symbiotic relationships and food selectivity of the species in question and to understand the foraminiferal ecological dynamics in polluted environment.


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Table A2. Mataripe Sound

APPENDIX A. ECOLOGICAL INDICES OF ESTUARINE SYSTEMS STUDIED

Mataripe Sound

Table A1. Potengi Estuary Potengi Estuary

PT02

PT03

PT04

PT05

Density of tests (50 ml) Number of species (50 ml) Number of stained tests (50 ml) Shannon Diversity Index (H 0 ) Ammobaculites dilatatus Ammobaculites exiguus Ammonia tepida Ammotium cassis Ammotium salsum Arenoparrella mexicana Bolivina doniezi Bolivina inflata Bolivina compacta Bolivina spatulata Bolivina spp. Bolivina translucens Buliminella elegantissima Cornuspira incerta Cornuspira planorbis Discorbis williamsonii Elphidium discoidale Elphidium excavatum Fissurina lucida Fursenkoina pontoni Haynesina germanica Lagena laevis Lagena perlucida Lagena spiralis Lagena striada Miliolinella subrotunda Nonionella opima Oolina vilardeboana Pseudononion atlanticum Quinqueloculina cf. tenagus Quinqueloculina laevigata Quinqueloculina lamarckiana Quinqueloculina seminula Quinqueloculina spp. Rosalina bradyi Rutherfordoides sp. Siphotrochammina lobata Spiroculina sp. Textularia earlandi Trochammina macrescens Trochammina inflata Trochamminita salsa Uvigerina peregrina Wiesnerella aviculata

304 24 90 1.8 — — 52.9 — — — — 0.6 0.3 — — 1 — 0.6 1.6 — 3 5 0.3 1.3 — 0.3 0.3 0.3 0.3 20 0.3 0.3 2.3 — 3.2 2.2 1.3 — 0.3 0.3 — — 0.3 1 — — — 1

116 13 18 1.3 — — 68 — — — — — — — 3.4 — 3.4 — — 0.9 4.3 8.5 0.9 0.9 — — — — — 2.6 — — — 0.9 1.7 — — — — — — 3.4 — — — — 0.9 —

485 15 94 0.8 — — 83.1 0.4 — — 1.4 — — 0.2 1.4 1 0.2 — — — 0.2 8.7 — — 0.4 — — — — — —

158 3 6 0.4 8.2 — — — — 89.8 — — — — — — — — — — — — — — — — — — — — — — — — — — — — — — 2 — — — — — — —

— — 0.2 — 1 0.2 — — — — 0.2 1.2 — — — —

MT 01 MT 02 MT 03

MT 04

MT 05

Density of tests (50 ml) 2100 2400 1559 1962 2000 Number of species (50 ml) 15 19 9 17 14 Number of stained tests (50 ml) 735 840 140 215 360 1.5 1.7 1.3 2 1.7 Shannon Diversity Index (H 0 ) Ammobaculites dilatatus 2.4 12.8 10.8 — 44.6 Ammobaculites exiguus — 2.4 1.4 — 4.1 Ammobaculites spp. — — — — 28 Ammonia parkinsoniana 1.4 3.12 — — — Ammonia tepida 52 46.8 49.3 45.7 — Ammotium salsum 0.3 — — — 4.8 Arenoparrella mexicana — 0.3 — — 3 Bolivina doniezi — — — 1.2 — Bolivina inflata — — — 3.5 — Bolivina striatula 4.5 2.1 — 7.8 — Bolivina sp. A 0.3 — — — — Bolivina sp. B 0.3 — — — — Buliminella elegantissima 1.7 0.3 — 1.2 — Cibicides spp. — — — 0.4 — Discorbis spp. 0.7 — — — — Elphidium advenum — — — 0.8 — Elphidium bartletti — — — 1.2 — Elphidium discoidale 0.3 1.4 0.7 0.4 — Elphidium excavatum 23.5 8.7 5.1 12.4 — Elphidium fimbriatulum — 1 — 1.9 — Elphidium galvestonensis 0.7 — — — — Elphidium gunteri — 2.4 2 0.8— — Elphidium translucens — 0.3 — — — Elphidium cf. poeyanum — 0.6 — 5.8 — Elphidium spp. — 0.3 — — — Elphidium sp. A — 0.3 — — — Fursenkoina pontoni — — 0.3 0.4 — Gaudryina exilis 8.3 14.58 29.6 0.4 0.4 Nonionella auris 0.4 — — — — Nonionella opima 0.4 — — 1.5 — Pseudononion atlanticum 1.9 — — 7 0.4 Quinqueloculina seminula 0.3 — — — — Reophax nana — — 0.7 — 5.2 Reophax sp. A — 0.34 — — — Siphotrocammina lobata — — — — 0.7 Textularia earlandi — — — — 0.7 Textularia paranaguaensis — — — 1.9 1.1 Trochammina inflata — — — — 0.4 Trochamminita irregularis — — — — 1.5 Trochamminita salsa — — — — 5.2


PB01

PB02

PB03

PB04

PB07 PB08

PB09

PB12

PB13

PB14

PB15

PB16 PB17 PB18 PB19 PB20

PB21

PB22

PB23

PB24 PB25

Density of tests (50 ml) 1420 3970 860 1020 130 270 1390 180 1230 1470 1690 390 930 350 100 180 2950 960 2830 930 810 Number of species (50 ml) 12 6 10 8 4 3 10 6 13 13 11 6 10 7 5 5 13 10 6 11 6 Number of stained tests (50 ml) 20 600 20 70 30 20 20 20 20 90 51 23 49 11 0 0 42 103 6 19 62 Shannon Diversity Index (H 0 ) 1.7 0.3 1.7 1.4 1.1 0.7 2.1 1.6 2 2.3 1.5 1.3 1.7 1.5 1.4 1.4 2.1 0.8 0.7 1.9 0.6 Ammonia tepida — — — — — — — — — — — — — — — — 4.1 — — 2.2 — Ammotium salsum — — — — — — — — — — — — — — — — — — 2.5 — 1.2 Arenoparrella mexicana — 0.3 2.3 — — — — — — — 1.2 2.6 2.2 — — — — 3.1 23 14 4.9 Elphidium gunteri — — — — — — — — — — — — — — — — 0.7 — — — — Haplophragmoides wilberti — 0.3 1.2 6.9 — — — — 0.8 2 — — 5.4 8.6 — — — — — 14 1.2 Jadammina polystoma — — — — — — — — 1.6 — — — — — — — — — — — — Miliammina fusca 28.8 93.4 2.3 2 — — — — — 6.1 59.8 53.8 49.5 40 30 5.6 14.6 81.3 73.5 28 84 Polysaccammina ipohalina — — — 23.5 — — — — — 12.9 2.4 7.7 — 2.9 — — — — 0.4 — — Siphotrochammina lobata — — — — — — — — — — 5.3 — — — — — — — — — — Textularia earlandi 0.7 — — — — — — — — — — — — — — — — — — — — Trochammina inflata — — — — — — — — — — 5.9 — — — — — — — — — — Trochammina macrescens 3.5 — — — — — — — — — — — — 5.7 — — — — — 1.1 — Trochammina ochracea 1.4 — — — — — — — — — — — — — — — 0.3 — — — — Trochamminita irregularis — — — — — — — — — 4.1 — — — — — — — — — — — Trochamminita salsa — — — 51 — — — — 1.6 9.5 — — 12.9 — — — 0.7 1 — 10.8 2.5 Arcella discoides 0.7 — — — — — — — — — — — — — — — — — — — — Centropyxis constricta 4.9 — 12.8 9.8 7.7 — 13.7 22.2 8.9 11.6 2.4 — 4.3 8.6 — — 9.5 1 — — — Centropyxis spp. 2.8 2 — — — — — — 17.9 — 8.3 — — — — 38.9 — — — — — Cucurbitela corona 1.4 — 8.1 2 7.7 — 7.9 16.7 16.3 4.8 0.6 — 3.2 — 10 16.7 7.8 2.1 — — — Cucurbitela tricuspis — — — — — — — — — — — — — — — — 0.3 — — — — Cyclopyxis impressa — — — — — — 5 — — — — — — 31.4 — — — — — — — Cyclopyxis spp. 33.8 1.3 34.9 — 30.8 77.8 15.8 27.8 28.5 27.2 — 20.5 11.8 — 40 — 33.6 6.3 0.4 21.5 6.2 Difflugia correntina — — — — — — — — 0.8 — — — — — — — — — — — — Difflugia capreolata — — — — — — 10.8 22.2 0.8 6.8 7.1 12.8 — — 10 — 6.8 2.1 — 1.1 — Difflugia oblonga — — 7 — 53.8 — 24.5 — 1.6 — 1.2 — 4.3 2.9 — 11.1 — 1 0.4 — — Difflugia urceolata — — — — — 7.4 7.2 — 4.1 1.4 — 2.6 1.1 — — — 5.1 1 — — — Difflugia viscidula 19.7 2.8 1.2 2 — — 0.7 5.6 — 6.8 — — — — — — 8.1 — — 1.1 — Lagenodifflugia vas 2.1 — 1.2 — — — 5 5.6 4.1 3.4 — — — — — — — 1 — 2.2 — Oopyxis spp. 0.7 — — — — — — — — — — — — — — — — — — — — Pontigulasia compressa — — 29.1 2.9 — 14.8 9.4 — 13 3.4 5.9 — 5.4 — 10 27.8 8.5 — — 4.3 —

Para´ıba do Sul Delta

Table A3. Para´ıba do Sul Delta



67

68

Laut et al.

Table A4. Surui River Estuary Surui River Estuary

SU01

SU03

SU04

SU05

SU06

SU07

SU08

Density of tests (50 ml) Number of species (50 ml) Number of stained tests (50 ml) Shannon Diversity Index (H 0 ) Acupeina triperforata Ammoastuta inepta Ammoastuta salsa Ammobaculites dilatatus Ammobaculites exiguus Ammonia tepida Ammotium cassis Ammotium pseudocassis Ammotium salsum Arenoparrella mexicana Elphidium gunteri Haplophragmoides manilaensis Haplophragmoides wilberti Jadammina polystoma Miliammina fusca Paratrochammina clossi Polysaccammina ipohalina Pseudothuramina limnetis Reophax nana Saccammina sphaerica Siphotrochammina lobata Textularia earlandi Textularia paranaguaensis Tiphotrocha comprimata Trochammina inflata Trochammina macrescens Trochammina squamata Trochamminita irregularis Trochamminita salsa Apodera vas Centropyxis constricta Curcubitella corona Cyclopyxis impressa Cyclopyxis spp. Difflugia correntina Difflugia caprelota Difflugia globulus Difflugia urceolata Difflugia viscidula Difflugia oblonga Lagenodifflugia vas Lagunculina urnala Lesquereusia spp. Pontigulasia compressa Plagiopyxis spp. Oopixis

661 19 0 1.9 — 0.5 — 1.4 8.1 — — — 6.1 13.8 — — 46.5 — — 0.2 0.2 — — — 2.3 4.3 1.8 0.5 9.7 0.5 0.2 0.2 3.4 — — — — — — 0.2 — — 0.2 — — — — — — —

854 29 2 2.4 — 1.2 0.2 — 0.2 8 0.2 — 5.2 12.6 1.6 0.5 37 0.2 — — 2.3 — 0.2 — 0.7 3.7 0.9 — 6.1 1.4 — 1.6 6.8 — 0.9 0.9 — — — 0.9 — 0.2 1.2 2.6 — — — 1.4 0.5 0.5

500 30 0 2.3 0.2 1.4 — — — — — 0.2 5.2 15.2 — 1.4 39.2 0.4 — 0.8 4.2 0.2 — 0.6 1.4 2.6 — 0.6 3.6 1 — 1.8 6.8 — 3.6 0.6 0.4 0.4 — 0.2 — 0.2 2.8 1.4 0.6 — — 2.6 0.4 —

323 30 0 2.5 — 0.3 0.9 — 0.6 — 0.3 — 7.7 14.9 — 1.5 33.7 1.5 — 0.3 3.7 — — — 2.5 1.2 0.6 — 3.1 0.3 — 3.1 8 1.2 1.9 1.5 — — 0.3 0.6 — 0.3 1.2 3.4 1.9 — 0.3 1.5 1.2 —

448 31 0 2.5 — — 0.4 0.2 — — 0.7 — 5.6 15 — 0.4 32.4 0.7 0.9 0.7 5.4 — — — 2.7 0.9 0.9 — 4.2 1.6 — 0.4 6.9 — 1.6 2.5 — 0.4 — 4 1.6 0.2 0.2 2.5 1.1 0.7 0.2 3.8 1.3 —

131 16 0 2.2 — — — — — — — — 0.8 21.4 — 0.8 23.7 0.8 7.6 4.6 — — — — 3.8 1.5 — 1.5 9.9 6.1 3.8 — 11.5 — 1.5 — — — — — — — — — — — — — 0.8 —

129 8 8 1.4 — — — — — 3.9 — — 8.5 27.9 — 2.3 50.4 — — — — — — — — 1.6 — — 3.9 — — — 1.6 — — — — — — — — — — — — — — — — —



69

Table A5. Itacorub´ı River Estuary Itacorub´ı River Estuary

IT 01

IT 02

IT 03

IT 04

IT 05

IT 06

IT 07

Density of tests (50 ml) Number of species (50 ml) Number of stained tests (50 ml) Shannon Diversity Index (H 0 ) Acupeina triperforata Ammoastuta inepta Ammoastuta salsa Ammonia tepida Arenoparrella mexicana Bolivina striatula Buliminella elegantissima Discorbinella berthelotti Elphidium discoidale Elphidium excavatum Elphidium gunteri Elphidium spp. Gaudryina exilis Haplophragmoides manilaensis Haplophragmoides wilberti Jadammina polystoma Miliolinella sp. A Miliolinella subrotunda Quinqueloculina lamarckiana Quinqueloculina seminula Quinqueloculina polygona Pseudononion atlanticum Siphotrochammina lobata Textularia earlandi Triloculina sp. A Trochammina inflata Trochammina macrescens Trochammina squamata Trochamminita irregularis Trochamminita salsa Centropyxis aculeata Difflugia globulus

6770 12 180 1.2 — 0.3 — 57 3 0.3 5 — — 24.3 8 — 0.6 0.3 — — — — — — 0.3 — — — — — 0.3 — 0.3 — — —

640 7 0 1.3 — — — 49 16 — — — — 3 26 — — — 2 2 — — — — — — — — — — 2 — — — — —

210 13 0 2.5 — — — 14 14 — — — — 5 — — 5 — 10 5 5 9 — 14

940 9 80 1.4 — — 2 13 55 — — — — 3 10 — — — 13 1 — — — — — — — — — 1 0 — 2 — — —

2880 9 0 0.8 — 1 0.5 — 80 — — — — — — 0.3 — — 12 0.7 — — 0.5 — — — — — — 4 1 — — — — —

520 14 0 2.3 2 — — 11 22 — 11 2 13 8 11 — — — — — — — 4 12 3 2 — — — — 0 — — — 2 2

280 8 10 1.7 — — — — 22 — — — — — — — 41 3 10 3 — — — — — — — 10 — 7 0 4 — — — —

— 5 — 5 — 0 — — 9 5 —
