Mar Biodiv DOI 10.1007/s12526-014-0243-2
DIVERSITY OF MARINE MEIOFAUNA ON THE COAST OF BRAZIL
Foraminiferal and testate amoeba diversity, distribution and ecology in transitional environments of the Tramandaí Basin (Rio Grande do Sul, South Brazil) Itamar Ivo Leipnitz & Fabricio Ferreira & Carolina Jardim Leão & Eric Armynot du Châtelet & Fabrizio Frontalini
Received: 21 December 2013 / Revised: 6 May 2014 / Accepted: 7 May 2014 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2014
Abstract In order to document benthic foraminiferal and testate amoeba diversity, a total of 115 sediment samples were collected from nine different transitional environments along a 100-km long coastal area located in Rio Grande do Sul (Brazil). This area is directly affected by both the input of freshwater from the Tramandaí River and a marine influence due to its proximity to the Atlantic Ocean. In particular, 14 and 101 species are recognized within the benthic foraminiferal and testate amoeba assemblages, respectively. Testate amoebae diversity is significantly higher than that documented in previous investigations carried out in other parts of the Electronic supplementary material The online version of this article (doi:10.1007/s12526-014-0243-2) contains supplementary material, which is available to authorized users. I. I. Leipnitz : C. J. Leão ITT FOSSIL—Instituto de Micropaleontologia da Universidade do Vale do Rio dos Sinos (UNISINOS), Avenida Unisinos, 950, 93022-000 São Leopoldo, RS, Brazil I. I. Leipnitz Programa de Pós-graduação em Geologia da Universidade do Vale do Rio dos Sinos (UNISINOS), Avenida Unisinos, 950, 93022-000 São Leopoldo, RS, Brazil F. Ferreira Fundação Euclides da Cunha (FEC)/Laboratório de Geologia Marinha (LAGEMAR), Instituto de Geociências, Universidade Federal Fluminense (UFF), 4o andar, Av. Gal. Milton Tavares de Souza s/n, 24210-346 Niterói, RJ, Brazil E. Armynot du Châtelet Université Lille 1, UMR 8217 CNRS Géosystèmes, UFR Sciences de la Terre, Bât. SN5, Avenue Paul Langevin, 59655 Villeneuve d’Ascq, France F. Frontalini (*) DiSTeVA, Università degli Studi di Urbino “Carlo Bo”, Campus Scientifico Enrico Mattei, Località’ Crocicchia, 61029 Urbino, Italy e-mail:
[email protected]
Brazilian coast. The two dominant testate amoeba families are Difflugidae and Hyalospheniidae, which are represented by 74 and 9 species, respectively. On the other hand, the benthic foraminiferal assemblages are poorly diversified and mainly dominated by agglutinated forms that are typical of transitional environments under the direct influence of a freshwater input. The distribution of these two groups characterizes both the freshwater environments, where testate amoebae are the only representatives, and the more marine conditions, where benthic foraminifera tend to dominate the benthic community, and allows the recognition of a marine influence gradient. The benthic foraminiferal assemblages are mainly observed in front of the direct opening to the sea, but are completely absent in the innermost environments, whereas testate amoebae are more widely distributed, albeit in variable abundances, but are completely missing close to the Tramandaí Basin’s outlet. Although the diversity of the benthic community in South Atlantic coastal regions is difficult to determine, this study represents, to our knowledge, the first investigation of benthic foraminifera and testate amoebae along the 100-km long coastal area, characterized by lagoons and lakes interconnected by canals and small rivers. Keywords Thecamoebians . Foraminifera . Distribution . Ecology . Tramandaí . Rio Grande do Sul coastal plain . South Brazil
Introduction Foraminifera are marine protozoa that have the advantage of possessing mineralized and agglutinated tests that are preserved in sediment. They live in marine and brackish waters and have been used as environmental indicators since 1959 (Zalesny 1959). They are small in size and often numerous in
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small volumes of sediment, providing a large database that is suitable for environmental characterization. Moreover, they react quickly to environmental change, whether natural or anthropogenic. In coastal areas, benthic foraminiferal species live in equilibrium with many parameters such as organic matter quantity and quality (Armynot du Châtelet et al. 2009), sediment size (Armynot du Châtelet et al. 2009, 2013), and oxygen content (Alve 1995; Kaminski 2012). Benthic foraminiferal assemblages might be also negatively influenced by pollution (Armynot du Châtelet and Debenay 2010; Frontalini and Coccioni 2011). They might respond to adverse conditions either natural or anthropic in origin by changing density and diversity, assemblages’ composition, reproduction capability, test morphology, including size (dwarfism), prolocular morphology, ultrastructure, pyritization, abnormality, and chemistry of the test (Frontalini et al. 2009). They might be used, therefore, as bioindicators of environmental conditions in marine and transitional marine ecosystems. Testate amoeba (also known as thecamoebians) is an informal term used to designate a group of unicellular organisms that have their origins in the Precambrian seas (Porter and Knoll 2000; Porter et al. 2003; Knoll 2014). These organisms are protozoa that build a simple unilocular agglutinated or organic shell or test in which the cell is enclosed. They live in various freshwater environments, such as peat land, rivers, lakes, and brackish-water settings (Porter and Knoll 2000; Charman 2001; Patterson and Kumar 2002; Duleba et al. 2005). Like foraminifera, testate amoebae live in equilibrium with the environmental conditions, and many factors control their abundance and assemblage types, including nutrition, oxygen availability, pH, salinity, substrate, temperature, subaerial exposure, or floral substrates (Scoot et al. 2001). They normally occur in large amounts, even when only small numbers of samples are available. They are also widely diversified and specialized, and are easy and inexpensive to collect (Scoot et al. 2001). All of these features make thecamoebians ideal bioindicators of environmental conditions in freshwater ecosystems. Studies on testate amoebae in Brazil have been conducted using two different approaches: (1) research focusing on benthic foraminifera in estuarine waters and coastal plains, in which testate amoebae are used as indicators of freshwater influence (Closs 1962; Closs and Madeira 1967; Closs and Medeiros 1967; Madeira-Falceta 1974; Zucon and Loyola e Silva 1992; Barbosa 1995; Eichler-Coelho et al. 1996, 1997; Bonneti and Eichler 1997; Oliveira 1999; Duleba and Debenay 2003; Semensatto and Dias-Brito 2004); (2) research in freshwater bodies within the continent that focus on the testate amoebae present in plankton, aquatic macrophytes and Sphagnum (Lansac-Tôha et al. 1992, 1993; Hardoim and Heckman 1996; Velho and Lansac-Tôha 1996; Velho et al. 1996, 1999; Rhoden 1996; Torres 1996; Hardoim 1997; Lansac-Tôha et al. 1997; Dabés and Velho 2001; Bini
et al. 2003; Azevedo and Bonecker 2003; Cardoso and Marques 2004). Both foraminifera and thecamoebians are found in brackish ecosystems. Changes in the diversity, abundance and distribution of these groups can reflect the occurrence of different environments or the influence of some parameters of water and sediment like salinity, pH, temperature, dissolved oxygen, grain-size organic matter, hydrological parameters, wind and tidal regime in the region (Scott et al. 1977, 1980, 1991; Colins et al. 1990; Boltovskoy et al. 1991; Schafer et al. 1991; Barbosa 1995; Bonneti and Eichler 1997; Debenay et al. 1998, 2001a; Patterson 2002; Duleba et al. 2005; Debenay and Luan 2006). Even though several studies of benthic foraminiferal and testate amoeba assemblages have been carried out in different parts of the world in a very wide range of environments, to our knowledge only few studies have been conducted in Southern Atlantic coastal areas in mixed environments that are both influenced by the sea and continental waters and on a scale that is larger than a few hundred meters to a few kilometers (i.e., Closs and Madeira 1962, 1967; Eichler-Coelho et al. 1997). The main objectives of this study were: (1) to document for the first time the foraminiferal and testate amoeba assemblages (composition, abundance and diversity) in a 100-km coastal area of the Rio Grande do Sul area (Brazil) that experiences freshwater and marine water influences, and (2) to underline the main factors influencing the distribution of these two assemblages.
Study area The coastal plain of Rio Grande do Sul extends about 640 km along the southern coast of Brazil, which corresponds to the surface geomorphological expression of the Pelotas Basin. Located between 29°12′, 33°48′S and 49°40′, and 53°30′W, this coastal plain has an estimated total surface area of over 37,000 km2, with 14,260 km2 corresponding to lakes, ponds and rivers (Schawrbold and Schäfer 1984; Tomazelli and Villwock 1991; Travessas et al. 2005; Tomazelli et al. 2007) (Fig. 1). The region formed during the transgressiveregressive processes of the Quaternary period with the development of the barrier lagoon system that was responsible for the formation of four barriers (I, II, III and IV) as a result of the emergence of the alluvial fan system in its inner portion and are responsible for their lateral development. The formation of the first three barriers occurred during the Pleistocene and the fourth during the Holocene (Villwock and Tomazelli 1995; Dillenburg et al. 2000; Tomazelli and Villwock 2000; Travessas et al. 2005; Villwock et al. 2005). Part of the northern coast of Rio Grande do Sul state was formed by a sequence of transitional environments (e.g., lagoons and lakes) parallel to the ocean coast. These lagoons and lakes are interconnected by canals and small rivers which comprise
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the large Tramandaí Basin (Freitas 2003). This basin has a drainage area of approximately 2,540 km2, of which 450 km2 is surface water coverage (Freitas 2003). The basin can be subdivided into two hydrographic subsystems where the Tramandaí River represents the line of separation. The estuary of the Tramandaí Basin (Tramandaí and Armazém lagoons) is under the influence of a micro-tidal regime, with waters ranging predominantly between mixohaline and freshwater, with the average salinity being within the limits of mixohaline to oligohaline waters (0.5–5‰). These variations are due to the actions of several environmental factors, including the hydrological, wind and tidal regime in the region (Closs and Madeira 1967; Madeira-Falceta 1974; Schawrbold and Schäfer 1984; Dillenburg 1994; Villwock and Tomazelli 1995; Fepam 2000; Freitas 2003). Wind is the modifier of the geomorphology physical agent with the greatest influence on water bodies in the region, with the area towards the northeast being more prominent (Tomazelli 1993; Machado 2000). The river basin permanently connects Tramandaí lagoon with the ocean through the inlet area, which has constantly changed its position due to the intense action of the winds and numerous sand dunes that were present. However, the channel connecting with the ocean was stabilized through the construction of artificial barriers (Madeira-Falceta 1974; Villwock and Tomazelli 1995). According to the Köppen classification system, the area is characterized by a humid subtropical climate, with an average annual temperature of around 20 °C and rainfall of about 1,300 mm (Salomoni 1997). The margins of its lagoons and ponds have fixed floating vegetation that is characterized by herbaceous species (Wilberger 2004). The margins of the Tramandaí and Armazém lagoons and the Barra region (inlet) are bounded by an urban area. Salomoni (1997) reports that the coastal plain of Rio Grande do Sul has had problems with the contamination of water due to the increasing effects of urbanization. In this system, nine lagoons and lakes have been considered herein: Itapeva Lake (IL), Quadros Lake (QL), Passo Lake (PL), Tramandaí Lagoon (TL), Armazém Lagoon (AL), Custódia Lake (CL), Gentil Lake (GL) and Manuel Nunes Lake (MNL) (Fig. 1). The Tramandaí River (TR) is also considered and subdivided into two sections, TR1 and TR2, which are respectively to the north and south of Lake Passo (Fig. 1).
Material and methods Sampling A total of 115 sediment samples were collected in March 2003 from these nine transitional environments. In particular, 22
samples from IL, 22 from QL, 9 from PL, 19 from TL, 7 from AL, 8 from CL, 8 from GL, 5 from MNL, 7 from TR1 and 8 from TR2 (Fig. 1) were sampled. The sampling coordinates were obtained using GPS Garmin Plus III (Model 6A29) with DGPS antenna (Appendix 1). The superficial sediments (first 5 cm) were collected with the aid of a grab (Boltovskoy 1965).
Benthic faunal analysis In the laboratory, 10 cm3 of sediment was washed through a 45-μm mesh sieve to remove the smallest particles (Leipnitz and Aguiar 2002; Leipnitz et al. 2005). The dried samples were then treated with carbon tetrachloride (CCl4) for separating the benthic fauna. The supernatant materials were removed with the aid of a brush and placed in a Petri dish to be analyzed under the stereomicroscope, where the benthic foraminifera and testate amoebae were sorted, counted and taxonomically classified. For taxonomic identification at the genus level, we used the classification proposed by Loeblich and Tappan (1964, 1987) and Medioli and Scott (1988). For the identification of species, we used the classifications of Decloitre (1976, 1978, 1979, 1981, 1982), Deflandre (1928, 1929), Gauthier-Lièvre and Thomas (1958, 1960), Medioli and Scott (1983), Ogden and Hedley (1980), Ogden and Ellison (1988), Patterson and Kumar (2002), Thomas and Gauthier-Lièvre (1959), and Vucetich (1972, 1973). All of the materials are housed in the collection at the Museum of Paleontology at the University of Valley Rio dos Sinos, São Leopoldo (RS). Some specimens were separated and used for SEM (Scanning Electron Microscope) pictures at the Center for Electron Microscopy (CME) in the Federal University of Rio Grande do Sul (UFRGS). For each sample, the relative abundances of recognized taxa, the species richness, the Shannon diversity and the density of both the foraminifera and testate amoebae were calculated.
Abiotic parameters of the Itapeva and Quadros lakes The physico-chemical parameters (depth, temperature, pH and dissolved oxygen [DO]) of the bottom waters were measured at the time of sampling for IL and QL by means of a conductivity-temperature-depth (CTD) probe. The second aliquots of the sediment samples were used for grain-size and organic matter analyses. For the grain size determination the methodology proposed by Pettijohn (1975) was followed. Sediment grain-size was determined by mechanical sieving, and Shepard’s (1954) triangular diagram was adopted for the sediment classification. Organic matter (OM) content was analyzed by sediment calcination in a muffle furnace (450 °C) for 4 h (Suguio 1973).
Mar Biodiv Fig. 1 Study area. Localization of the 115 studied samples within the nine coastal lakes and lagoons of the Tramandaí Basin (Rio Grande do Sul region, Brazil)
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Descriptive statistics and geostatistics All of the calculations were carried out with R (v2.13, http:// www.r-project.org/). A principal component analysis (PCA) was first conducted on the relative abundance of all of the recognized species (foraminifera and testate amoebae) and then only on testate amoeba relative abundances. The PCA was calculated using the ade4 package. The first two principal components were then extracted and plotted. On the first plane, the samples were grouped with respect to their geographical location and the major species for the axes construction were extracted. A hierarchical cluster analysis (HCA) was performed with respect to the testate amoeba relative abundances. The HCA was calculated using the stats package. Euclidean distance correlation coefficients were used to measure similarities and the Ward’s linkage method was used to arrange pairs and groups into hierarchic dendrograms. To assess the uncertainty in the HCA, p values were calculated with approximately unbiased (AU) tests after multiscale bootstrap resampling. The p value of a cluster is a value between 0 and 1, which indicates how strongly the cluster is supported by data. Clusters with p values greater than 95 % are strongly supported by data. Clusters and p values are given for both samples and species. The correlations were tested between the major species for the PCA axis construction and the abiotic parameters of the Itapeva and Quadros lakes. Two sample t tests were conducted using the package base from the R-suite. Relationships with a p value 0.75. The relationships between the same key species and the abiotic parameters within IL and QL were also plotted with a bagplot (Rousseeuw et al. 1999). The bagplot represents in two dimensions several characteristics of bivariate data. The bagplot is a bivariate extension of the box and whisker plot. The general location of the data is indicated by the depth median, its spread is demonstrated by the size of the bag, the correlation of the two datasets can be deduced from the orientation of the bag and, generally, the skewness can be observed from the shape of the bag and the loop. The bagplot was calculated with the aplpack package. For the parameters of QL, the spatial distribution of selected abiotic (depth, temperature, pH, OM, sand, silt, clay) and biotic (testate amoeba density, richness, diversity, Shannon index) proportions of the most abundant species in the lake (Pontigulasia compressa, Cucurbitella dentata var. simplex f. crucilobata, Lesquereusia modesta and Difflugia lobostoma f. argentinensis) are described by using geostatistical analysis (Wackernagel 1988). The QL samples were selected because it is the only location with
a reasonable number of stations and a good spatial distribution of the sampling points. The semivariance of the faunal content is defined as half the expected squared difference between the values at places x and x + h. A semivariogram of each family and group was calculated by Eq. 1: h 1 X ½Z ðxi þ hÞ−Z ðxi Þ2 2nh i¼1
n
γ ð hÞ ¼
ð1Þ
where γ(h) is the semivariance at the lag distance h, n(h) is the number of observation pairs separated by h, and Z(xi) and Z(xi +h) give the paired values of the variable Z at two locations separated by h. Numerous models can be used to fit the semivariogram. In the present study, these are exponential, spherical and Gaussian, and linear (Eqs. 2–5), and sometimes mixed with a nugget model (Eq. 6). The nugget represents variability at distances smaller than the fixed sample spacing, including measurement error. In the following equation, a is the range. γ ð hÞ ¼ C 1
−jhj expð a Þ
3j hj γ ð hÞ ¼ C 2a
jhj3 2a3
ð2Þ
! if h ≤ a and γ ðhÞ ¼ C if h > a ð3Þ
γ ð hÞ ¼ C 1
exp−ð a Þ
h 2
γ ð hÞ ¼ C h γ ð hÞ ¼
0 if h ¼ 0 C if h > 0
ð4Þ
ð5Þ
ð6Þ
In the analysis, the sill value is the upper limit of the fitted semivariogram model. As a consequence, the ratio of nugget to sill indicates the spatial dependency of the foraminiferal distribution (Webster and Oliver (2001). Ratios are low (75 %). A low ratio means that a large part of the variance is introduced spatially, implying the strong spatial dependence of the variable (abiotic parameters or fauna). A high ratio often indicates weak spatial dependency in the sampling resolution. The range of the semivariogram represents the average distance over which the variable semivariance reaches its peak value. A small effective range implies a distribution pattern composed of small patches. The geostatistical analysis was carried out using the geoR package.
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Results Foraminiferal and testate amoeba assemblages Benthic foraminifera were mainly observed in front of the outlet (Fig. 2a). In particular, they were found in all of the stations in TL, AL, CL and GL and in some of the stations along TR2. No foraminifera were encountered in IL, QL, TR1, PL and MNL (Fig. 2a). The testate amoebae were, however, more widely distributed, albeit in variable abundances, and were completely absent close to the Tramandaí Basin’s outlet (Fig. 2a). Testate amoebae were observed in 85 samples and benthic foraminifera in 49. In 23 of these samples, foraminifera and testate amoebae were observed together. Accordingly, for the remaining 26 samples located in TR2, TL, AL and CL, foraminifera were the only component. The foraminiferal and testate amoeba densities (live plus dead specimens) were also highly variable. The density of the former ranged between 0 and 2,328 specimens per 10 cm3, while that of the latter varied from 0 to 15,568 specimens per 10 cm3. The highest foraminiferal density was observed in GL, CL and TR2 (Fig. 2b). The highest testate amoeba densities were observed in QL, although quite high values were also encountered in IL, PL, TR1 and TR2. Benthic foraminiferal species richness and Shannon-Weaver diversity ranged from 0 to 7 and from 0 to 1.77, respectively. A total of 14 species were recognized within the foraminiferal assemblages (Appendix 1). Those identified were: Ammonia beccarii, Ammoscalaria pseudospiralis, Ammotium salsum, Arenoparrella mexicana, Elphidium excavatum, Elphidium gunteri, Haplophragmoides wilberti, Miliammina earlandi, Miliammina fusca, Protoschista findens, Quinqueloculina seminula, Trilocularena patensis, Trochamminita salsa, and Trochammina inflata (Plate 1). The dominant benthic foraminiferal taxa, in order of abundance, were: M. fusca (ca. 13.4 %), A. salsum (ca. 8 %), T. salsa (ca. 3.4 %), M. earlandi (ca. 2.9 %), H. wilberti (ca. 2.6 %), P. findens (ca. 1.7 %) and T. patensis (ca. 1.3 %) (Fig. 3a and Appendix 2). A total of 101 testate amoeba taxa were recognized within these transitional environments. The species richness and Shannon diversities were also quite variable ranging from 0 to 38, and from 0 to 3.2, respectively. The recognized genera were: Arcella (two species), Centropyxis (13 species), Bullinularia (one species), Hoogenraadia (two species), Cyclopyxis (four species), Heleopera (three species), Lesquereusia (six species), Cucurbitela (eight species), Difflugia (53 species), Lagenodifflugia (three species), Pontigulasia (four species), Suiadifflugia (one species) and Phryganella (one species) (Plate 1 and Appendix 1). The two dominant testate amoeba families were Difflugidae and Hyalospheniidae, which were represented by 74 and 9 species, respectively (Appendix 1). The most abundant species, in order of abundance, were:
Pontigulasia compressa (ca. 8.7 %), Cucurbitella dentata var. simplex f. trilobata (ca. 7.8 %), Difflugia oblonga f. tenuis (ca. 4.1 %), Lesquereusia modesta (ca. 3.8 %). Accessory species include Difflugia oblonga (ca. 2.7 %), Centropyxis platystoma (ca. 2.6 %), Centropyxis aculeata (ca. 2.4 %), Difflugia lobostoma f. argentinensis (ca. 2.3 %), Difflugia oblonga var. compressa (ca. 2.1 %), and Lagenodifflugia vas (ca. 2.1 %) (Fig. 3b and Appendix 2). Statistical analysis First, a PCA analysis was carried out on all of the fauna (foraminifera and testate amoebae), with the first two axes among the 115 taxa representing 11.1 % of the total inertia. These two axes were constructed by the opposition of foraminiferal and testate amoeba species (Fig. 4a). Miliammina fusca had a strong relationship with axis 1 and A. salsum with axis 2 (Fig. 4a). Other benthic foraminiferal and testate amoeba species were only weakly related to these two axes. On the other hand, the sample stations were grouped by geographical origin, namely transitional environments (Fig. 4b). The samples belonging to TL, AL and CL had a transversal pattern on the PCA plane, whereas TR2 exhibited clear opposition between A. salsum and several testate amoeba taxa. Meanwhile, GL revealed strong opposition between M. fusca and some testate amoeba taxa. A second PCA was carried out on the relative abundances of the testate amoeba taxa (Fig. 5). The PCA’s first plane revealed the opposition between P. compressa, D. oblonga f. tenuis and the group D. oblonga–Centropyxis discoides (Fig. 5a). This first plane represented 11.6 % of the inertia. The stations grouped by geographical origin were principally based on the influence of D. oblonga f. tenuis (TL, TR2 and CL, which were those closest to the opening to the sea) and P. compressa (IL, QL, MNL and GL, which were those that were distant from the sea openings) (Fig. 5b). More specifically, C. discoides and D. oblonga seemed to occur more in MNL and GL. The geographical position of these species demonstrated the clear signatures of the different lakes (Fig. 5). TL, QL and TR1 had a faunal assemblage dominated by testate amoebae and, more precisely, P. compressa, whereas the southern lakes (GL and MNL) were dominated by D. oblonga and C. discoides (Fig. 5b). In the lakes where benthic foraminifera occur, most of the assemblages were generally dominated either by A. salsum or M. fusca (Fig. 4). In order to underline species affinities as well as highlight groups of samples with similar assemblages (i.e., similar ecology), the testate amoeba taxa were then grouped by means of an HCA. To test the significance of the relationships, both of the HCAs were validated by a p value calculation that demonstrated a good association (p value >95 %) (Fig. 6).
Mar Biodiv Fig. 2 a Proportion of foraminifera vs testate amoebae in the study area; b density of benthic foraminifera (when present) and testate amoebae. The size of the pie is proportional to the density of the benthic foraminifera and testate amoebae/ 10 cm3 of sediment. For the testate amoebae, the relative abundances of selected families are given within the pie
Few of the significantly grouped samples were close to each other. Many of the samples from IL and QL were grouped together (Fig. 6a). Sixteen groups of taxa had good probabilities (p>0.95) and these species were expected to have the same ecological requirements (Fig. 6b).
Influence of abiotic parameters The selected physico-chemical parameters of the bottom water and the grain-size of the sediment values were only measured in the QL and IL (Appendix 3). Correlations among benthic
Mar Biodiv Plate 1 Principal testate amoebae and benthic foraminifera: 1 Pontigulasia compressa; 2 Difflugia oblonga f. tenuis; 3 Cucurbitella dentata var. simplex f. trilobata; 4, 8 Centropyxis platystoma; 5 Lesquereusia modesta; 6 Lesquereusia gibbosa; 7 Difflugia oblonga; 9 Ammotium salsum; 10 Miliammina fusca; 11 Trilocularena patensis; 12, 16 Trochamminita salsa; 13, 14 Elphidium gunteri; 15 Ammonia tepida
foraminiferal and testate amoeba densities, species richness, diversity and abiotic parameters (water: depth, temperature and pH; sediment: organic matter proportions, sediment size) were calculated with significant p values (
