Recent benthic foraminifera from the Itaipu Lagoon , Rio de Janeiro ( southeastern Brazil )

Itaipu Lagoon is located near the mouth of Guanabara Bay and has great importance for recreation to the city of Niterói, Rio de Janeiro state, Brazil. Several studies have documented foraminiferan diversity at Guanabara Bay, but none in Itaipu Lagoon. Therefore, this study lists and provides images of foraminiferal species collected from Itaipu Lagoon. A total of 35 species belonging to 23 genera were collected, grouped in 17 families and four orders. Ammonia tepida was the species with the highest occurrence. This study represents a baseline work for future investigations.


INTRODUCTION
The infrakingdom Rhizaria is one of the six supergroups of eukaryotes based on molecular and phylogenetic data (Cavalier-Smith 2002;Sierra et al. 2013) and comprehend numerous flagellate and amoeboid protists such as the phylum foraminifera.Historically, paleontologists invest on the study of foraminifera, specifically related to petroleum exploration (Frontalini et al. 2015).Since the 1960s, benthic foraminifera have been successfully used to define the quality of marine environments (Alve 1995;Yanko et al. 1999;Eichler et al. 2001;Frontalini and Coccioni 2011;Schönfeld et al. 2012).Recent studies have focused on living foraminifera, particularly for biodiversity, biological, ecological and biomonitoring studies (Murray 2006).
There are many advantages of applying foraminifera to environmental monitoring when compared with macrofaunal organisms (e.g., Alve 1995;Mojtahid et al. 2006;Bouchet et al. 2007;Alve et al. 2009;Jorissen et al. 2009).In fact, the high density and diversity in marine sediments, specific ecological requirements, short life and reproductive cycles make benthic foraminifera an early-warning of environmental changes.Furthermore, tests of foraminifera have a tendency to be preserved in sediments and provide useful paleoenvironmental information, such as paleoclimatological and paleoecological reconstructions (Murray 2006;Schönfeld et al. 2012).
Rio de Janeiro state has a set of coastal environments where studies on the recent foraminifera have been made in impacted areas (Eichler et al. 2001;Eichler et al. 2003Eichler et al. , 2014)).Lagoon ecosystems represent ecotones or transitional units where landscapes, sea and waterscapes meet and support a large biodiversity (Gönenç 2005).Coastal lagoons are therefore one of the most ecologically valuable components of coastal areas (Vadineanu 2005).
Itaipu Lagoon is a brackish water body that belongs to the Itaipu-Piratininga Lagoon System, which has great importance to recreation and tourism in Rio de Janeiro state.These lagoons, as well as other coastal systems in Brazil, are affected by human pressure and increasing changes in its morphometry, physical-chemical, biological and granulometric characteristics (Eichler et al. 2001;Rodrigues et al. 2003;Eichler et al. 2003Eichler et al. , 2014;;Díaz et al. 2014).

Sample collection and treatment
Bottom sediment samples were collected in January 2013 at 13 stations (Table 1) that represent the different environmental settings of the lagoon (Figure 1).Using a shallow-draft boat and an Ekman Grab sampler, triplicate samples of 50 ml of the surface sediment (1 cm of surface) were collected.Immediately after collection, an alcohol solution 70% with Rose Bengal stain (2 g of Rose Bengal in 1,000 ml alcohol) was added to the sediment samples to identify living organism at the time of collection according to the methodology proposed by Schönfeld et al. (2012).Rose Bengal adsorbs onto proteins and stains the cytoplasm a pinkish or reddish color.Samples were washed on a 63-μm screen and In order to serve as a background to future ecological and paleoecological studies, as well as contribute to research on the biodiversity and distribution of foraminifera throughout Rio de Janeiro lagoons, the aim of this study is to characterize the living benthic foraminiferal assemblages on surface sediments from Itaipu Lagoon.

Study site
Itaipu Lagoon is located between latitudes 22°57ʹ S to 22°58ʹ S and longitudes 043°01ʹ W to 043°03ʹ W in Niterói, Rio de Janeiro state, southeast Brazil (Figure 1).The lagoon covers an area of 1.2 km 2 and has a water depth between 0.2 and 2.0 m.The climate in the city of Niterói, as well as throughout Rio de Janeiro state, is warm and humid with a rainy season in summer (December to March), dry season in winter (June to September) and an average rainfall between 1,000 and 1,500 mm/year (Barbiére and Coe-Neto 1999).Itaipu Lagoon is connected to the Atlantic by the Tibau Channel which is an artificial channel that provides an open tidal inlet (Salvador et al. 2002).The lagoon is affected by a microtide effect that has an average height of 0.71 m and the width can increase up to 10 m during the tide of syzygy.Waves coming from the south and southeast reach the Itaipú Embayment after being diffracted by Itaipú Point and the nearby islands (Salvador et al. 2002).The present study analyzes only the living benthic foraminifera.Using a stereoscope microscope, as close as possible to 100 living individuals per sample were counted.However, in some samples few specimens of foraminifera were found.All stained foraminifera were removed from each sample.The values of absolute abundance were determined by the average of the number of specimens found in the triplicates (Table 2).Species recognition and the systematic classification are according to Boltovskoy et al. 1980, Loeblich and Tappan 1987, Martins and Gomes 2004, Poag 1981, Walton and Sloan 1990and Yassini and Jones 1995.Finally, the name of the each species was checked and revised in accordance to the on-line database WoRMS (World Register of Marine Species; Hayward et al. 2016).All the specimens were stored in micropaleontological slides, recorded with a voucher number, and properly archived (Schönfeld et al. 2012).Images of selected specimens of each species were made using a scanning electron microscopy (EVO MA10, Zeiss).

RESULTS
A total of 35 benthic foraminiferan species belonging to 23 genera was identified (Table 2).The species belong to 17 families and four orders (Figures 2-4).The most abundant family was Rotaliidae, followed by Bolivinitidae and Elphidiidae in diminishing order of individuals.The order Rotaliida was predominant in the lagoon, with the greatest numbers of individuals and species, especially at stations IT03, IT05 and IT09 (Table 2).Samples from stations IT10 and IT12 did not contain any living foraminifera.The most abundant
Description: test elongate, laterally compressed, with rounded periphery.Wall translucent, smooth (not ornate) and bright, perforated in the bottom chamber.Aperture is narrow and surrounded by a lip, higher in one the sides.

Family Rotaliidae
Ammonia parkinsoniana (d'   Description: test elongate-ovate, triserial.Aperture is a wide slit extending up from the base of the last chamber to the middle of the apertural face.Wall calcareous, surfasse smooth, but numerous spines occur at the lower margins of the chambers.

Bulimina patagonica d'Orbigny, 1839
Original citation: Bulimina patagonica d 'Orbigny, 1839: 50.Description: test oblong, conical, very polished on the last whorls, rough, covered with small spines on the remainder, these projecting all the more as they are at the base and completely conceal the spire, composed of 5 rounded whorls, separated by somewhat depressed sutures.Chambers broader than high, 3 to a whorl, all somewhat inflated and distinct, the last inflated and larger than the rest.Aperture virguline, placed almost in the center of width of the chamber.Color white.Length 0.66 mm.
Description: Test circular in outline, somewhat compressed, peripheral margin rounded and slightly lobate; chambers inflated, 7-10 in final whorl; wall smooth, transparent or opaque, radial; sutures gently curved, depressed, often covered with pustules; fossettes of variable size and shape; umbilici concave, covered with pustules; aperture formed by series of holes at base of smooth apertural face.Description: test relatively small, laterally compressed, planispiral involute, umbilical regions slightly depressed, with rapidly enlarging chambers in the last whorl and rounded periphery.Suture very depressed and marked by short and narrow septal bridges.Wall calcareous, finely perforated.Apertural consists on series of basal pores.

Genus Elphidium de Montfort, 1808
Elphidium discoidale (d'Orbigny, 1839) Original citation: Polystomella discoidale d 'Orbigny, 1839. Sen Gupta et al. 2009: 87-129.Description: test planispiral, involute, strongly biconvex, with rounded periphery and up to 25 chambers in the last whorl, sutures are slightly depressed.Aperture is formed of a series of small openings at the base of the apertural face of the last chamber, apertural face low and triangular.Wall calcareous, perforated, umbilical knob protruding with several large pores.Cole, 1931 Original citation: Elphidium gunteri Cole, 1931. Gross 2001: 60−75.Description: test subcircular to ovate in outline, expanded in umbilical area, peripheral margin broadly rounded.Chambers slightly inflated, 10-13 in final whorl.Wall radial, translucent to opaque, with large pores.Sutures radial, umbilici with one or several knobs.Aperture composed of various holes on and at base of apertural face.

Subclass Textulariia Order Lituolida Family Haplophragmoididae Maync, 1952
Genus Trochamminita Cushman & Brönnimann, 1948 Trochamminita salsa (Cushman & Brönnimann, 1948) Original citation: Labrospira salsa Cushman and Bronnimann, 1948: 16.Description: Test planispiral, semi-involute or involute, with a lobate equatorial periphery.Axial periphery rounded.Wall sand grains set in fine cement; surface smooth, may be somewhat polished.Coarseness of wall varies considerably in specimens from different localities.Color fawn to light brown.Chambers: Slightly inflated; seven to eight in the last whorl, increasing fairly rapidly in size.Earlier chambers may be partially visible.Sutures: Slightly curved, depressed.Aperture: In the adult stage may be represented by a single areal slit near the base of the terminal face of the chamber, or multiple pores of rounded, though somewhat irregular, shape.If the aperture is multiple, the pores are usually in a linear series where the single areal aperture would otherwise be situated, though some specimens show multiple apertures distributed widely across the terminal face.If a single aperture is present, it may show one or more constrictions, suggesting a tendency toward the formation of a number of separate openings.All apertural openings are completely surrounded by prominent lips.
Genus Warrenita Loeblich & Tappan, 1984 Warrenita palustris (Warren, 1957) Original citation: Sulcophax palustris Warren, 1957. Sen Gupta et al. 2009: 87-129.Description: test free, elongate, arcuate, with numerous gradually enlarging and laterally slightly compressed chambers that are strongly overlapping, covering about one-half the lenght of the preceding chamber.Wall very thin and delicate, finely agglutinated, smoothly finished.Aperture a terminal arcuate slit, extending about one-third the breadth of the test.

Genus Textularia Defrance, 1824
Textularia earlandi Parker, 1952 Original citation: Textularia earlandi Parker, 1952. Gross 2001: 60−75.Description: test elongate, very small, four time longer than wide, sometime curved, peripheral margin rounded, lobate, chambers inflated, rounded with a initial coiled portion composed of 4−6 chambers, and a very long biserial stage.Wall agglutinated, thin composed of coarse and grains.Aperture is an arched opening on the inner margin of the final chamber.

DISCUSSION
Studies on the biodiversity of foraminifera were conducted in neighboring ecosystems of Itaipu Lagoon, such as Guanabara Bay (Eichler et al. 2001;Eichler et al. 2003Eichler et al. , 2014;;Vilela et al. 2004Vilela et al. , 2014;;Santos et al. 2007;Donnici et al. 2012;Clemente et al. 2015), Maricá Lagoon (Bomfim et al. 2010) and Rodrigo de Freitas Lagoon (Vilela et al. 2011).Eichler et al. (2001) Santos et al. (2007) from the Guanabara Bay and grouped into three assemblages.Assemblage I, in the northeast part of the bay showed the dominance of A. tepida that was explained by the resistance of this species to heavy metal pollution.Assemblage II, in the northwest, was represented by Textularia earlandi Parker 1952 and B. elegantissima and was associated with low salinity and areas contaminated with organic matter (domestic sewage).Assemblage III, in the central part and at the bay mouth, was represented by Cribroelphidium poeyanum (d'Orbigny 1826) and Quinqueloculina seminula (Linnaeus 1758), which were also related to polluted and stressed environments.Donnici et al. (2012) identified 68 species within the combined assemblages of Guanabara Bay and found that A. tepida and B. elegantissima dominated, which showed a positive correlation to heavy metals.The study also found an area with dominance of Q. seminula associated with species of genus Elphidium, indicative of a lagoon environment with a good exchange with sea water.In a paleocological survey by Vilela et al. (2014) on nine Holocene cores, 41 species of foraminifera were identified along different areas of Guanabara Bay.Vilela found dominance of agglutinated species (Ammotium salsum (Cushman & Brönnimann 1948), Haplophragmoides wilberti Andersen 1953, T. earlandi andTrochammina inflata (Montagu 1808)), indicating a proximity to mangrove ecosystem in the Guapimirim Environmental Protected Area and along the São Gonçalo coast on the northeast shore.
Some species identified in the present study commonly occur in lagoons, such as those belonging to the genus Ammonia, Buliminella, Elphidium and Fursenkoina pontoni (Cushman 1932) (Vilela et al. 2011).However, marine species such as Bulimina marginata d'Orbigny 1826, Nonionella atlantica Cushman 1936, Nonionella auris (d'Orbigny 1839) and Nonionella opima Cushman 1947 were also found in Itaipu Lagoon, mainly at station IT03 that is very close to the channel that connects the lagoon to the ocean.A previous study in Rodrigo de Freitas Lagoon found 52 species of foraminifera: 11 were also common in Itaipu Lagoon and three are typical of marine environments (B.marginata, N. atlantica and N. opima) (Vilela et al. 2011).The occurrence of these typically marine species in Itaipu Lagoon suggests transportation by tidal currents from the adjacent shallow continental shelf.A. tepida appears as the dominant species in Itaipu and Rodrigo de Freitas (Vilela et al. 2011) lagoons.This species is commonly found in environments that are polluted and under both natural and anthropogenic stresses (Vilela et al. 2004;Yanko et al. 1994Yanko et al. , 1999;;Alve 1995;Culver and Buzas 1995;Sousa et al. 1997;Debenay et al. 2000;Van der Zwann 2000;Rodrigues et al. 2003).Bomfim et al. (2010) recognized 22 species with a dominance of Miliammina fusca (Brady 1870) in Maricá Lagoon.The highest number of agglutinated species and a reduction in the number of tests were associated with hyposaline conditions and the absence of marine species was explained by a lack of tidal transport from the ocean.In Itaipu Lagoon, the high number of species at stations IT03, IT05 and IT09 may also be interpreted by their geographic positions with regards to the accumulation of species brought into the lagoon by tidal currents; IT03 and IT05 are the stations closest to the channel that connects the lagoon to ocean and IT09 is located where the influence of currents ends.
Itaipu Lagoon has high species richness and is greatly influenced by the sea, despite having a small area.The data in this study will provide a valuable baseline for future investigations, including paleoclimatological and paleocological reconstructions, into the foraminifera of this and other lagoons of Rio de Janeiro state.
Raposo et al. | Foraminifera from the Itaipu Lagoon with large chambers, almost lineal.Wall very agglutinated.Aperture simple, spherical on the last chamber.

Table 1 .
Geographic coordinates of sampled station in the Itaipu lagoon.Raposo et al. | Foraminifera from the Itaipu Lagoon dried in a kiln at 50°C for 48 hours to remove silty and clayey fractions of the sediment.The foraminifera were removed from the remaining sediment by flotation density difference in trichloroethylene.
Figure 1.Location of the study area with sampling stations collected in Itaipu Lagoon, Rio de Janeiro.

Table 2 .
Foraminiferal species identified on the Itaipu Lagoon.
Raposo et al. | Foraminifera from the Itaipu Lagoon Raposo et al. | Foraminifera from the Itaipu LagoonAperture is a triangular opening sited deep in the depression of the apertural face of the terminal chamber, tooth plate is very much reduced.Wall calcareous hyaline.
test, large, in quinqueloculine mode, with sharp periphery.Aperture is a large opening with bifid tooth.Wall calcareous, imperforate and porcelaneous, surface smooth. Description: Raposo et al. | Foraminifera from the Itaipu Lagoon Eichler et al. (2003) in Guanabara Bay, with the genera Ammonia, Bolivina, Bulimina, Buliminella, Cassidulina, Elphidium and Quinqueloculina dominant.Also in Guanabara Bay,Eichler et al. (2003)found Buliminella elegantissima (d'Orbigny 1839), B. striatula and Bulimina elongata d'Orbigny 1826 dominant in areas with poor water exchange (therefore low salinity and dissolved oxygen) with the open ocean.Vilela et al. (2004) identified 36 species from the combined living and dead assemblages in Niterói Harbor and noted the predominance of B. elegantissima, A. tepida and Bolivina lowmani Phleger & Parker 1951 in this impacted habitat.Twenty-two species were identified by