Occurrence of Arcellidae (Amorphea, Arcellinida) in a coastal stream in the State of Rio de Janeiro

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Testate amoebae are considered a polyphyletic group of eukaryotic unicellular organisms, they are surrounded by a carapace (shell) formed by organic secretion and aggregated particles of silica or limestone (Alves, Lansac-Tôha, Velho, Joko, & Costa, 2007; Lansac-Tôha, Velho, Costa, Simões, & Alves, 2014). They are heterotrophic organisms, feeding on many different food resources (e.g. algae, bacteria), and classified as carnivorous, omnivorous, osmotrophic or mixotrophic (Arrieira, Schwind, Alves, & Lansac-Tôha, 2017; Rosa, Orikassa, Lopes, & Silva, 2017).

These protists inhabit different biotopes such as riparian vegetation, periphyton, sediment and plankton in continental waters (Alves, Velho, Costa, & Lansac-Tôha, 2012; Miranda & Mazzoni, 2015). Most studies on testate amoebae focuses on lentic systems (standing water or little movement environments) (Fulone, Vieira, Velho, & Lima, 2008; Tôha et al., 2014). Some authors such as Crispim and Watanabe (2000) and Wetzel (2001) suggest that the advective or continuous turbulence downstream of an aquatic ecosystem, considered as the primary factor, negatively affects the development of these groups in this type of environment (Neves, Serafim-Júnior, Ghidini, & Brito, 2007). Considering lotic environments, particularly low order, such as streams, few studies include these organisms, although they are frequent and sometimes dominant in these environments (Fulone, Lima, Alves, Velho, & Lansac-Tôha, 2005; Fulone et al., 2008; Miranda & Mazzoni, 2015).

Arcellidae is one of the most common testate amoebae families in neotropical aquatic ecosystems, ubiquitous in many types of environments across the world (Vucetich, 1978; Miranda & Mazzoni, 2015; Silva, Rangel, Lansac-Tôha, Schwind, & Joko, 2016). Species of this family build their shells with endogenous material and present discoid or hemispherical shape and centered pseudostoma (Souza, 2008). Within this family, Arcella is the most taxa-rich genus (Meisterfeld, 2002).

Knowledge about species richness and composition of an environment represents the most important attributes when studying a biological system (Ricklefs & Schluter, 1993). It is known that there are numerous studies aimed at describing the composition and focused on the taxonomy of many groups of organisms (Frota, Ota, Deprá, Ganassin, & Graça, 2020; Pacifico, Almeda, Carmo, & Fidanza, 2019). However, protists especially planktonics, are under-explored groups today (Lansac-Tôha, Bonecker, Velho & Lima, 2004). There are indications that in Brazil, in particular, there are many regions in which knowledge about testate amoebae is in its initial stages (Schwind, Dias, Joko, Bonecker, & Lansac-Tôha, 2013).

Thus, given the importance of testate amoebae in continental aquatic environments and the scarcity of research related to these protists in low order lotic environments, especially in the State of Rio de Janeiro (Miranda & Mazzoni, 2015), the present study aimed to describe and illustrate the testate amoebae taxa of Arcellidae from a coastal stream. In addition, we aim to contribute to the knowledge about the occurrence and geographic distribution of these organisms in this State and in the Southeast region of Brazil.

During the study period, the sampled points showed significant variation in the environmental variables related to productivity. The coefficient of variation showed that the ammonia concentration presented the largest variation, followed by chlorophyll-a (Table 2).

Table 2.
Mean values and coefficient of variation (CV%) of the environmental variables in the preserved and dammed system during the study period. (DO= Dissolved oxygen; pH=pH; Turb=Turbidity; Chlor= Chlorophyll-a; Phos= Phosphate; Ammo= Ammonia).

Eight Arcellidae species were recorded in the Ubatiba Stream (Figure 1). In each species, the description and information about the presence in biotopes and sampling points along the river were provided.

AMORPHEA Domain Adl et al., 2019

AmoebozoaLühe 1913, sensu Cavalier-Smith 1998

•Tubilinea Smirnov et al., 2005

••Elardia Kang et al., 2017

•••Arcellinida Kent 1880

••••Sphaerothecina Kosakyan 2016

•••••Arcellidae Ehrenberg1843

Arcella artocrea (Leidy, 1876) (Figure 2: 1,1a)

Leidy (1876): p. 57; Deflandre (1963): p. 239, fig. 9.25.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 18.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. The shell is circular, conical and often covered by depressions. Presents irregular border. Surface mammillated or pitted. Pseudostoma brown, circular, invaginated and circulated by about thirty large and small pores; Measurements: DS = 150-162μm; SH = 9-12μm; PD = 55-57μm.

Ubatiba Stream: This species was recorded in all sampling points (P1 to P5), in the plankton and riparian vegetation. However, Arcella artocrea was observed only in the rainy season (C4, C5 and C6).

Ecological distribution in the Southeast region of Brazil. This species has been observed in riparian vegetation of a stream (Miranda & Mazzoni, 2015).

Arcella conica (Playfair, 1917) (Figure 2: 2, 2b)

Playfair (1917): p. 640, figs. 16-17; Deflandre (1928): p. 238-240, figs. 244-255; Velho, Tôha, and Serafim-Junior (1996): p. 40, pl. I, fig. 8; Lansac-Tôha, Alves, Velho, Robertson and Joko (2008): p. 179-181, pl. I, fig.2; Souza (2008): p. 72, figs. a-b; Silva et al. (2016): p. 231-235, fig. 4.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 19.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. In lateral view, the shell is composed of facets forming a pyramid. In apical view, the shell is approximately circular with a polygon of eight or nine concave sides and rounded edges. The pseudostoma is circular with or without a buccal tube. Shell color is yellow to brown; Measurements: DS = 64-67 μm; SH = 34-36 μm; PD = 37-39 μm.

Ubatiba Stream: Arcella conica was observed in preserved and impacted points (P1, P3, P4 and P5), associated with riparian vegetation and plankton. It was present in the dry and rainy seasons (C1, C2, C3, C5 and C6).

Ecological distribution in the Southeast region of Brazil. This species has been observed in association with riparian vegetation of streams and in lakes (Barbosa et al., 2014; Miranda & Mazzoni, 2015; Lopes et al., 2017).

Arcella costata Ehrenberg, 1847 (Figure 2; 3, 3a)

Deflandre (1928): p. 240-241, figs. 257-258; fig. 45; Souza (2008): p. 73, figs. a-c; Tôha et al. (2008): p. 181, pl.I, fig. 3; Silva et al. (2016): p. 231-235, fig. 5.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 23.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. The shell is formed by an incomplete pyramid of five to seven facets. The apical profile of the shell is approximately circular and presents a star with five to seven points formed by the pyramid facets. The oral face is wider than the apical face. The pseudostoma is circular with a buccal tube. The color of the shell is yellow to brown. Measurements: DS = 88-90μm; SH = 37-41μm; PD = 24-27μm.

Ubatiba Stream: Arcella costata was recorded in impacted points with lentic characteristics (P4 and P5). It was present in the riparian vegetation and in the plankton. Although observed in the dry season, this species was more common in the rainy season. (C3, C4 and C5).

Ecological distribution in the Southeast region of Brazil. This species has been recorded in samples of plankton, sediments and riparian vegetation of distinct aquatic environments (Ferraz, Landa & Paprocki, 2009; Miranda & Mazzoni, 2015; Lopes et al., 2017; Misailidis, et al., 2017).

Arcella discoides Ehrenberg, 1843 (Figure 2; 4, 4a)

Penard (1902): p. 403, figs. 1-2; Deflandre (1928): p. 256-257, figs. 324-326; Velho et al. (1996): p. 43, pl. II, fig. 14; Lahr and Lopes (2009): p.133-134; Silva et al. (2016): p. 232, fig. 9.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 24.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. Shell generally circular in apical view, plane-convex in lateral view, sometimes arched; diameter about three to four times the height; without a distinct rim or border. Two nuclei or more. Pseudostoma circular, invaginated, bordered by a shallow lip, usually surrounded by a ring of numerous small pores. Shell yellow or brown. Measurements: DS = 85-88μm; SH = 11-13μm; PD = 37-40μm.

Ubatiba Stream: Arcella discoides has been recorded in preserved and impacted points (P2, P3, P4 and P5). It was present in the riparian vegetation and in the plankton and only in the dry season (C1, C2 and C3).

Ecological distribution in the Southeast region of Brazil. Arcella discoides has been identified in different biotopes as mosses, sediments, plankton and aquatic macrophytes of lotic and lentic systems (Fulone et al., 2005; Laut, Silva, Figueiredo Jr., & Laut, 2011; Barbosa et al., 2014, Miranda & Mazzoni, 2015; Silva, Oliveira, & Wisniewski, 2017; Lopes et al., 2017).

Arcella gibbosa Penard, 1890 (Figure 2: 5, 5a)

Deflandre (1928): p. 227-229, figs. 190-206; Deflandre (1953): fig. 89-F; Velho et al. (1996): p. 39, pl. I, fig. 5; Souza (2008): p. 77, figs. a-b.; Lahr and Lopes (2009): p. 128, 129, 137, figs 1-f; Silva et al. (2016): p. 232, fig. 15.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 25.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. Shell colorless, yellow, orange or brown, circular in dorsal view and hemispherical in lateral view, with an enlargement at the basis (the keel or basal border). Surface is smooth, but the aboral surface has a series of regular depressions. Invaginated pseudostoma, circular and with a distinct rim or lip; Measurements: DS = 118-121μm; SH = 35-37μm; PD = 39-42μm.

Ubatiba Stream: Arcella gibbosa was recorded in all sampling points (P1 to P5), in the plankton and riparian vegetation, in the rainy and dry seasons (C1, C2, C3, C4, C5 and C6).

Ecological distribution in the Southeast region of Brazil. Records of this species were obtained from plankton samples, aquatic macrophytes and sediments (Barbosa et al., 2014, Miranda & Mazzoni, 2015; Lopes et al., 2017; Misailidis et al., 2017).

Arcella hemisphaerica undulata Deflandre, 1928 (Figure 2: 6,6a)

Deflandre (1928): p. 214, figs. 122-124; Vucetich (1973): p. 290, pl. I, fig. 3; Lahr and Lopes (2009): p. 130; Silva et al. (2016): p. 233, 235, fig. 21.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 30.05.2015. Thirty organisms (C1-C6/P1-P5).

Short description. At lateral view, the dorsal face of the shell is hemispherical, with regular undulations. The pseudostoma is circular and slightly invaginated, with buccal tube. The shell is yellow or brown; Measurements: DS = 50-62μm; SH = 28-31μm; PD = 20-23μm.

Ubatiba Stream: Arcella hemisphaerica undulata was recorded exclusively in the riparian vegetation and only in one point with lentic characteristics, P5. This species was observed only in the dry season (C1).

Ecological distribution in the Southeast region of Brazil. In Southeast region, this species has been recorded in planktonic, sediment and aquatic macrophytes samples from lotic systems (Lahr & Lopes, 2009; Miranda & Mazzoni, 2015; Silva-Neto et al., 2015).

Arcella megastoma Penard, 1902 (Figure 2: 7, 7a)

Penard (1902): p. 409; Wailes (1913): p. 204-205, pl. XV, figs. 1-2; Deflandre (1928): p. 267-268, figs. 363-372; Lansac-Tôha et al. (2008): p.182, pl. I, fig. 6; Lahr and Lopes (2009): p. 128; Silva et al. (2016): p. 234, 236, fig. 16.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 04.05.2015. Thirty organisms (C1-C6/P1-P5).

Short description. Apically, the shell outline is discoid. It presents a circular pseudostoma proportionally large and rounded by fine pores. The oral face is little invaginated without buccal tube. The shell is flattened laterally. Shell color is yellow to dark brown; Measurements: DS = 204-206μm; SH = 18-22μm; PD = 175-178μm.

Ubatiba Stream: This species was recorded in all sampling points (P1 to P5), in the plankton and riparian vegetation and in the rainy and dry season (C1, C2, C3, C4 and C5).

Ecological distribution in the Southeast region of Brazil. Records of this species has been obtained from samples of mosses, sediments, plankton and aquatic macrophytes (Fulone et al., 2005; Fulone et al., 2008; Ferraz et al., 2009; Barbosa et al., 2014;Lahr & Lopes 2009; Miranda & Mazzoni, 2015; Misailidis et al., 2017).

Arcella vulgaris Ehrenberg, 1830 (Figure2: 8, 8a)

Penard (1890): p. 151, pl. V, figs. 56-66; Wailes (1913), pl. XV, fig. 5; Deflandre (1928): p. 219-221, figs. 156-164; Velho et al. (1996): p. 37, pl I, fig. 1; Lansac-Tôha et al. 2008: p. 182, pl. I, fig. 7; Silva et al. (2016): p. 234-235, fig. 22.

Material examined. Brazil: Maricá (Rio de Janeiro): Ubatiba Stream (22º 55' 10" S; 42° 49' l04" W). Viviane Bernardes dos Santos Miranda, 18.04.2015. Thirty organisms (C1-C6/P1-P5).

Short description. In lateral view, the shell is rounded with an expansion in the oral part. In apical view, the shell is circular, with folded edge and presents two concentric circles. The inner circle represents the pseudostoma and the outermost circle corresponds to the expansion in the oral part. Circular and invaginated pseudostoma, presenting a buccal tube. Shell color is dark brown, orange or yellow; Measurements: DS = 92-96μm; SH = 59-62μm; PD = 38-36μm.

Ubatiba Stream: This species was observed in all sampling points (P1 to P5). It was recorded in the plankton and riparian vegetation and in the rainy and dry seasons (C1, C2, C3, C4, C5 and C6).

Ecological distribution in the Southeast region of Brazil. This species is very common in different aquatic environments. Present in plankton, sediment, aquatic macrophytes and in internal bromeliads (Barbosa et al., 2014; Miranda & Mazzoni, 2015; Lahr & Lopes 2009; Lopes et al., 2017).

Our results showed that the variables that varied the most throughout the study were those related to productivity, such as ammonia and chlorophyll-a. It is known that the variation in productivity variables is closely related to the nutritional status of aquatic ecosystems and consequently the occurrence of zooplanktonic species therein (Mantovano et al., 2019), such as testate amoebae (Schwind, Arrieira, Simões, Bonecker, & Lansac-Tôha, 2017).

In aquatic environments, the Family Arcellidae is considered one of the most representative families among testate amoebae, being highlighted by several other studies developed in inland aquatic environments (Velho et al., 1996), especially in the upper Paraná River floodplain (Lansac-Tôha et al., 2008).

The results show an important richness of Arcella compared to other studies in the Center-West, Southeast, North, South and Northeast regions of Brazil (Miranda & Mazzoni, 2015; Silva et al., 2016; Rosa et al., 2017), confirming the importance of studies on the record of these protists in the Ubatiba Stream. In addition, this study showed the presence of species found in environments with more studies, for example, in the floodplain of the Upper Paraná River (Velho et al., 1996;Lansac-Tôha et al., 2009; Lansac-Tôha et al., 2014) and the Middle Doce River basin (Barbosa et al., 2014).

The species richness found in the Ubatiba Stream may be associated with structuring of the sampled environments provided by riparian vegetation. The areas along the stream banks encompass a variety of microhabitats (Esteves, 2011; Silva et al., 2016). This condition could favor the biological richness of testate amoebae (Schwind, Arrieira, Mantovano, Bonecker, & Lansac-Tôha, 2016). The presence of Arcella in the planktonic environment can be justified by the flow of water from the stream, which promotes the resuspension of the sediment, facilitating the availability of nutrients for the species (Thomaz, Bini, & Bozelli, 2007). The current of the stream would also collaborate with the exchange of organisms among the existing biotopes, besides favoring the dispersion of the species throughout the stream (Miranda & Gomes, 2013; Miranda & Mazzoni, 2015).

The first records on Arcella in the State of Rio de Janeiro were made by Wailes (1913), which identified some species in mosses, and Cunha (1914), who registered this genus in samples of river plankton. Later Miranda and Gomes (2013) identified some species of Arcella composing the plankton of a small-order river located in the Baixada Fluminense. Miranda and Mazzoni (2015) reported species in a coastal stream in the metropolitan region, inhabiting plankton and ciliary vegetation, being the only study developed in streams in the State of Rio de Janeiro. Laut et al. (2011) reported some species in sediments of lagoons in the State, as well as Silva-Neto et al. (2015), which in addition to registering Arcella species in sediment samples, also found species in bromeliad tanks. Finally, Lopes et al. (2017) found some species of Arcella in reservoirs in the State.

Figure 2
Arcellidade of Ubatiba stream, Rio de Janeiro. (1) Arcella artocrea lateral view, (1a) ventral view; B (2) Arcella conica lateral view, (2a) ventral view; (3) Arcella costata lateral view, (3a) ventral view; (4) Arcella discoides lateral view, (4a) ventral view; (5) Arcella gibbosa lateral view, (5a) ventral view; (6) Arcella hemisphaerica undulata lateral view, (6a) ventral view; (7) Arcella megastoma lateral view, (7a) in ventral view; (8) Arcella vulgaris lateral view, (8a) ventral view.

Most species of the Family Arcellidae were present in the Ubatiba Stream during the dry and rainy seasons. This suggests that these organisms are able to adapt to seasonal variations that interfere with the hydrological and abiotic aspects of the stream, as well as the availability of nutrients to capture these testate amoebae (Miranda & Mazzoni, 2015, Rosa et al., 2017).

The presence of the Family Arcellidae in the Ubatiba Stream shows that lotic environments have a considerable richness of testate amoebae. However, the present study emphasizes the importance of encouraging the development of taxonomic surveys on testate amoebae in lotic ecosystems, especially in the State of Rio de Janeiro, where there is little information available about this community.

The current study is part of the PhD Thesis of VBSM and was supported by the Brazilian Agencies FAPERJ – 26-101.606/2014 and E-26/202.762/2018, CAPES 23038.012519/2018-46 and CNPq 301463/2017-4. Thanks to people from Laboratory of Fish Ecology/UERJ that helped in the field work. Thanks to PhD Gleyci Aparecida Oliveira Moser and other professionals of the Laboratory of Cultivation and Ecology of Marine Microalgae/UERJ (LABCULT/UERJ).