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Gomphonema Ehrenberg (Bacillariophyceae) in a lotic environment of the Upper Paraná River floodplain, Brazil
Gomphonema Ehrenberg (Bacillariophyceae) em ambiente lótico da planície de inundação do Alto Rio Paraná
Acta Scientiarum. Biological Sciences, vol. 39, no. 2, pp. 135-147, 2017
Universidade Estadual de Maringá

Algas



Received: 01 June 2016

Accepted: 28 October 2016

DOI: https://doi.org/10.4025/actascibiolsci.v39i2.32134

Abstract: A taxonomic study of species of the genus Gomphonema Ehrenberg (Bacillariophyceae) was performed in alotic environment (Ipoitã Channel) of the Upper Paraná River Floodplain. Samplings were performed in June, September and December 2013 and February 2014. Two petioles of Eichhornia azurea (Sw) Kunth were sampled at three different sites in the channel. Twelve species and two taxonomic varieties were identified. All species identified were recorded at the sampling site 3, loca ated close to the Ivinhema River. The lowest number of taxa occurred at the sampling site 1 (9 specific and infra specific taxa), in the confluence with the Paraná River. All taxa of Gomphonema were the first record for the Upper Paraná River Floodplain. Our results emphasize the lack of taxonomic studies for the region and the importance thereof to the knowledge of biodiversity.

Keywords: diatom, distribution area, periphyton, taxonomy.

Resumo: Realizou-se o estudo taxonômico das espécies do gênero Gomphonema Ehrenberg (Bacillariophyceae) em um ambiente lótico (canal Ipoitã) da planície de inundação do alto rio Paraná. As coletas foram realizadas em junho, setembro e dezembro de 2013 e fevereiro de 2014. Dois pecíolos de Eichhornia azurea (Sw) Kunth foram amostrados em três pontos distintos do canal. Foram identificadas 12 espécies e duas variedades taxonômicas, sendo que todas foram registradas no ponto 3, situado próximo ao rio Ivinhema. O menor número de táxons ocorreu no ponto 1 (9 táxons específicos e infra específicos), na área de junção com o rio Paraná. Todos os táxons do gênero Gomphonema são primeiro registro para a planície de Inundação do Alto Rio Paraná. Os resultados ressaltam a carência de trabalhos taxonômicos para a região e a importância destes para o conhecimento da biodiversidade.

Palavras-chave: diatomácea, área de distribuição, perifíton, taxonomia.

Introduction

The Upper Paraná River floodplain is characterized by heterogeneous habitats that confer high biodiversity to this environment (Thomaz, Bini, & Bozelli, 2007, Agostinho, Pelicice, & Gomes, 2008). Periphytic algae are one of the aquatic communities found in this ecosystem, with a high proportion of diatoms (Bacillariophyceae), especially in lotic environments. These algae present morphological adaptations that favor their attachment to substrates (Wehr & Sheath, 2003).

The diatom genus Gomphonema Ehrenberg is well represented in aquatic environments, presenting high richness and abundance. Gomphonema species are characterized by cuneiform cells in girdle view and hetero polar cells in valve view (Round, Crawford, & Mann, 1990). They generally attach to solid substrates through mucilage pads or stalks, secreted from the apical pore field located at the valve basis (Tremarin, Ludwig, Bertolli, Faria, & Costin, 2009a). In addition, cells possess a single H-shaped plastid with a central pyrenoid (Cox, 1996, Round et al., 1990). Several Gomphonema species are cosmopolitan. However, the morphological variability of frustules makes the taxonomy of this genus difficult (Krammer & Lange-Bertalot, 1986, 1991).

Approximately 90 Gomphonema species have been described for South America, 28 of which were recently proposed (Reichardt, 1995, Lange-Bertalot, Külbs, Lauser, Nörpel-Schempp, & Willmann, 1996, Metzeltin & Lange-Bertalot, 1998, Rumrich, Lange-Bertalot, & Rumrich, 2000, Metzeltin, Lange-Bertalot, & Garcia-Rodrigues, 2005, Silva, Nogueira, & Souza, 2011). Approximately 40 of those species have been recorded in Brazil (Torgan, Becker, & Prates, 1999, Tremarin et al., 2009a, Santos, Tremarin, & Ludwig, 2011).

Almost 22 species of Gomphonema have been recorded for aquatic environments in Paraná (Tremarin, Freire, Bertolli, & Ludwig, 2009b), and only four species for Mato Grosso do Sul. The present study is the first floristic survey of Gomphonema in the Paraná River floodplain, contributing to the knowledge and characterization of aquatic biodiversity in this region, including ecology and biomonitoring studies, for which the correct identification of taxa is essential.

The goal of the present study was to perform a taxonomic analysis of species of the genus Gomphonema in a lotic environment of the Upper Paraná River Floodplain, contributing to the knowledge regarding the distribution of these species.

Material and methods

The study site is the Ipoitã Channel (22° 50'S; 53° 33'W), located in the Upper Paraná River floodplain, which connects the Ivinhema and Paraná rivers, with an average depth of 3.2 m. Samples were taken at three different sampling sites in this channel: site 1 at the connection with the Paraná River, site 2 in the middle of the channel, and site 3 at the connection with the Ivinhema River (Figure 1). This channel is inserted in the state of Mato Grosso do Sul, although it is practically on the border with the state of Paraná.

The substrates used were petioles of Eichhornia azurea (Sw) Kunth in the adult stage (Schwarzbold, 1990), selected from banks of this macrophyte of similar shape and size and under similar environmental conditions.


Figure 1.
Upper Paraná River floodplain. The dashed line indicates the Ipoitã Channel.

Collections were performed in June, September and December 2013, and in February 2014. Periphytic algae were collected from the sixth or seventh plant internode of submerged mature petioles of Eichhorniaazurea (Sw.) Kunthas recommended by Schwarzbold (1990). This macrophyte was selected to this research because it was the most abundant and is used as a standard plant for the PELD- Long Term Ecological Research. Two petioles were collected randomly at each site, placed in 150 mL Wheaton bottles, sprayed with distilled water, and kept in boxes with ice. The periphytic material was subsequently removed using stainless steel bladesw rapped inaluminum foil and jets of distilled water. The resulting material was fixed in1:1 Transeau solution (Bicudo & Menezes, 2006).

Part of the sample was oxidized with potassium permanganate and hydrochloric acid, according to Simonsen (1974) as modified by Moreira-Filho and Valente-Moreira (1981). Due to the high amount of organic matter in the blades, the material was oxidized again according to Hasle and Fryxell (1970). The resins used to mount permanent slides were Hyrax for the first method and Nafrax for the second. One slide was mounted per site sampled in certain periods, resulting in 12 slides, in total. These slides were not quantified, but all of them were analyzed for species richness.

Gomphonema species were analyzed using a binocular microscope with amicrometer ocular and 100x objective, and images were captured using an Olympus DP-071 camera. The terminology used for species description followed Round et al. (1990). Taxa identification was based, whenever possible, with the original literature referred to in the text. Samples were deposited in the Herbário of Universidade Estadual de Maringá (HUEM).

To record the occurrence of taxa distribution was conducted a review of literature with taxonomic approach.

Results and discussion

A total 11 species and 3 taxonomic varieties belonging to genus Gomphonema were identified (Table 1). These taxa were distributed in one channel of the Upper Paraná River floodplain, located between the states of Mato Grosso do Sul and Paraná (Table 2).

Table 1.
Taxa of Gomphonema (Gomphonemataceae) recorded in Ipoitã Channel in the Upper Paraná River floodplain. It occurs in different regions (1: connection with Paraná River, 2: middle of the channel; 3: connection with Ivinhema River) and months (Jun: June, Sep: September, Nov: November, 2013; and Feb: February, 2014).

Table 2.
Taxa distribution of Gomphonema recorded in Ipoitã Channel in the Upper Paraná River floodplain, located between the states of Mato Grosso do Sul and Paraná.

Theses and dissertations were included, since they register the species and this information was not published in scientific article.

Identification key for Gomphonema species and varieties included the following observations:

Gomphonema affine var. affine Kützing, Bacill. Nordhausen. p. 86, pl. 30, fig. 54, 1844 (Figure 2/ 1-19).

Valves slightly heteropolar, lanceolate, with apices rounded and bases attenuate-rounded. Raphe sternum

narrow and linear. Raphes lightly sinuous with proximal ends slightly bent towards the stigma. Central area is asymmetrical, expanding until the valve margin is on one side of the valve due to the wider spacing of the median striae. Stigma located close to the medianstria. Striae straight to radiate, with one shortened striaon one side of the central nodule. Areola inconspicuous. Length: 35.8-51.7 µm; width: 7.6-10.5 µm; 9-13 striae in 10 µm.

Gomphonema affine is similar to Gomphonema amoenum Lange-Bertalot in its dimensions and valve outline. However, G. amoenum presents subrostrateapices and more radiate striae (Reichardt, 1999). The results of the analyzed population are in agreement with the morph metric data (length 36-88 µm, width 9-13.6 µm, 8-11 striae in 10 µm) of the tropical species material analyzed by Reichardt (1999).

Occurrence in samples: Huem-24354, 24355, 24356 collected on June 15th, 2013; Huem-24357, collected on August 30th, 2013.

Gomphonema angustatum (Kützing) Rabenhorst, Fl. Eur. Alg. I, p. 283, 1864.

Basionym: Sphenella angustata Kützing, Kies. Bacill. Diat., p. 83, pl. 8, fig. 4, 1844 (Figure 2/ 27-31).

Valves heteropolar, narrow lyclavate-lanceolate, with apices subrostrate and bases attenuate. Raphe sternum linear and narrow. Raphe straight or slightly sinuous, with proxima lends slightly bent towards the stigma. Central area unilateral formed by a shortened median stria. Stigma located close to the median stria. Striae straight, slightly radiate at the ends and with wider spacing at the median region of the valve. Areolae inconspicuous. Length: 16.4-21.1 µm; width: 3.5-4.7 µm; 11-15 striae in 10 µm.


Figure 2.
1-19: Gomphonema affine var. affine. 20: Gomphonema brasiliense. 21-26: Gomphonema sphaerophorum. 27-31: Gomphonema angustatum. 32-38: Gomphonema lagenula. 39-42: Gomphonema costei. Scale: 10 μm.


Figure 3.
Gomphonema turris var. coarctata. 45-48: Gomphonema neonasutum. 49-52: Gomphonema laticollum. 53: Gomphonema pumilum. 54-60: Gomphonema parvulum. 61-63: Gomphonema subtile. 64-65: Gomphonema salae. 66-73: Gomphonema mexicanum. Scale: 10 μm.

This species was found in others studies conducted in the state of Paraná. In Tremarin et al. (2009a), this species was found in the macrophyte Potamogeton polygonus and the individuals were larger than observed in our study.

Occurrence in samples: Huem-24354, 24355, 24356 collected on June 15th, 2013; Huem-24361, collected on November 29th, 2013.

Gomphonema brasiliense Grunow in Schneider, Naturw. Beitr. Kenntn. Kauk., p. 110, 1878 (Figure 2/ 20).

Valves slightly heteropolar, lanceolate, with apices cuneate-rounded and bases narrowly rounded. Raphe sternum wide and lanceolate. Raphes lightly sinuous with proxima lends bent towards the stigma. Central area rounded. Stigma absent. Striae short, straight toradiate along the length of the valve. Areolae inconspicuous. Length: 36.4 µm; width: 6.4 µm; 15 striae in 10 µm.

Gomphonema brasiliense ssp. pacificum Moser, Lange-Bertalot and Metzeltin can be differentiated from Gomphonema brasiliense by its narrower valves (3.6-5.2 µm) (Moser, Lange-Bertalot, & Metzeltin, 1998).

Occurrence in samples: Huem-24354, collected on June 15th, 2013; Huem-24363, collected on February 18th, 2014.

Gomphonema costei Metzeltin and Lange-Bertalot in Lange-Bertalot, Iconogr. Diatomol. 5: 115, pl. 154, fig. 7-12, 1998 (Figure 2/ 39-42).

Valves heteropolar, lanceolate, slightly swollen at the median region, with rounded apices and bases. Raphe sternum lanceolate. Raphe sinuous with proxima lends bent towards the stigma. Stigma rounded located close to the central nodule. Striae straight toradiate at the ends, coarse and shortened long the full length of the valve. Areolae conspicuous, difficult to observe. Length: 41.7-48.8 µm; width: 7.0-8.2 µm; 9-10 striae in 10 µm.

Gomphonema costei and Gomphonema evexus Hohn has very similar valve outline as well as identical dimensions and density of striae, suggesting that the species may be synonymized in the future (Patrick et al., 1966).

Occurrence in samples: Huem-24354, 24355, 24356 collected on June15th, 2013; Huem-24357, collected on August 30th, 2013; Huem-24360, collected on November 29th, 2013; Huem-24365, collected on February 18th, 2014.

Gomphonema lagenula Kützing, Kies. Bacill. Diat., p. 85, pl. 30, fig. 60, 1844 (Figure 2/ 32-38).

Valves heteropolar, lanceolate to elliptic-lanceolate, with apices subcapitateto subrostrate and bases subcapitate. Raphe sternum narrow and linear. Raphe straight with proxima lends bent towards the stigma. Central area unilaterally expanded, delimited by shortened median striae. Stigma located at the end of the median stria. Striaeuniseriate, straight to slightly radiate, with central striae more widely spaced than the others. Areola inconspicuous. Length: 21.1-25.8 µm; width: 5.8-6.4 µm; 14-16 striae in 10 µm.

Occurrence in samples: Huem-24354, 24355, 24356 collected on June15th, 2013; Huem-24357, 24358, 24359 collected on August 30th, 2013; Huem-24360, 24361, 24362, collected on November 29th, 2013; HUEM-24363, 24364, 24365, collected on February 18th, 2014.

Gomphonema laticollum Reichardt (2001) in Jahn et al., Studies on Diatoms, p. 199, pl. 5, fig. 1-14, 2001 (Figure 3/ 49-52).

Valves clavate, swollen at the median region and with little pronounced constriction between the median region and the apex. Apices widely rounded and bases attenuate-rounded. Raphe sternum narrow and linear. Raphe sinuous with proxima lends dilated in a pore shape, bent towards the stigma. Central area irregular delimited by shortened median striae. Stigma present. Striae uniseriate and radiate, formed by conspicuous areolae. Length: 21.1-25.8 µm; width: 5.8-6.4 µm; 14-16 striae in 10 µm.

Reichardt (2001) reviewed the species Gomphonema truncatum Ehrenbergand G. capitatum Ehrenberg and proposed G. laticollum Reichardt because it presents striae less pronounced constriction close to the valve apices.

Occurrence in samples: Huem-24354, 24355, 24356 collected on June15th, 2013; Huem-24357, collected on August 30th, 2013.

Gomphonema mexicanum Grunow in Van Heurck, Syn. Diat. Belg., pl. 24; fig.3, 1880. (Figure 3/ 66-73).

Valves heteropolar, lanceolate, with apices broadly rostrate and bases attenuate-rounded to subcapitate. Raphe sternum narrow and linear. Raphe weakly undulate, with proxima lends dilated in a pore shape. Central area unilaterally expanded, delimited by a shortened median stria. Stigma punctiform located close to the median stria. Striae straight to radiate close to the valve ends. Areola conspicuous, difficult to observe. Length: 20-34.7 µm; width: 8.8-10.5 µm; 12-13 striae in 10 µm.

Gomphonema mexicanum is very similar to G. affinopsis Metzeltin, Lange-Bertalot and García-Rodríguez, differentiated by the punctiform shape of the stigma, whereas in G. affinopsis, the stigma is elongated (Metzeltin & Lange-Bertalot, 1998).

Occurrence in samples: Huem-24354, collected on June 15th, 2013; Huem-24357, collected on August 30th, 2013.

Gomphonema neonasutum Lange-Bertalot and Reichardt in Lange-Bertalot, Iconogr. Diatomol. 5: 121, pl. 156, figs. 1-4, 1998 (Figure 3/ 45-48).

Valves heteropolar, lanceolate, slightly wollen at the median region, with apices cuneate-apiculate to cuneate-subrostrate and bases attenuate-rounded. Raphe sternum narrow and linear. Raphe sinuous with proxima lends dilated in a pore shape, bent towards the stigma. Central area irregular delimited by shortened median striae. Stigma located close to the median stria. Striae uniseriate, radiate. Areola conspicuous. Length: 67-89.4 µm; width: 14.7-17 µm; 9-10 striae in 10 µm.

Gomphonema neonasutum is similar to G. turris in valve morphology and size but differs in the apiculate shape of the apices (Metzeltin & Lange-Bertalot, 1998).

Occurrence at the samples: Huem-24354, collected on June 15th, 2013; Huem-24357, 24358, collected on August 30th, 2013; Huem- 24361, 24362, collected on November 29th, 2013; Huem-24363, collected on February 18th, 2014.

Gomphonema parvulum (Kützing) Kützing, Spec. Alg., p. 65, 1849. Basionym: Sphenella parvula Kützing, Kies. Bacill. Diat., p. 83, pl. 30, fig. 63, 1844 (Figure 3).

Valves heteropolar, lanceolate to elliptic-lanceolate, with apices subrostrate and bases attenuate-rounded. Raphe sternum linear, narrow. Raphe straight to slightly sinuous with proxima lends bent towards the stigma. Central area irregular and narrow, delimited by a shortened median stria. Stigma present. Striae uniseriate, straight to slightly radiate at the ends. Areola inconspicuous. Length: 14.1-19.4 µm; width: 4.7 µm; 14-17 striae in 10 µm.

Gomphonema micropus Kützing is morphologically similar to Gomphonema parvulum var. parvulum. However, the two species can be differentiated according to their differently organized apices and striae (Krammer & Lange-Bertalot, 1986, Reichardt, 1999). Gomphonema micropus also differs by being longer (19-44 µm) and wider (6.3-9 µm), and by its lower density of striae (11-14 in 10 µm) (Reichardt, 1999).

Occurrence in samples: Huem-24355, 24356, collected on June 15th, 2013; Huem-24357, collected on August 30th, 2013; Huem- 24361, 24362, collected on November 29th, 2013.

Gomphonema pumilum (Grunow) Reichardt and Lange-Bertalot, Nova Hedwigia 53(3-4): 528, pl. 6, figs. 4-11, 1991.

Basionym: Gomphonema intrincatum Kützing var. pumila Grunow in Van Heurck, Syn. Diat. Belg., pl.24, figs. 35-36, 1880 (Figure 3/ 53).

Valves clavate, with apices rounded and bases attenuate. Raphe sternum linear, narrow. Raphe filiform with proxima lends dilated in a pore shape, bent towards the stigma. Central area rounded. Stigma present. Striae straight to radiate. Areola inconspicuous. Length: 19.4 µm; width: 4.1 µm; 10 striae in 10 µm.

Occurrence in samples: Huem-24354, 24355, 24356, collected on June15th, 2013; Huem-24357, 24359, collected on August 30th, 2013; Huem-24360, 24361, 24362, collected on November 29th, 2013; Huem-24363, 24364, 24365, collected on February 18th, 2013.

Gomphonema salae Lange-Bertalot and Reichardt in Lange-Bertalot, Iconogr. Diatomol. 5: 548, pl. 157, figs. 3-5, 1998 (Figure 3/ 64-65).

Valves clavate, swollen at the median region and with slightly pronounced constriction between the median region and the apex. Apices cuneate-subrostrate and bases attenuate-rounded. Raphe sternum slightly linear, narrow. Raphe weakly sinuous with proxima lends bent towards the stigma. Central area unilateral, delimited by a shortened median stria. Stigma located close to the median stria. Striae uniseriate, straight to radiate close to the apices, with wider spacing at the median region. Areola inconspicuous. Length: 42.3-48.2 µm; width: 10-10.5 µm; 12-13 striae in 10 µm.

Gomphonema neonasutum differs from G. salae in size, and the apiculate shape of the apices. Furthermore, the number of striae in G. salae is greater than in G.neonasutum and G. turris (Metzeltin & Lange-Bertalot, 1998).

Occurrence in samples: Huem-24354, 24356, collected on June 15th, 2013.

Gomphonema sphaerophorum Ehrenberg, Ber. Bek. Verh. Köngl. Preuss. Akad. Wiss. Berl., p. 78, 1845 (Figure 2/ 21-26).

Valves heteropolar, lanceolate, with apices rostrate-capitate to subrostrate and bases capitate to subcapitate. Raphe sternum linear and narrow. Raphe filiform with proximal ends simple and rounded. Central area unilateral formed by a shortened median stria. Stigma located close to the median stria. Striae slightly radiate. Areolae rounded. Length: 43.5-56.4 µm; width: 12.9-13.5 µm; 9-12 striae in 10 µm.

Occurrence in samples: Huem-24354, 24355, 24356 collected on June 15th, 2013; Huem-24363, 24364, 24365, collected on February 18th, 2014.

Gomphonema subtile Ehrenberg, Abh. Königl. Akad. Wiss. Berl. 1841: 416, 1843 (Figure 3/ 61-63).

Valves heteropolar,lanceolate, with apices capitate and bases rounded. Raphe sternum narrow, linear. Raphe straight with proxima lend dilated in a pore shape. Central area unilateral formed by a shortened median stria. Stigma located close to the median stria. Areolae conspicuous but difficult to observe. Length: 46.4-49.4 µm; width: 7.6-8.2 µm; 9-10 striae in 10 µm.

Occurrence in samples: Huem-24354, collected on June 15th, 2013; Huem-24360, collected on November 29th, 2013; Huem-24363, 24365, collected on February 18th, 2014.

Gomphonema turris var. coarctata (Frenguelli) Frenguelli, Rev. Mus. La Plata, Sec. Bot. 3: 275, 1941.

Basionym: Gomphonema turris f. coarctata Frenguelli, An. Mus. Nac. Hist. Nat. 4: 423, pl. 4, figs. 35-36, 1933 (Figure 3/ 43-44).

Valves clavate, lanceolate, with apices cuneate-subrostrate and bases attenuate-rounded. Raphe sternum linear, narrow. Raphe slightly sinuous with proximal ends dilated in a pore shape and bent towards the stigma. Central areae lliptic or asymmetric, delimited by irregular shortening of the median striae. Stigma located close to the median stria. Striae uniseriate, straight to radiate near the ends. Areolae conspicuous. Length: 54.7-58.2µm; width: 15.2-15.8 µm; 10 striae in 10 µm; 18-22 areolae in 10 µm.

Occurrence in samples: Huem-24354, 24356 collected on June 15th, 2013.

In this study, only Gomphonema neonasutum is the first record to the state of Paraná (Table 1). The species that have been widely distributed was G. lagenula and G. parvulum. Only Gomphonema lagenula Kützing, a species with cosmopolitan distribution, occurred in all sampling sites and in all months.

The Ipoitã Channel is influenced hydro- logically by Paraná and Ivinhema rivers. The sampling site 3, located close to the Ivinhema River, was the most species-rich area (Table 2). This can be explained by the characteristics of the Ivinhema River, which has natural hydrodynamics, and because it is located in a protected area where there is still marginal vegetation and many flood areas (Souza Filho & Stevaux, 1997).

The lowest number of taxa occurred in the sampling site 1, at the connection with the Paraná River (Table 2). Paraná River is strongly impacted by dams and has higher water transparency and lower nutrient concentrations (Agostinho et al., 2008, Roberto, Santana, & Thomaz, 2009). The differences between these rivers may help to explain the distribution of species in the floodplain, and even the success of some species in certain habitats. Fluctuations in the water level of the Ivinhema River are independent from levels in the Paraná River (Souza Filho, Comunello, & Rocha, 2005), and this pattern also contributes to increase habitat heterogeneity among different riverine habitats in the floodplain (Roberto et al., 2009), elevating the biodiversity in this area. Higher periphyton biomasses, for example, are usually found in the Ivinhema River, which carries more phosphate than the Paraná River (Leandrini, Fonseca, & Rodrigues, 2008).

Conclusion

The present study contributes to the knowledge regarding diatom biodiversity in this region, and it provides support to future ecological and biomonitoring studies in the Upper Paraná River Floodplain. The results emphasize the lack of taxonomic studies for the region and the importance thereof to the knowledge of biodiversity.

Acknowledgements

The authors wish to thank the Long Term Ecological Research (Programa Ecológico de Longa Duração - PELD) and the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq) for financial support, and the Center for Research in Limnology, Ichthyology and Aquaculture (Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura - Nupélia) for logistic support during the field work.

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Author notes

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