Denticula, Hantzschia and Tryblionella (Bacillariaceae, Bacillariophyta) from northwestern Ceará freshwaters

Abstract

Diatoms constitute a representative portion of the algal community of freshwater aquatic environments, but their studies are centered mostly in the south and southern regions of Brazil, making the microalgae biodiversity of water bodies in the semiarid practically unknown. In the state of Ceará, the few records of the Bacillariaceae are centered in the southern region of the state and are generally not identified at specific level. Denticula, Hantzschia, and Tryblionella are worldwide distributed diatom genera that belong to the family Bacillariaceae. The group is characterized by raphe located on a channel, internally supported by silica extensions, the fibulae. This is a taxonomic study on the genera Denticula, Hantzschia, and Tryblionella found in water bodies in northwestern Ceará state. Planktonic and periphytic samples were collected in four hydrographic basins, which are influenced by the semiarid climate, located in northwestern Ceará, northeastern Brazil. Fourteen infrageneric taxa were identified, described, and illustrated, all being pioneer citations for Ceará. The present study highlighted the underestimated diversity of diatoms in the semiarid region of Ceará and the need to cover undersampled or never explored regions to significantly contribute to the knowledge of the diatom flora and its distribution in Brazilian aquatic environments.

Key words:
caatinga ; canal raphe; diatoms; microalgae; taxonomy

Resumo

As diatomáceas constituem uma porção representativa da comunidade algácea de ambientes aquáticos dulcícolas, mas seu estudo está centrado principalmente nas regiões sul e sudeste do Brasil, sendo a biodiversidade das microalgas em regiões semiáridas praticamente desconhecida. No estado do Ceará, os poucos registros das Bacillariaceae estão centrados na região sul do estado e, geralmente, os táxons não se encontram identificados em nível específico. Denticula, Hantzschia e Tryblionella são gêneros de diatomáceas distribuídos mundialmente, pertencentes à família Bacillariaceae. O grupo caracteriza-se pela rafe localizada em canal, internamente estruturada por extensões de sílica, as fíbulas. Este é um estudo taxonômico sobre os gêneros Denticula, Hantzschia e Tryblionella encontrados em corpos d’água no Noroeste do estado do Ceará. Amostras planctônicas e perifíticas foram coletadas em quatro bacias hidrográficas, que sofrem influência do clima semiárido, localizadas na região noroeste do Ceará, nordeste do Brasil. Quatorze táxons infragenéricos foram identificados, descritos e ilustrados, sendo todos citações pioneiras para o Ceará. O presente estudo evidenciou a subestimada diversidade de diatomáceas na região semiárida cearense e a necessidade de ampliação de abranger coletas em regiões subamostrados ou nunca exploradas para contribuir de maneira representativa para o conhecimento da diatomoflora e de sua distribuição em ambientes aquáticos brasileiros.

Palavras-chave:
caatinga; rafe em canal; diatomáceas; microalgas; taxonomia

Introduction

Denticula Kutzing, Hantzschia Grunow, and Tryblionella W. Smith, diatoms belonging to the Bacillariaceae family, are relatively widely distributed in marine and continental environments worldwide (Round et al. 1990). It is estimated that the genera comprise 45, 159, and 80 respectively, taxa taxonomically accepted respectively (Guiry & Guiry 2022).

Denticula Kutzing was described in 1844. Representatives from this genus have small, solitary, or short-chained frustules with linear or lanceolate valves, obtuse or slightly rostrated ends. The main characteristic is the presence of transapical ribs crossing the valve surface, visible under light microscopy, which are extensions of the fibulae (Ludwig & Tremarin 2006; Taylor & Cocquyt 2016).

Hantzschia was proposed by Grunow, in 1877, to group forms that differed from Nitzschia Hassall by their shape, positioning of the raphe system, and arrangement of fibulae (Round et al. 1990). Hantzschia has a dorsiventral valve, concave ventral margin, and convex dorsal margin, with capitate to rostrated ends, presenting a marginal raphe system and fibulae on the ventral margin of both frustule valves.

Tryblionella was originally proposed by Smith (1853). Round et al. (1990) placed Tryblionella and Nitzschia in the same family, but in different genera. This proposal was not adopted by Krammer & Lange-Bertalot (1997), for example, who adopted the subgeneric status for Tryblionella. Molecular studies confirm the paraphyletic character of the Nitzschia lato sensu (Lundholm et al. 2002a, b) and support Tryblionella as a distinct genus, in a phylogenetic clade close to Nitzschia strictu sensu (Rimet et al. 2011). Tryblionella has elliptical, linear or panduriform valves, wedge-shaped, rounded or sub-rostrated apices, a longitudinally undulating valve face, channeled and eccentric raphe, and transapical ribs parallel to the striae (Taylor & Cocquyt 2016).

The Brazilian catalogs (Tremarin et al. 2009; Torgan et al. 1999; Silva et al. 2011) register 13 species of Hantzschia, six species of Denticula and ten Tryblionella. Recently, Bertolli et al. (2020) updated to 23 species of Tryblionella registered in Brazil. The majority of this richness was found in the south and southeast Brazil, demonstrating the lack of studies in other regions of the country.

Studies on diatoms from Ceará began with Patrick (1940a, b), recording 52 species. Amorim et al. (2013) and Vieira et al. (2013) centered their studies in the southern region of the state and recorded about 65 taxa of diatoms, generally not identified at a specific level. None of these works, however, register species of Denticula, Hantzschia or Tryblionella.

To contribute to the expansion of the diatomological composition of the state of Ceará, the registration and description of morphological and metric variations of the species of Denticula, Hantzschia, and Tryblionella found in water bodies inserted in the northwest region of the state were carried out.

Material and Methods

The state of Ceará, located in the Northeast region of Brazil, covering an área of 148,886.3 km², and is subdivided into 12 hydrographic basins which encompass rivers, streams, lakes, and dams (IPECE 2016). Regarding to the rainfall in the region, there is a predominance of the rainy season, which occurs for around three to five months, alternating with the dry period, which lasts from seven to nine months (Bastos & Cordeiro 2012).

Approximately 90% of the total area of the state of Ceará has a semi-arid climate. Most water resources are limited and unstable, showing compromising points of pollution caused by industrial and agricultural activity, and from large urban centers (IPECE 2016).

The study area comprises the territorial portion of the mesoregion of Noroeste Cearense (Fig. 1), with about 58,500 km². The region influenced by the semiarid climate covers 48 municipalities and four hydrographic basins: Parnaíba Basin, Acaraú Basin, Coreaú Basin and Coastal Basin (FUNCEME 1993; IPECE 2008; Nascimento 2011).

Figure 1
Map of study area: hydrographic basins of northwestern region (in grey) of the state of Ceará, Brazil. Sampling locations (black circles) were numbered from 1 to 20. Information about the sampling points is shown in Table S1 (available on supplementary material <https://doi.org/10.6084/m9.figshare.23650905.v1>).

The collections were carried out between January 2016 and May 2019 in 20 locations, including dams, streams, rivers, waterfalls, and spouts inserted in hydrographic basins in northwestern Ceará (Fig. 1; Tab. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23650905.v1>). Periphytic samples (scraping rocks, subaerial humid bryophytes, and roots of underwater plants) and planktonic (net with 20μm mesh) were collected and preserved with a 4% v/v formalin solution. Temperature, pH and conductivity values were sampled in the field (from site water, collected with a container), using GHka portable pH meter (Model PG 1400) and conductivity meter (Model CG 1400).

In the laboratory, samples were oxidized using the Simonsen method (1974) changed by Moreira-Filho & Valente-Moreira (1981). Permanent slides were prepared with the oxidized samples and mounted with Naphrax® resin (i.r. = 1.74). Images were obtained by a DP 071 capture camera coupled to a light microscope (LM), Olympus BX 40. Subsamples of the oxidized material were deposited on aluminum supports, sputtered with gold-palladium in Balser Sputtering/SDC300, and observed in a TESCAN VEGA 3 LMU scanning electron microscope, operated at 15 kV and 8 mm away, at the Electron Microscopy Center (CME/UFPR).

The identification of taxa was based on morphological and meristic analysis of populations, consultations in classical literature (Schmidt 1874-1959; Hustedt 1930; Huber-Pestalozzi 1942; Krammer & Lange-Bertalot 1988), Iconographies (Metzeltin & Lange-Bertalot 1998, 2007) and more recent taxonomic articles (Bertolli et al. 2020). The terminology for the description of taxa follows Barber & Haworth (1981), Round et al. (1990), and Hamsher et al. (2014).

Liquid samples and their permanent studied slides were deposited in the herbarium of UFPR (UPCB) and the State University of Vale do Acaraú - Sobral (HUVA) (Tab. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23650905.v1>).

Results and Discussion

Based on the analysis of 20 samples from the northwest region of Ceará, mostly of periphytic origin, fourteen infrageneric taxa were observed. Tryblionella was the most representative genus, with eight taxa, followed by Hantzschia (five taxa) and Denticula (one taxa).

The respective descriptions and comments are presented below.

Denticula Kutzing.

Denticula aff. ranierensis Sovereign, Proceedings of the California Academy of Sciences, series 4, v. 31, n. 14, p. 364; figs. 22-24, 1963. Fig. 2a-j

Figure 2
a-j. Denticula ranierensis – a-h. valves in LM; i-j. valves in SEM – i. external view of the whole valve, transapical fibulae with thickenings near the valve margins and raphe canal open to the valve interior by elliptical portulae; j. internal view of the whole valve showing striation pattern and raphe endings. Bars: a-h = 10 µm; i-j = 2 µm.

At LM the valves are lanceolate to linear-lanceolate, with acutely rounded apices. Length 11–13.9 µm; breadth 2.5–3 µm. Striae unresolved in LM, fibulae (costae) 7–8 in 10 µm, extending transapically from margin to margin. (n = 41).

At SEM are observed filiform raphe, proximal raphe endings are dilated in pores, curved toward the valve mantle (Fig. 2i), distal raphe ends hooked, 6–8 striae between the fibulae (Fig. 2i,j), 45 striae in 10 µm, arranged in double rows, with 45–48 in 10 µm small rounded areolae (n = 2). Two thickenings occur near the valve margins on each transapical fibulae (Fig. 2j). The raphe canal is open to the valve interior by circular to elliptical portulae (Fig. 2j). (n = 2).

Examined material: Ipu, Bica do Ipu (UPCB: 78396, HUVA: 24520). Population found in epifíton of humid subaerial samples, associated with bryophytes.

Denticula ranierensis is described with acutely to broadly rounded ends and slightly radiating fibulae (costae) at the apices, in contrast to D. subtilis with very sharp apices and parallel fibulae throughout the valve (Lange-Bertalot & Krammer 1993; Johansen et al. 1994). Furthermore, the density of striae (26–30 in 10 µm) assigned to D. subtilis is much lower than the range reported to D. ranierensis (45–52 in 10 µm) (Lange-Bertalot & Krammer 1993; Johansen et al. 1994). The shape of the apices, the fibulae pattern and the striae density of the population studied here are closer to the circumscription of D. ranierensis. However, as we observed by SEM (Fig. 2i-j), the striae of Ceará population are organized in double rows throughout the valve. In D. ranierensis, as presented in Johansen et al. (1994), the striae in the type material are composed of irregular rows of areolae, showing a distinct striation pattern. Lange-Bertalot & Krammer (1993, figs. 39-43) presented a population from Ulla River (Spain), very similar to the individuals found in the present study, with striae in double rows, identified as D. sundaysensis Archibald. However, D. sundaysensis is originally described by Archibald (1982), as having striae in double rows composed of much larger areolae, consequently, lower striation density (ca. 20 in 10 µm). More detailed studies comparing type materials of mentioned species complex are necessary to resolve the precise identification of the taxon described and illustrated here (Fig. 2a-j).

Hantzschia Grunow.

Hantzschia abundans Lange-Bertalot, Bibliotheca Diatomologica v. 27, p. 75-76; pl. 85, fig. 12-18, pl. 89, fig. 1-6, pl. 90, fig. 1-6, pl. 92, fig. 1, 1993. Fig. 3a-c

Figure 3
a-c. Hantzschia abundans – valves in LM. d. H. calcifuga – valves in LM. Bars: d = 10 μm.

At LM the valves are donsiventral with a weakly convex to almost straight dorsal margin and a ventral margin slightly concave in the center to convex near the apices. Apices subcapitate to capitate slightly deflected to the dorsal side. Length 43.1–82.6 µm, breadth 5.6–11.6 µm. Fibulae equidistant, 5 in 10 µm, the two median more distant than the others. Each fibula is connected to 1–4 transapical costae. Striae parallel, 16–18 em 10 µm. (n = 3).

Examined material: Meruoca, Sítio Cachoeira (UPCB 78418; HUVA 24542). Sobral, Acaraú river (UPCB-78406; 78407; HUVA 24530, 24531). The species occurred in epiphytic and phytoplanktonic samples.

Hantzschia abundans is similar to H. amphioxys (Ehrenberg) Grunow due to its valve shape, differing basically in terms of dimensions, striae density, and raphe structure (Zidarova et al. 2010). H. abundans is 40–80 µm long and 7–10 µm wide, with 5–8 fibulae and 15–20 striae and 40 areolae in 10 µm. The dimensions of H. amphioxys are 15–50 µm in length and 5–7 µm in width, in addition to 20–29 striae and 40–50 areolae in 10 µm (Lange-Bertalot 1993). Observations of the frustule in scanning electron microscopy help to delimit the species Hantzschia amphioxys and Hantzschia abundans. The proximal raphe endings in H. amphioxys have an “L” shape directed to opposite sides and in H. abundans the termination is rounded directed to the same side, almost straight (Zidarova et al. 2010; Bulínová et al. 2018). It was not possible to get images of the raphe endings. Although different shapes are still found in literature, the length, valve width and density of striae were decisive to differentiate them. In a recent study (Maltsev et al. 2021), H. abundans was described according to all the main morphological characteristics already documented by Lange-Bertalot (1993), except for some smaller strains (37.5–39 µm and 6–7 µm). Also, the molecular data of H. abundans studied strains shared 95.61–96.67% similarities with those of H. amphioxys, and, according to Maltsev et al. (2021), H. abundans needs to have a taxonomic revision.

Hantzschia amphioxys (Ehrenberg) Grunow K. Svenska Vetenskapsakademiens Handlingar, v. 17, p. 103, 1880.

Basionym: Eunotia amphioxys Ehrenberg, Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin p. 413, pl. 1/1, fig. 26, pl. 1/3, fig. 6. 1843. Fig. 4a-s

Figure 4
a-s. Hantzschia amphioxys – a-o. valves in LM; p-s. valves in SEM. Bars: a-q = 10 µm; r-s = 2 µm.

At LM the valves are dorsiventral, with a concave ventral margin in the middle, convex at the ends, and convex dorsal margin. Apices rostrated to subcapitated. Length 23.6–49.1 µm, breadth 4–8.4 µm. Fibulae irregular in size, 6–11 in 10 µm, the two medians farther apart than the others. Striae radiate to parallel near the apices, 22–24 in 10 µm, (n = 76).

At SEM the striae are unisseriate parallel, to curve radiate and convergent near the apices, areolae small, 7–8 in 2 µm (Fig. 4r-s). Fibulae irregular in size, connected to 1–3 interstriae (n = 3).

Examined material: Catunda, Celso weir (UPCB: 78411, HUVA: 24535). Ipu, Bica do Ipu (UPCB: 78396, HUVA: 24520). Sobral, Acaraú River (UPCB 78405, HUVA 24529). The species occurred in epiphytic, epilithic, and epipsammic samples.

Hantzschia calcifuga E. Reichardt & Lange-Bertalot, in: Werum & Lange-Bertalot, p.163, pl. 96, figs. 1-6, pl. 97, figs. 1-4, 2004. Fig. 3d

At LM the valves are dorsiventral, with a concave ventral margin in the center and a slightly convex dorsal margin. Apices prolonged rostrated to subcapitated. Length 75.6 µm, breadth 7.8 µm. Fibulae irregular in size, 8 in 10 µm, connected to 1–4 transapical striae, the two medians farther apart than the others. Striae 19 in 10 µm, radiated, parallel near the apices. (n = 1).

Examined material: Massapê, temporary pond near the Acaraú river (UPCB- 78399, HUVA 24523). The species occurred in an epiphytic sample.

Hantzschia calcifuga differ from H. amphioxys and H. abundans by the most elongated shape, the more concave median region of the ventral margin, and by the apices facing the dorsal side (Lange-Bertalot et al. 2017).

Hantzschia elongata (Hantzsch) Grunow, Monthly Microscopical Journal, London, v. 18 p.174, pls 193-196, 1877.

Basionym: Nitzschia vivax var. elongata Hantzsch, Hedwigia v. 2, n. 7, p. 1-40, pl. 6, 1860. Fig. 5a-e

Figure 5
a-e. Hantzschia elongata – a-d. valves in LM; e. valve in SEM. f. H. yili -valve in LM. Bars: a-d, f = 10 µm; e = 2 µm.

At LM the valves are dorsiventral with convex dorsal margin and concave ventral margin. Apices attenuated, subcapitate. Length 99.4-222.7 µm, breadth 5.9-10.3 µm. Fibulae delicate, not equidistant, 6-8 in 10 μm, and the two medians farther apart than the others. Striae paralell, 16-18 in 10 µm. Length/breadth ratio: 26.2-30 μm. (n = 9).

At SEM the striae are unisseriate, areolae rounded 7 in 2 µm, fibulae irregular in size (Fig. 4e). (n = 06).

Examined material: Sobral, Acaraú River (UPCB-78408; HUVA 24532). The species occurred in epiphytic samples.

The observed individuals displayed shorter lengths than those measured by Krammer & Lange-Bertalot (1988) and Hustedt (1930) (Length 230-430 μm and width 10-14 μm in width). Individuals with smaller valves fit in the Hantzchia vivacior concept in terms of length, but differ in width dimensions (Length 77-150 µm, width 9.5-12.5 µm) (Lange-Bertalot 1993; You et al. 2015). The studied population were identified as H. elongata due to their more elongated shape.

Hantzschia yili Q.-M.You & Kociolek, in: You Q, Kociolek JP & Wang Q Phytotaxa, v. 1, pl.5-6, fig.6, 2015. Fig. 5f

At LM the valves are dorsiventral with slightly convex dorsal margin; ventral margins almost straight and slightly concave in the median region. Prolonged capitate apices. Length 85.9 µm, breadth 7.5 µm. Fibulae equidistant, 11 in 10 µm, the two medians farther apart than the others. Striae parallel, 21 in 10 µm, difficult to resolve in LM. (n = 01).

Examined material: Massapê, temporary pond near the Acaraú River (UPCB- 78399; HUVA 24523). The species occurred in an epiphytic sample.

Hantzschia angusta a similar species, differs from H. yili by the narrower valve dimension (6-6.5 µm) (Lange-Bertalot et al. 2003; You et al. 2015).

Tryblionella Smith.

Tryblionella angustata W.Smith, A synopsis of the British Diatomaceaee British Diatomaceae, p.36, pl.30, fig.262, 1853. Fig. 6a-j

Figure 6
a-j. Tryblionella angustata – valves in LM. k-t. T. balatonis – valves in LM. u-x. T. callida – valves in LM. Bars: a-x = 10 µm.

At LM the valves are lanceolate with acute wedge-shaped apices (Fig. 5a-i). Length 18-46.3 µm breadth, 4.9-7.2 µm in width. Fibulae delicate equidistant marginal. Striae equidistant uniseriate, parallel on valve extension slightly radiating at ends 12-17 to 10 μm. Areolae rounded, coarse, 13-16. (n = 16).

Examined material: Massapê, Acaraú River (UPCB 78405, 78406; HUVA 24529, 24530). Sobral, Acaraú River (UPCB 78403; HUVA 24527). Sobral/Taperuaba, Olho d´água do Pajé (UPCB- 78400; HUVA 24524). The species occurred in epiphytic, epilithic, epipsammic and phytoplanktonic samples.

Tryblionella angustata is similar to T. brunoi (Lange-Bertalot) Cantonati & Lange-Bertalot, but T. brunoi has greater length (45-80 μm) and breadth (9-13 μm) and lower striae density (12-13 in 10 μm) (Lange-Bertalot et al. 2017).

Tryblionella balatonis (Grunow) DG Mann, in: Round FE, Crawford, RM & Mann, DG The diatoms p. 678. 1990.

Basionym: Nitzschia balatonis Grunow, Kongliga Svenska Vetenskaps-Akademiens Handlingar v.17, p.70, pl.7, 1880. Fig. 6k-t

At LM the valves are eliptic-lanceolate with narrowly rostrated apices (Fig. 5j-s). Length, 14.8–17.1 µm, breadth 4.6–5.5 µm. Fibulae faintly distinguishable, 17–19 in 10 µm. Striae uniseriate, equidistant, 17-19 in 10 μm, parallel to slightly curved in the apices, formed by rounded areolae. Longitudinal fold barely visible. (n = 12).

Examined material: Massapê, Acaraú River (UPCB 78405, HUVA 24529). Sobral, Acaraú River (UPCB 78403, 78407; HUVA 24527, 24531). The species occurred in epipsammic and phytoplanktonic samples.

The population analysed in samples from Ceará state is quite similar to Nitzschia compressa var. balatonis Lange-Bertalot, described by Krammer & Lange-Bertalot (1998), regarding the valve shape and dimensions (lenght 12.5–30 µm, breadth 3.5–8 µm) and the striae density (16–21 em 10 µm). The taxon was previously denominated as a variety of T. compressa due to similarities in the valve shape. However, T. compressa (Bailey) Poulin has coarser areolae and larger measures of length (34 µm) and width (18,5 µm) and density of striae (9 in 10 µm) (Potapova et al. 2022), justifying the species taxonomic level in T. balatonis.

Tryblionella calida (Grunow) D.G. Mann, in: Round, R.M. Crawford & D.G. Mann, p. 678, 1990. Basionym: Nitzschia calida Grunow, in: Cleve & Grunow Kongliga Svenska Vetenskaps-Akademiens Handlingar, v.17, p.75, pl.7, 1880.

Fig. 6u-w At LM the valves are linear with slightly concave margins in the median region, more noticeable on the fibular margin, with wedge-shaped, subrostraste apices (Fig. 5t-x). Length 35.1–55.5 µm, width 6.5–7.1 µm. Fibulae distinct, 9-11 at 10 µm and the two medians further apart than the others. Parallel transapical ribs 17-20 at 10 µm. Striae parallel on valve extension to slightly curved at apices, 17-20 at 10 m. Areolae indistinct in LM. Longitudinal fold barely visible. (n = 4).

Examined material: Massapê, Acaraú River (UPCB 78405,78406; HUVA 24529, 24530). The species occurred in epiphytic, epipsammic samples.

Tryblionella debilis Arnott ex O’Meara, Quarterly Journal Microscopical Science, (13): 310, 1873. Fig. 7a-o

Figure 7
a-o. Tryblionella debilis – a-l. valves in LM; m-o. valves in SEM. Bars: a-l = 10 µm; m-n = 2 µm; o = 5 µm.

At LM the valves are elliptical-lanceolate with wedge-shaped to subrostrated apices (Fig. 6a-l) valve surface with differentiated ornamentation, one side with transverse ribs and the other with delicate granules. Length 18.7-21.5 μm, breadth 6-8.1 μm. Conspicuous marginal fibulae, not equidistant. Crossed ribs longitudinal fold, producing a zigzag pattern appearance, 13 in 10 µm. (n = 59).

At SEM are observed the longitudinal folds on the valve surface (Fig. 6m-n). Transapical costae alternate with sriae. Striae parallel in the central valve and radiated in the apices, 5 in 2 µm, composed of 2-3 rows of areolae (Fig. 6o). Valve surface with longitudinal live of grouped scales (Fig. 6o). Mantle with elongated areolae (Fig. 6m). (n = 4).

Examined material: Ipu, Bica do Ipu (UPCB: 78396, HUVA: 24520). Viçosa do Ceará, Mamoeiro pond, Quatiguaba River (UPCB: 78413, HUVA: 24537). The species occurred in epiphytic and epilithic samples.

Tryblionella debilis Bertolli & Torgan resembles T. confusa in dimensions (length 16.3– 27.6 μm, width 7.17-10 μm and 7-10 fibulae in 10 μm) (Bertolli et al. 2019), but in T. debilis transapical ribs are not asymmetric, and the striae are more distinguishable in the whole valve face. (Bertolli et al. 2020; Krammer & Lange-Bertalot 1988).

Tryblionella granulata (Grunow) DG Mann, in: Round, RM Crawford & DG Mann, The Diatoms, p. 678. 1990.

Basionym: Nitzschia granulata Grunow, in: Cleve, P. T. & Grunow, A. Kongliga Svenska Vetenskaps-Akademiens Handlingar, v.17, p. 68, pl. 7, 1880. Fig. 8a-c

Figure 8
a-c. Tryblionella granulata – valves in LM; d-j. Tryblionella hungarica – valves in LM; k-l. T. persuadens – valves in LM; m-t. T. victoriae – valves in LM. Bars: a-t = 10 µm.

At LM the valves are elliptical-lanceolate. Apices rounded to slightly wedge-shaped. Length 21.8-27.7 µm, breadth 9-12 µm. Fibulae equidistant, 7-8 in 10 µm. Striae uniseriate, parallel to slightly curve-radiated at the apices, 7-8 in 10 µm, composed by large rounded or elliptical areolae, 8-9 in 10 µm. (n = 4).

Examined material: Massapê, Acaraú River (UPCB 78406; HUVA 24530). Sobral/Taperuaba, Olho d’água do Pajé (UPCB 78400; HUVA 24524). The species occurred in epiphytic and epilithic samples.

Tryblionella granulata is similar to T. compressa by the striae with coarse areolae, but T. compressa has a larger linear-elliptical valve contour and rostrate to apiculate ends. (Bertolli et al. 2020; Krammer & Lange-Bertalot 1988).

Tryblionella hungarica (Grunow) Frenguelli, Revistadel Museo de La Plata. p.178, pl.8, fig.12, 1942.

Basionym: Nitzschia hungarica Grunow, Verhandlungen der kaiserlich-königlichen zoologisch-botanischen Gesellschaft in Wien, p.568, pl. 28-12, fig.31, 1862. Fig. 8d-j

At LM the valves are linear-lanceolate slightly constricted in the median region. Apices subrostrate little prolonged. Length 63.1-87.8 μm, width 10.2-11.6 μm. Fibulae irregularly distributed the two medians further apart, 9 in 10 µm. Transapical ribs 15-17 in 10 µm. Striae 15-17 in 10 µm. Presence of a median longitudinal undulation. (n = 08).

Examined material: Graça, Belizário waterfall (UPCB 78398, HUVA 24522). Massapê, Acaraú River (UPCB 78405, 78406; HUVA 24529, 24530). Sobral, Acaraú River (UPCB 78403, 78407; HUVA 24527, 24531). The species occurred in epiphytic, epilithic, epipsammic and phytoplanktonic samples.

Tryblionella hungarica is similar to T. acuminata. The last difers by having wider transapical axis (13-18 μm), and lower striae and fibulae densities (12-16 in 10 µm striae, 4-6 in 10 µm fibulae) (Krammer & Lange-Bertalot 1988).

Tryblionella persuadens (Cholnoky) K.P. Cavalcante, PI. Tremarin & T.A.V Ludwig, in: Cavalcante et al. Annals of the Brazilian Academy of Science, (85): 1420. 2013.

Basyonim: Nitzschia persuadens Cholnoky, Hydrobiologia, p.319, fig.74, 1961. Fig. 8k-m

At LM the valves are linear-lanceolate, slightly panduriform, constricted in the median region. Apices wedge-shaped to subrostrated. Length 19.7-19.9 µm, breadth 5.1-5.4 µm. Fibulae equidistant, 13-15 at 10 µm, and the two medians further apart than the others. Striae parallel along valve extension and slightly radiating at the ends. Presence of longitudinal undulation. Areolas indistinct in LM. (n = 2).

Examined material: Sobral, Acaraú River (UPCB 78403, 78407; HUVA 24527, 24531). The species occurred in phytoplanktonic samples.

Tryblionella persuadens is similar to T. aerophila Hustedt, differing by having a higher density of fibulae in 10 µm and shorter length and breadth compared to T. aerophila (length 23-31 µm, breadth 6-8 µm, 26-30 striae in 10 µm, 9-11 fibulae in 10 µm) (Krammer & Lange-Bertalot 1988). This taxon was originally described for brackish water (Cholnoky & Claus 1961). Cavalcante et al. (2013) proposed the new combination T. persuadens, previously belonging to the genus Nitzschia, documenting its occurrence in the state of Bahia by LM and SEM.

Tryblionella victoriae Grunow Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien, v.12, p.553, pl.12, fig.34, 1862. Fig. 8n-u

At LM the valves are linear-lanceolate slightly constricted in the median region. Apices cuneate. Length 25.8-53.3 µm, breadth 12.6-21.5 µm. Fibulae equidistant from the two most distant medians, 6-7 at 10 µm. Coarse transapical costae, equidistant, 7-9 by 10 µm, alternately distributed on both sides producing a zigzag pattern, parallel in valve extension and slightly radiating at the ends. Presence of longitudinal undulation (n = 15).

Examined material: Massapê, Acaraú River (UPCB 78406; HUVA 24530). Sobral, Acaraú River (UPCB 78403; HUVA 24527). Viçosa do Ceará, Mamoeiro pond, Quatiguaba River (UPCB 78413; HUVA 24536). The species occurred in epiphytic and phytoplanktonic samples.

Tryblionella victoriae taxon is similar to T. levidensis W. Smith. According to Lange-Bertalot et al. (2017), the valve morphology and dimensions overlap (18-65 μm long, 8-23 μm wide, and 7-10 striae 10 μm ribs). However, T. levidensis display a different morphology, very delicate striae and costae, and more elongated valve (18-54 μm long, 9-14 μm wide) (Hustedt 1930; Mann 1978).

All taxa are first citations to the state of Ceará and Tryblionella was the most representative genus with eight species documented. Analyzing the diatomological studies in the Northeast of Brazil (Gomes et al. 2003; Santiago-Hussein & Oliveira, 2006; Sá et al. 2018; Aquino et al. 2015; Ferrari et al. 2014; Cavalcante et al. 2014; Dantas 2010; Dantas et al. 2008; Souza et al. 2007; Azevedo 1999), we noticed the lack of registry entries of the documented taxa for the region. Only three had been previously cataloged: Tryblionella hungarica and T. granulata, registered in the archipelago of Fernando de Noronha, state of Pernambuco (Costa et al. 2009), and T. persuadens, registered in the state of Bahia (Cavalcante et al. 2013). Hantzschia calcifuga and Tryblionella balatonis were registered for the first time in Brazil. Denticula aff ranierensis needs more detailed studies comparing type materials of D. subtilis and D. sundaysensis to resolve the precise identification of the taxon described and illustrated here.

The caatinga is one of the most extensive semi-arid regions in the world. Unfortunately, in Brazil, this important environment is suffering anthropic impacts with widespread devastation and compromise of water resources. We highlight the importance of carrying out inventories of species, detailed taxonomic studies, fundamental information in environmental assessments and in the knowledge of biodiversity in regions that are still little or not explored, spread across this huge country.

Acknowledgments

To the Center for Electron Microscopy of the Federal University of Paraná, for SEM availability. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) provided a Master’s degree scholarship for GAM, and a productivity Grant for TAVL (process number: 311876/2019-6).

• See supplementary material at <https://doi.org/10.6084/m9.figshare.23650905.v1>

References

• Amorim C.A, Lucas F.HR, Rangel AJ & Lacerda SR (2013) Variação sazonal de microalgas perifíticas associadas a macrófitas aquáticas em reservatório na região do Cariri - Ceará. In: Seabra G (org.) Educação e cooperação pela água para a conservação da biodiversidade. Vo . 3. Editora Universitária, João Pessoa. Pp. 412-419.
• Aquino EP, Borges GCP, Silva MH, Passavante JZO & Cunha MGGS (2015) Phytoplankton in a tropical estuary, Northeast Brazil: composition and lifeforms. CheckList 11: 1633.
• Archibald REM (1982) Diatoms of South Africa 1. New species from the Sundays River (Eastern Cape Province). Bacillaria 5: 23-42.
• Azevedo ACG (1999) Composição florística das diatomáceas (Bacillariophyta) epífitas em duas espécies de Bostrychia Montagne (Rhodophyta). Insula 28: 101-101.
• Bastos FH & Cordeiro AMN (2012) Fatores naturais na evolução das paisagens no semiárido brasileiro: uma abordagem geral. Revista Geonorte 3: 464-476.
• Bertolli LM, Talgatti DM, Nascimento TMS & Torgan LC (2019) Two new species of Tryblionella W. Smith (Bacillariaceae, Bacillariophyta) from a southern Brazil salt marsh. Phytotaxa 399: 173-186.
• Bertolli LM, Talgatti DM, Nascimento TMS & Torgan LC (2020) The genus Tryblionella W. Smith (Bacillariaceae, Bacillariophyta) in southern Brazil salt marshes. Biota Neotropica 20: 1-14.
• Barber HG & Haworth EY (1981) A guide to the morphology of the diatom frustule. Freshwater Biological Association, Ambleside. 57p.
• Bulinová M, Kochman-Kędziora N, Kopalová K & Vijver BV (2018) Three new Hantzschia species (Bacillariophyta) from the maritime antarctic region. Phytotaxa 371: 168-184.
• Cavalcante KP, Tremarin PI, Freire EG & Ludwig TAV (2013) Tryblionella persuadens comb. nov. (Bacillariaceae, Diatomeae): new observations on frustule morphology of seldom recorded diatom. Ann. Braz. Acad. Sci 85: 1419-1426. <http://dx.doi.org/10.1590/0001-37652013108112>.
  » https://doi.org/10.1590/0001-37652013108112
• Cavalcante KP, Tremarin PI & Ludwig TAV (2014) New records of amphoroid diatoms (Bacillariophyceae) from Cachoeira River, Northeast Brazil. Brazilian Journal of Biology 74: 257-263.
• Cholnoky BJ & Claus G (1961) Beiträge zur Kenntnis der Algenflora und der Ökologie der Diatomeen in dem Stausee Wemmershoek-Dam nahe Kapstadt. Österreichische Botanische Zeitschrift 108: 325-350.
• Cleve PT & Grunow A (1880) Beiträge zur Kenntniss der arctischen Diatomeen. Kongliga Svenska Vetenskaps-Akademiens Handlingar 17: 1-121.
• Costa MMS, Leça EE, Pereira SMB & Pedrosa MEB (2009) Diatomáceas epífitas em Galaxaura rugosa (J. Ellis & Solander) JV Lamouroux (Rhodophyta) no Arquipélago de Fernando de Noronha, PE, Nordeste do Brasil. Acta Botanica Brasilica 23: 713-719.
• Dantas EW, Moura AN, Bittencourt-Oliveira MC, Neto JDTA & Cavalcanti ADC (2008) Temporal variation of the phytoplankton community at short sampling intervals in the Mundaú reservoir, Northeastern Brazil. Acta Botanica Brasilica 22: 970-982.
• Dantas EW (2010) Ecologia da comunidade de algas planctônicas em reservatórios de Pernambuco (Nordeste, Brasil). Tese Doutorado. Universidade Federal Rural de Pernambuco, Recife. 143p.
• Ehrenberg CG (1843) Verbreitung und Einfluss des mikroskopischen Lebens in Süd- und NordAmerika. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin 1841: 291-466.
• Ferrari F, Wetzel CE, Ector L, Bicudo DC & Bicudo CEM (2014) A new uncommon epilithic Eunotia (Bacillariophyceae, Eunotiaceae) from the Chapada Diamantina region, Northeast Brazil. Phytotaxa 164: 161-174.
• Frenguelli J (1942). XVII Contribución al conocimiento de las diatomeas argentinas. Diatomeas del Neuquén.(Patagonia). Revista del Museo de la Plata 5: 73-219.
• FUNCEME (1993) Redimensionamento da região semi-árida do nordeste do Brasil. FUNCEME, Fortaleza.
• Gomes DAB, Silva EM & Fernandes LF (2003) Diatomáceas como indicadoras de mudanças ambientais da Baía de Iguape, Baixo Paraguaçu (Bahia, Brasil). In: IX Congresso da ABEQUA-Associação de Estudos do Quaternário. CD-ROM de resumos expandidos.
• Grunow A (1862) Die Österreichischen Diatomaceen nebstAnschluss einiger neuen Arten von andern Lokalitäten und einer kritischen Uebersicht der bisher bekannten Gattungen und Arten. Verhandlungen der kaiserlichköniglichen zoologisch botanischen Gesellschaft in Wien 12: 553.
• Grunow HA & Kitton F (1877) New diatoms from Honduras. The Monthly Microscopical Journal 18: 165-186.
• Guiry MD & Guiry GM (2022) AlgaeBase. National University of Ireland, Galway. Available at <http://www.algaebase.org>. Access on 10 January 2022.
  » http://www.algaebase.org
• Hamsher SE, Graeff CL, Stepanek JG & Kociolek JP (2014) Frustular morphology and polyphyly in freshwater Denticula (Bacillariophyceae) species, and the description of Tetralunata, gen. nov. (Epithemiaceae, Rhopalodiales). Plant Ecology and Evolution 3: 346-365.
• Hantzsch CA (1860) Neue Bacillarien: Nitzschia vivax var. elongata, Cymatopleura nobilis Hedwigia 7: 1-40.
• Huber-Pestalozzi G (1942) Diatomeen. In: Thienimann A (ed.) Das Phytoplankton des Süsswassers Systematik und Biologie. Stuttgart E. Schweizerbart’sche Verlagsbuchhandlung 2: 549.
• Hustedt F (1930) Bacillariophyta (Diatomeae). In: Pasher A (ed.) Die Süsswasser-Flora Mitteleuropas. Zweite Auflage. Heft 10. Gustav Fisher, Jena. 466p.
• IPECE (2008) Características geográficas, recursos naturais e meio ambiente. Ceará em números. Instituto de Pesquisa e Estratégia Econômica do Ceará. Pp. 21-43. Available at <http://www2.ipece.ce.gov.br/publicacoes/ceara_em_numeros/2008/completa/Ceara%20em%20Numeros%202008_completa.pdf>. Access on 13 July 2020.
  » http://www2.ipece.ce.gov.br/publicacoes/ceara_em_numeros/2008/completa/Ceara%20em%20Numeros%202008_completa.pdf
• IPECE (2016) Características Geográficas, recursos naturais e meio ambiente. Ceará em números. Instituto de Pesquisa e Estratégia Econômica do Ceará. Pp. 21-45. Available at <http://www2.ipece.ce.gov.br/publicacoes/ceara_em_numeros/2016/completa/Ceara_em_Numeros_2016.pdf>. Access on 9 July 2020.
  » http://www2.ipece.ce.gov.br/publicacoes/ceara_em_numeros/2016/completa/Ceara_em_Numeros_2016.pdf
• Johansen JR, La Cognata SL & Kociolek JP (1994) Examination of the type material of Denticula rainierenis Sovereign. In: Kociolek JP (ed.) Proceedings of the 11^th Diatom Symposium. Vol. 17. Academy of Sciences, San Francisco. Pp. 211-219.
• Krammer K & Lange-Bertalot H (1997) Bacillariophyceae. In: Ettl H, Gerloff J, Heynig H & Mollenhauer D (eds.) Süsswasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart. Pp. 1-620.
• Krammer K & Lange-Bertalot H (1988) Bacilariophyceae: Bacillariaceae, Ephithemiaceae, Surirellaceae. In: Ettl H, Gerloff J, Heyning H & Mollenhauer D (eds.) Süsswasserflora von Mitteleuropa. Gustav Fischer, Stuttgart. Pp. 1-596.
• Lange-Bertalot H (1993) 85 Neue Taxa und über 100 weitere neu definierte Taxa ergänzend zur Süsswasserflora von Mitteleuropa. Bibliotheca Diatomologica 27: 1-393.
• Lange-Bertalot H, Cavacini P, Tagliaventi N & Alfinito S (2003) Diatoms of Sardinia. Iconographia Diatomologica 12: 1-438.
• Lange-Bertalot H, Hofmann G, Werum M & Cantonati M (2017) Freshwater benthic diatoms of Central Europe: over 800 common species used in ecological assessment. Koeltz Botanical Books, Schmitten-Oberreifenberg. 942p.
• Lange-Bertalot H & Krammer K (1993) Observations on Simonsenia and some small species of Denticula and Nitzschia. Nova Hedwigia 106: 121-131.
• Ludwig TAV & Tremarin PI (2006) Bacillariophyta. In: Bicudo CEM & Menezes M (eds.) Gêneros de algas de águas continentais do Brasil (chave para identificação e descrições). 3ª ed. Rima, São Carlos. 462p.
• Lundholm N, Hasle GR, Fryxell GA & Hargraves PA (2002a) Morphology, phylogeny and taxonomy of species within the Pseudonitzschia americana complex (Bacillariophyceae) with descriptions of two new species, Pseudonitzschia brasiliana, and Pseudo-nitzschialinea. Phycologia 41: 480-497.
• Lundholm N, Daugbjerg N & Moestrup O (2002b) Phylogeny of the Bacillariaceae with emphasis on the genus Pseudonitzschia (Bacillariophyceae) based on partial LSU rDNA. European Journal of Phycology 37: 115-134.
• Maltsev Y, Maltseva S, Kociolek JP, Jahn R & Kulikovskiy M (2021) Biogeography of the cosmopolitan terrestrial diatom Hantzschia amphioxys sensu lato based on molecular and morphological data. Scientific Reports11: 1-19.
• Mann DG (1978) Studies in the Nitzschiaceae (Bacillariophyta). Vols 1 & 2 - XXXIII + 146 plates. PhD Dissertation. University of Bristol, Bristol. 386p.
• Metzeltin D & Lange-Bertalot H (1998) Tropical diatoms of South America I. About 700 predominantly rarely known or new taxa representative of the neotropical flora. In: Lange-Bertalot H (ed.) Iconographia Diatomologica. Annoted diatom micrographs. Vol. 5. Koeltz Scientific Books, Stuttgart. 695p.
• Metzeltin D & Lange-Bertalot H (2007) Tropical Diatoms of South America. In: Lange-Bertalot H (ed.) Iconografia Diatomologica. Vol. 1. Koeltz Scientific Books, Stuttgart. 877p.
• Moreira-Filho H & Valente-Moreira IM (1981) Avaliação taxonômica e ecológica das diatomáceas (Bacillariophyceae) epífitas em algas pluricelulares obtidas nos litorais dos Estados do Paraná, Santa Catarina e São Paulo. Boletim Museu Botânico Municipal de Curitiba 47: 1-17.
• Nascimento FR (2011) Categorização de usos múltiplos de recursos hídricos e problemas ambientais: cenários e desafios. In: Medeiros CN, Gomes DDM, Albuquerque ELS & Cruz MLB (eds.) Os recursos hídricos do Ceará: integração, gestão e potencialidades. Instituto de Pesquisa e Estratégias Econômicas do Ceará (IPECE), Fortaleza. 268p.
• O’Meara E (1873) Tryblionella debilis Arnott in Ireland. Quarterly Journal of Microscopical Science 13: 310.
• Patrick R (1940a) Diatoms of Northeastern Brazil. Part I. Coscinodiscaceae, Fragilariaceae and Eunotiaceae. Proceedings of the Academy of Natural Sciences of Philadelphia 92: 191-226.
• Patrick R (1940b) Some new diatoms from Brazil. Notulae Naturae of the Academy of Natural Sciences of Philadelphia 59: 1-7.
• Potapova M, Veselá J, Smith C, Minerovic A & Aycock L (2022) Diatom new taxon file at the Academy of Natural Sciences (DNTF-ANS), Philadelphia. Available at <http://dh.ansp.org/dntf>. Access on 13 January 2022.
  » http://dh.ansp.org/dntf
• Rimet F, Kermarrec L, Bouchez A, Hoffmann L, Ector L & Medlin L (2011) Molecular phylogeny of the family Bacillariaceae based on 18S rDNA sequences: focus on freshwater Nitzschia of the section Lanceolate. Diatom Research 26: 273-291.
• Round FE, Crawford RM & Mann DG (1990) The diatoms: biology & morphology of the genera. Cambridge University Press, New York. 747p.
• Sá H, Evangelista IB, Costa EC, Silva CIPR, Silva MF & Viana DC (2018) Primeiro levantamento de microalgas no riacho Pequiá do município de Açailândia-Maranhão. Revista Arquivos Científicos (IMMES) 1: 74-79.
• Santiago-Hussein MC & Oliveira PE (2006) Taxonomia de Diatomáceas fósseis do Holoceno da lagoa Olho D’Água (Recife-Pe). Revista Geociências-UNG-Ser 4: 17-34.
• Schmidt A (1874-1959) Atlas der Diatomaceen-Kunde. (continued by Martin Schmidt, Friedrich Fricke, Heinrich Heiden, Otto Muller, Friedrich Hustedt) Reprint 1984. Koeltz Scientific Books, Konigstein. 480 plates.
• Silva WJ, Nogueira IS & Souza MGM (2011) Catálogo de diatomáceas da Região Centro-Oeste brasileira. Iheringia Série Botânica 66: 61-86.
• Simonsen R (1974) The diatom plankton of the Indian Ocean Expedition of R/V “Meteor”, 1964-65. “Meteor” Forschungsergbnisse, Reihe D-Biologie 19: 1-66.
• Smith W (1853) Synopsis of British Diatomaceae. John Van Voorst, London. 89p.
• Souza GS, Koening ML, Leça EE & Coêlho MPCA (2007) Diatomáceas indicadoras de paleoambientes do Quaternário de Dois Irmãos, Recife, PE, Brasil. Acta Botanica Brasilica 21: 521-529.
• Sovereign HE (1963) New and rare diatoms from Oregon and Washington. Proceedings of the California Academy of Sciences (Series 4) 31: 364.
• Taylor JC & Cocquyt C (2016) Diatoms from the Congo and Zambezi Basins: methodologies and identification of the genera. Vol. 16. ABC Taxa and the Belgian Development Cooperation, Belgium. Pp. 1-550.
• Torgan LC, Becker V & Prates HM (1999) Checklist das diatomáceas (Bacillariophyceae) de ambientes de águas continentais e costeiros do estado do Rio Grande do Sul. Iheringia, Série Botânica 52: 89-144.
• Tremarin PI, Freire EG, Bertolli LM & Ludwig TAV (2009) Catálogo das diatomáceas (Ochrophyta-Diatomeae) continentais do estado do Paraná. Iheringia Série Botânica 64: 9-107.
• Vieira RS, Lacerda RS, Oliveira ECC, Nascimento KJN & Dias AS (2013) Biodiversidade de microalgas perifíticas do Rio da Batateira (Sítio Fundão - Crato-CE). Cadernos de Cultura e Ciência 12: 7-15.
• Werum M, Lange-Bertalo H (2004) Diatomeen in Quellen: Unter Hydrogeologischen und Anthropogenen Einflüssen in Mitteleuropa und andere Regionen. Iconographia Diatomologica 13: 480.
• You Q, Kociolek JP & Wang Q (2015) The diatom genus Hantzschia (Bacillariophyta) in Xinjiang province, China. Phytotaxa 197: 1-14.
• Zidarova R, Vijver BV, Quesada A & Haan M (2010) Revision of the genus Hantzschia (Bacillariophyceae) on Livingston Island (South Shetland Islands, Southern Atlantic Ocean). Plant Ecology and Evolution 143: 318-333.

Edited by

Area Editor: Dra. Lana Sylvestre

Publication Dates

• Publication in this collection
  11 Aug 2023
• Date of issue
  2023

History

• Received
  14 Jan 2022
• Accepted
  23 Nov 2022