First record of Parvodinium umbonatum ( Stein ) Carty ( Peridiniaceae , Dinophyta ) for northeast Brazil

This paper presents the first record of the freshwater dinoflagellate Parvodinium umbonatum (Stein) Carty (Peridiniaceae, Dinophyta) for northeast Brazil, based on samples collected in 2015 from a tank bromeliads at Serra da Jiboia, Bahia. This species was an important component in the local phytotelm community and categorized as frequent in the bromeliads of the area. A description based on morphometrical features, illustrations (LM and SEM), abiotic conditions of the stored water, and geographic distribution of P. umbonatum in Brazil are provided.

Phytotelmata are small-water habitats formed by vegetal structures and are capable of maintaining diverse associated organisms, including algae (Kitching 2000).Dinoflagellates are a group of algae found in both marine and freshwaters and are considered important components of ecosystem being; next to diatoms, they are the most important aquatic primary producers (Carty 2008;Sophia 1999;Graham et al. 2009;Sahu et al. 2014).
Little is known about the diversity of dinoflagellates in Brazilian continental waters (Gomes et al. 2010), especially in northeast Brazil, where there are just a few records: Araújo et al. (2000) in Rio Grande do Norte; Moschini-Carlos et al. (2008) in Maranhão; Lira et al. (2009) in Pernambuco; Severiano et al. (2012) in Bahia; Oliveira et al. (2011) in semi-arid regions of Alagoas, Bahia, Pernambuco and Sergipe;and recently, Aragão-Tavares et al. (2015) at Itaparica and Xingó Reservoirs, São Francisco River.In total, 13 taxa, but only five are to specific level, were cited.However, except Oliveira et al. (2011), none of these works has detailed information on the species, such as descriptions, measurements or figures, to confirm their identifications or to compare them with taxonomic studies.
The genus Parvodinium Carty (2008) was proposed to accommodate representatives of Peridinium Ehrenberg presenting an apical pore, two apical intercalary plates, and six cingular plates.Parvodinium consists of 10 species (Guiry & Guiry 2016), and the occurrence of four species was recorded in Brazil: Parvodinium africanum (Lemmermann) Carty; P. inconspicuum (Lemmermann) Carty; P. pusillum (Penard) Carty; and P. umbonatum (Stein) Carty.From these, only P. pusillum was cited for the Northeast Region of Brazil (Moschini-Carlos et al. 2008;Menezes et al. 2015).Parvodinium umbonatum is the only known dinoflagellate inhabiting tank bromeliads in Brazil (Sophia 1999); however, its role, as well as the conditions in the phytotelm habitats, are unknown.
This study presents the first record of Parvodinium umbonatum from the northeast Brazil.This record is a result of a floristic survey of the algae and cyanobacteria from bromeliad phytotelmata in Serra da Jiboia, Bahia state.
The study area is located at Monte da Pioneira, northern Serra da Jiboia (12°51ʹS, 039°28ʹ W), 850 m altitude, in the municipality of Santa Teresinha, Bahia, Brazil.This area is characterized by a great population of the bromeliads Alcantarea nahoumii (Leme) J.R.Grant, which inhabits the tops of rock outcrops (Figure 1).
The samples were taken in January, July, September and November 2015.In each of these months, 20 tank bromeliads were sampled totalizing 80 sampling units.
The material was collected using a 50-mL syringe coupled to a polyethylene hose.Abiotic parameters of the water, such as temperature, pH, electric conductivity (EC), and total dissolved solids (TDS), were obtained during sampling with a multiparameter probe (Hanna HI98130).Dissolved oxygen (DO) was measured with a portable digital dissolved oxygen Meter (Instrutherm MO-910).
The species was identified using specialized literature (Carty 2008;Lewis & Dodge 2011;Carty 2014), and plate designation was based on Kofoid (1909).Samples of P. umbonatum, fixed in Transeau's solution, were observed using an Olympus light microscope (LM; model BX-43), and the digital images were taken with a 5.0-MP QImaging camera using the software Image-Pro Premier 9.1.4.The fine external morphology was observed under scanning electron microscopy (SEM).For SEM preparations, the Transeau's-fixed cells were adhered to a glass coverslip with poly-L-lysine (Sigma, 1:10 in distilled water) to ensure better adhesion of the dinoflagellates.Coverslips with material adhered were dehydrated in acetone series (30, 50, 70, 85, 95, 100, 100%, 10 min each).Finally, the material was dried to critical-point in a Leica EM CPD030 critical point dryer; the stubs were mounted and coated with gold and observed with a JEOL 6390 LV SEM (JEOL Ltd., Tokyo, Japan).In the specimens analyzed, we observed some morphological variations such as epitheca slightly conical to (more commonly) rounded (Figure 2).Our material is morphologically like those described by Carty (2014), who also described cells with rounded epitheca.This polymorphism can be explained by changes in water temperature (Popovský & Pfiester 1990).Despite this phenotypic plasticity, we consider it more appropriate to identify our material as P. umbonatum.
There are two species morphologically related to Parvodinium umbonatum recorded from Brazil: P. africanum and P. inconspicuum (Menezes et al. 2015).The former differs from P. umbonatum by having thecal plates with vertical surface striations whereas P. inconspicuum has cells are approximately pentagonal, the cingulum is more equatorial, and the apical pore is prominent (Carty 2008;Tardio et al. 2009;Lewis & Dodge 2011;Carty 2014).
The Serra da Jiboia is considered one of the 182 priority areas for conservation of the Brazilian Atlantic Forest biodiversity and one of the 99 areas of extreme biological importance (MMA 2002).Thus, it is necessary to preserve the bromeliads that inhabit the Monte da Pioneira, especially Alcantarea nahoumii, a vulnerable species (Martinelli & Moraes 2013), that harbors also other interesting algae such as desmids (Ramos et al. 2011).Finally, we recommend expanding taxonomic studies of freshwater dinoflagellates in Brazil, especially in the Northeast Region, where almost all records are only restricted to checklists.
Frequency of occurrence (FO) of Parvodinium umbonatum in the bromeliads was categorized according to Matteucci & Colma (1982).Four samples (one of each period) were deposited in the Herbarium of the State University of Feira de Santana (HUEFS).

Parvodinium umbonatum (Stein) Carty
This species has cells ovoid to elliptical, 19.5-25 µm long, 15.5-18 µm wide, with the epitheca broadly rounded or slightly conical and longer than hypotheca.There is an apical pore covered by a cover plate and surrounded by a pore plate, and a canal plate runs ventrally to the apex of the 1ʹ plate.Plate formula: Po, x, 4ʹ, 2a, 7ʺ, C6, S5, 5ʹʹʹ, 2ʹʹʹʹ (Figure 2).The antapical plates and six cingular plates are not neatly aligned with pre-or post-cingular plates.The cell wall is composed of thecal plates, with slightly reticulate ornamentation, and have large pores towards plate edges.The chloroplasts pale brown; the eyespot was not observed.
In the Serra da Jiboia, Parvodinium umbonatum was commonly found in the bromeliads exposed to bright sunlight.This species had the highest frequency of occurrence of all species of algae (unpublished data) inhabiting these tank bromeliads (FO = 78.7%,frequent).Thus, P. umbonatum is probably an important primary producer in the local phytotelm community.
Although freshwater dinoflagellates are tolerant of wide range of environment conditions, they are commonly found in well-oxygenated water bodies with oligotrophic conditions (Rosen 1981;Pollingher 1988;Oda & Bicudo 2006;Gomes et al. 2010).Although the nutrient concentrations were not measured in the present study, Ngai & Srivastava (2006) and Lopez et al. (2009) demonstrated that bromeliad tanks might have oligotrophic conditions.
The abiotic water conditions, such as acidic pH, low conductivity, and high level of dissolved oxygen probably are favorable for the occurrence of P. umbonatum in the bromeliad tanks.This species also was recorded in a phytotelm habitat in bromeliads of the Rio de Janeiro state (as Peridinium umbonatum; Sophia 1999), but neither detailed information on this species nor abiotic data of the bromeliad tanks were provided.

Figure 1 .
Figure 1. A. Map of study area and Brazilian states where Parvodinium umbonatum have been previously recorded (grey areas).Red dot represents the local of the new record for the northeast Brazil (yellow area).Detail of the Serra da Jiboia (green area), highlighting the Monte da Pioneira, municipality of Santa Teresinha (red dot) (adapted from Ramos et al. 2011).B. Alcantarea nahoumii.C. Habitat of Alcantarea nahoumii.