First record of Tetraspora gelatinosa Link ex Desvaux ( Tetrasporales , Chlorophyceae ) in the state of Goiás , Central-Western Brazil

Tetraspora gelatinosa is rare and has been recorded only in 3 Brazilian states since the 2000s. The flora of the state of Goiás is incipiently known, but there is no record of Tetraspora thus far. We record the occurrence of T. gelatinosa in Goiás and characterize this species’ morphology and ecological preferences. Specimens were found in the Samambaia Reservoir, Goiânia, Goiás. Physical and chemical characteristics of the water were measured. Where T. gelatinosa was found, the water was shallow and characterized as ultraoligotrophic. These conditions agree with those reported for other environments in Brazil.


Introduction
The genus Tetraspora Link ex Desvaux (1818: 17) was originally proposed to include algae with spores arranged four-by-four in a thick substance ("Spores disposés quatre à quatre dans l'épaisseus de la substance").Currently, it is included in Tetrasporaceae and encompasses representatives with green cells within a mucilaginous matrix, forming macroscopic spherical colonies; cells spherical to elliptical, arranged two-by-two or four-by-four, with 2 pseudoflagella extending beyond the mucilage; chloroplasts parietal, cupuliform, single pyrenoid, and sometimes covered by starch grains; stigma absent; contractile vacuole in the cytoplasm; asexual reproduction resulting in the formation of 2 or 4 daughter cells or biflagellate zoospores; and sexual reproduction by isogamy (Bourrely 1972, Ettl and Gartner 1988, Pentecost 2011).
Tetraspora differs from other genera of the family (i.e., Apiocystis Nägeli, Paulschulzia Skuja, Octosporiella Kugrens, Polychaetochloris Pascher, Chaetochloris Pascher & Korshikov, and Chlorangiochaete Korshikov) because the cells are free and more or less uniformly distributed throughout the mucilaginous matrix, which is macroscopic, and presents an irregular outline with irregularly demarcated shapes and edges (Ettl and Gartner 1988).Dispora Printz (Radiococcaceae, Sphaeropleales) is also considered morphologically similar to the genus Tetraspora; however, it differs in terms of the types of reproduction, which occurs exclusively by autospores in Dispora (Komárek and Fott 1983).
Originally  Fungi, and Plants (McNeill et al. 2012), by the exclusion of the other original taxa by Agardh (1824).
Currently, Tetraspora encompasses 18 species (Guiry and Guiry 2017), including T. gelatinosa, the type of the genus.This species is distributed in various freshwater systems across all continents, including polar, temperate, and tropical zones (Richter et al. 2014).In Brazil, T. gelatinosa is known in the states of São Paulo, Paraná, and Rio Grande do Sul (Branco et al. 2005, Krupek et al. 2007, 2008, Peres 2011, Tucci et al. 2015).Herein we provide the first record of T. gelatinosa in the state of Goiás, Central-Western Brazil.

Methods
Benthic samples were taken in a small channel constantly supplied with water from the Samambaia Reservoir in Goiânia, state of Goiás (Fig. 1).This reservoir is formed by damming the Samambaia Stream and supplies water to part of the Northern region of Goiânia.The Samambaia Stream is a tributary of the Meia Ponte river basin, whose main channel runs 491.4 km and drains an area of 12,323 km 2 in 39 municipalities (Veiga et al. 2013).
Samples were collected by scrapping the wall of the channel using a scalpel.The benthic material was placed in 100 mL glass bottles and fixed with Transeau (Bicudo and Menezes 2017) deposited in the Herbarium of the Universidade Federal de Goiás (UFG).The material was analyzed by light microscopy using a Zeiss Axioscop 40 microscope equipped with an Axiocam HRc digital camera (Carl Zeiss Microscopy GmbH, Germany).The metric characteristics were obtained using AxioVision Rel 4.8 image software (Carl Zeiss Microscopy GmbH).Identification was performed using specific literature (e.g., Bourrely 1972, Ettl andGartner 1988).Physical and chemical variables of the water were determined according to the American Public Health Association (APHA 2017).

Discussion
This species is similar to T. lubrica, but differs by the morphology of the mucilaginous matrix (whole and non-fenestrated versus tubular and fenestrated) (Pentecost 2011).Ettl and Gartner (1988) also highlighted differences in the number of starch grains, of which there are only 2 in T. lubrica and numerous in T. gelatinosa; however, we were not able to observe this characteristic.However, some authors (e.g., Pentecost 2011) suggest that these taxa could be conspecific and that the fenestrated and tubular mucilaginous matrix in T. lubrica could be a morphological variability of T. gelatinosa, or more specifically, a growth condition of this species.Indeed, these 2 species can occur in the same environment at the same time, which could support this conspecificity hypothesis (Peres 2011), but more detailed studies should be conducted to confirm this or solve other taxonomic doubts in the group, perhaps by including molecular data, as suggested by Richter et al. (2014).Individuals of T. gelatinosa are normally non-motile in the vegetative phase and, similar to other Tetrasporaceae, present pseudoflagella (Ettl and Gartner 1988).These pseudoflagella differ from flagella because they lack the 2 central microtubules (Entwisle and Skinner 2001).In some cases, the pseudoflagella do not extend beyond the mucilaginous matrix, and therefore, are difficult to observe (Entwisle and Skinner 2001).However, in zoospores and gametes, the pseudoflagella are shed and flagella are produced (Entwisle and Skinner 2001).
Tetraspora gelatinosa has been recorded in Europe (Britain, Netherlands, Romania, Spain, and Turkey), Asia (Bangladesh, India, Iraq, Pakistan, China, Russia, and Turkey), Oceania (Australia and New Zealand) (Guiry and Guiry 2017), and North America (Mexico) (Rodriguez-Flores and Carmona-Jimenez, 2018).In South America, the species has been observed in Argentina (Tell 1985;Daga et al. 2014) and Brazil, specifically in the states of São Paulo, Paraná, and Rio Grande do Sul (Branco et al. 2005, Krupek et al. 2007, 2008, Peres 2011, Tucci et al. 2015).Despite its wide distribution, the environmental condition in which it occurs appears to be specific.
Richter et al. ( 2014) considered T. gelatinosa characteristic of cold habitats and suggested that, in tropical regions, the vegetative cells tend to be smaller compared with temperate areas.Indeed, some cells of specimens found in the Samambaia Reservoir were smaller (< 6 µm) than some obtained from temperate and even tropical zones (Ettl and Gartner 1988, Entwisle and Skinner 2001, Peres 2011, Richter et al. 2014); however, dimensions close to the largest cells representative of this taxon were also observed, independently from the region of occurrence.
The channel of the Samambaia Reservoir, where T. gelationosa was found, is shallow with clean water, which agreed with some of the ecological conditions in which this species has been recorded (Pentecost 2011, Richter et al. 2014).Branco et al. (2005) confirmed that T. gelatinosa develops better in shallow environments.Moreover, longer periods of irradiance also influence the establishment of this species in Brazilian tropical streams (Branco et al. 2005).Thus, it is possible that the species exhibits a positive relationship with light in the water column, which is directly affected by irradiance, water transparency, turbidity, and depth (Margalef 1983, Kalff 2002).
The Samambaia Reservoir presented low nutrient concentrations (Table 1) and is considered ultraoligotrophic according to the levels of phosphorus and orthophosphate (Lamparelli 2004).Similarly, T. gelatinosa has been found in pristine environments, with oligotrophic to mesotrophic conditions and, consequently, low concentration of nutrients (Entwisle and Skinner 2001, Gutowski et al. 2004, Richter et al. 2014).Differently from the population recorded in the most disturbed sites in streams of the Mexican basin, and therefore, tolerant to high DIN concentrations (Rodríguez-Flores and Carmona-Jiménez 2018).This species appears to be sensitive to higher values of orthophosphate, as suggested by Branco et al. (2005).This occurred because the higher abundance of this species was found during rainy periods when concentrations of this nutrient were the most negatively affected.A relationship with nitrite was also verified in the analysis performed by Branco et al. (2005), although this was influenced by only one event that occurred during the sampling period.
Morphological characteristics of representatives of the taxon and ecological conditions of the environment where it was recorded confirm the records of T. gelatinosa.Although it is distributed worldwide, the species is considered rare.It appears to be dependent on pristine conditions, including in Brazil.Thus, occurrence records are important for knowing its ecology and the conservation of the environments where it is established, as the current trend, especially in Brazil, is the deterioration of environments due to extensive agricultural practices and high production of industrial and urban waste (Tundisi 2003).Future studies should focus on the population relationships of this species to verify distribution patterns and possible sites where the species occurs and the risks for its conservation.

Table 1 .
Physical and chemical parameters of water in the Samambaia Reservoir, Goiânia, Goiás, Brazil.