1 Introduction

Euastrum Ehrenberg ex Ralfs is considered one of the most representative genera of Desmidiaceae, comprising about 649 taxonomically accepted species (Guiry and Guiry 2021), and so like other groups of the family, has a wide geographic distribution, mainly in tropical and subtropical regions (Coesel 1996; Moresco et al. 2009), occurring in oligo-mesotrophic aquatic environments, with low conductivity and slightly acidic (Coesel and Meesters 2007; Stastny 2010). The genus is polyphyletic (Gontcharov and Melkonian 2005; Hall et al. 2008) and polymorphic, characterized by having apical lobes with a U- or V-shaped medial incision (Brook 1981; Anissimova 2016; Bicudo and Menezes 2017).

In Brazil, there are reported 64 species and 53 non-typical Euastrum varieties (Araújo et al. 2015; Menezes et al. 2015; Flora do Brasil 2020); of these, 37 species and 41 non-typical varieties were listed for the state of Bahia. Part of these taxa appears in the study performed by Förster (1964), who analyzed material associated with Utricularia L. (Lentibulariaceae) from the Chapada Diamantina region. Oliveira et al. (2011, 2017) also studied periphyton from several macrophytes in lakes and rivers on the north coast of Bahia, and Costa et al. (2018, 2020) carried out a study on material associated with macrophytes from the Pantanal dos Marimbus, Chapada Diamantina.

In lotic and lentic environments, aquatic macrophytes function as natural substrates for colonization of the periphytic community (Ferreiro et al. 2014). These plants have great ecological importance, influencing nutrient availability for the periphyton (Felisberto and Murakami 2013), allelopathic substances production, and shading promoted light reduction (Erhard and Gross 2006; Meerhoff et al. 2007). The macrophytes with certain characteristics tend to favor the occurrence of desmids, for example, macrophyte that have cut leaves usually support a more diverse desmids community (Laugaste and Reunanen 2005; Mutinová et al. 2016). Among the periphytic algae community, desmids emerge as one of the predominant groups (Díaz-Olarte et al. 2007; Díaz-Olarte and Duque 2009; Menezes et al. 2013), having genera with high specific diversity such as Cosmarium Corda ex Ralfs and Euastrum.

The characteristics physical (architecture, composition, orientation, roughness) and chemical (allelopathy and excretion of nutrients) of macrophytes affect the periphyton structure (Gross 2003; Zhang et al. 2013), being as interactions between these plants and the desmids community potentially higher in floodplains (Domozych and Domozych 2007; Rosen et al. 2019). Therefore, given the necessity of taxonomic studies on desmids from the Caatinga, we investigated the composition and morphological characteristics of Euastrum taxa associated with three species of aquatic macrophytes (Utricularia foliosa Linnaeus, Cabomba caroliniana A. Gray, and Eichhornia azurea Kunth) in a floodplain area (Pantanal dos Marimbus) in northeastern Brazil. Our main question was whether the: (a) does taxa composition of Euastrum change between macrophytes studied? (b) What are the main morphological characteristics of the taxa studied in the Pantanal dos Marimbus? (c) Do environmental variables influence of Euastrum variability?

2 Material and methods

Study area

– The study was carried out in Marimbus do Baiano, southern region of the Pantanal dos Marimbus, located in the municipality of Andaraí (Fig. 1a), in Chapada Diamantina, Bahia, Brazil. The Pantanal dos Marimbus is formed by the confluence of the Santo Antônio, Utinga, and São José rivers, characterized by flooded areas where several species of aquatic macrophytes occur (Utricularia foliosa, Cabomba caroliniana, Eichhornia azurea, Nymphaea amazonum Mart & Zucc and Salvinia auriculata Aublet) (França et al. 2010; Ramos et al. 2014; Lima et al. 2018).

Fig. 1
figure 1

Map of Bahia State showing localization of Andaraí municipality and Pantanal dos Marimbus (a) and Marimbus do Baiano (b) and sampling stations (white circles)

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Sampling

– Periphytic samples were collected bimonthly (May, July, September and November/2017; January and March/2018), in 10 sampling stations along the floodplain lake (Fig. 1b). Based on life forms, three species of macrophytes were selected: Cabomba caroliniana, macrophyte rooted submerged, characterized by light branching and highly cut leaves; Eichhornia azurea, macrophyte emerged floater characterized by branched roots and entire leaves; and Utricularia foliosa, macrophyte free submerged, characterized by dense branching and numerous smaller leaves.

We obtained a total of 180 sampling units of periphytic material from the squeeze of macrophyte species whole for qualitative analysis. All samples were preserved in the Transeau solution (Bicudo and Menezes 2017).

Abiotic water and meteorological variables

– In each sampling station, we also measured the abiotic variables of the water such as temperature (°C), pH, conductivity (µS cm−1), and total dissolved solids using the portable Hanna HI98130 probe, dissolved oxygen (mg L−1) using the portable Instrutherm probe (MO-910), and water transparency by secchi disk.

Historical precipitation data (30 years) for the collection period in the municipality of Andaraí were obtained from the National Institute of Meteorology—INMET (2018).

Microscopic analysis

– We analyzed the Euastrum specimens in an Olympus BX45 microscope and photographed using a MicroPublisher-QImaging digital camera and Image-Pro Premier 9.1.4 software. The methodology proposed by Mann et al. (2007) and Pickett-Heaps (1974) was adapted, separating aliquots of the material, which were transferred to Eppendorf and added sodium hypochlorite (NaClO) at 2% or sodium hydroxide (NaOH) at 20% (1:1, v/v) for 24 h to show the ornamentation of the cell wall of taxa under light microscopy. We incorporated all sampling units into the liquid collection in the herbarium of the Universidade Estadual de Feira de Santana (HUEFS).

Taxonomic identification and analyzed attributes

– The specimens were identified based on morphological characteristics, such as cell and semi-cell shape; cell size identified by its maximum length, maximum width, maximum polar lobe width, and isthmus width; number and shape of apical and basal lobes; the shape of the lateral margins of the semi-cell; type of midline apical incisions; type of cell wall ornamentation. All identifications were performed based on specialized literature (Krieger 1937; Förster 1964, 1969; Prescott et al. 1977; Růžička 1977, 1981; Croasdale and Flint 1986; Coesel and Meesters 2007). Species richness was determined by the number of taxa in each sample.

The taxa occurrence frequency was calculated according to the formula: F = n·100/N, where: n = number of samples in which a species was recorded, and N = total samples analyzed. The frequency categories were determined according to Matteucci and Colma (1982): > 70%—very frequent (MF); ≤ 70% to > 40%—frequent (F); ≤ 40% to > 10%—uncommon (I); ≤ 10%—rare (R).

Data analysis

– We applied the Kruskal–Wallis test to detect significant differences (α = 0.05) in the abiotic variables between the collection months, after checking normality (Shapiro–Wilk test) and homoscedasticity (Levene test) (Hammer et al. 2001).

Non-metric multidimensional scaling (NMDS) was applied to the data matrix of Euastrum composed of five categories (incision deep, wall with granules and spines, wall only with scrobicules, size < 59 µm, size > 60 µm), filled with 1 (presence of category) and 0 (absence of category). This analysis aimed to detect differences between the morphological characteristics and the taxa size, using the Jaccard similarity index (Legendre and Legendre 1998), performed in e R software vegan package (R Development Core Team 2009).

We constructed the Venn diagram to demonstrate Euastrum taxa distribution richness among the three macrophyte species studied, using software available on The Bioinformatics and Evolutionary Genomics group website at the University of Ghent, Belgium (http://bioinformatics.psb.ugent.be/webtools/Venn/).

3 Results

Meteorological conditions and abiotic water variables

– The average precipitation of the sampled period presented values ​​below the historical average of the last 30 years (Fig. 2). The months of July and September/17 had a low volume of precipitation (around 45 mm), characteristic of the dry season, while November/17 and March/18 were typical of the rainy season, with 161 and 230 mm, respectively.

Fig. 2
figure 2

Historical average and total accumulated precipitation (collection period) in the municipality of Andaraí, Bahia. Arrows indicate sampling months

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All abiotic water variables showed significant differences between the sampled months (Fig. 3). Water temperature recorded the lowest mean value in July/17 (26.6 °C) and highest in January and March/18 (30.3 and 31.0 °C, respectively). We verified the highest dissolved oxygen concentration in March/18 (14.8 mg L−1), followed by July and September/17 (6.2 and 8.7 mg L−1, respectively). During the collection period, water conditions were slightly alkaline, except for May/17 and March/18, where they were slightly acidic (mean 6.7). The conductivity values, as well as the total dissolved solids, were considerably different throughout the study period and with a wide range of variation, especially in July and September/17 and January/18; in both variables, the lowest means (48 µS cm−1, 0.02 ppt) were recorded in the month with the highest rainfall (March/18). Regarding water transparency, we registered the highest average in January/18 (1.34 m) and the lowest in July (0.47 m) and September/17 (0.50 m).

Fig. 3
figure 3

Temporal variation of abiotic variables in the Pantanal dos Marimbus do Baiano, municipality of Andaraí, Bahia. F: Kruskal–Wallis test result

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Taxonomic composition and morphology

– We identified a total of 32 Euastrum taxa from the periphyton of the macrophytes studied (Table 1). In all months sampled, Utricularia foliosa was the macrophyte with the highest taxonomic richness (30 taxa), followed by C. caroliniana (24 taxa) and E. azurea (23 taxa).

Table 1 Euastrum taxa from the Pantanal dos Marimbus, Bahia
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Comparing the occurrence of the taxa over the months, it was evident that U. foliosa presented the highest richness values, with emphasis on May/17 (26 taxa) and November/17 (22 taxa). On the other hand, we registered the lower values ​​in March/18 for all studied macrophytes: U. folisosa (14 taxa), C. caroliniana (11 taxa), and E. azurea (9 taxa) (Fig. 4). Considering the months of lowest and highest rainfall, we noticed that ten taxa were exclusive to the driest months: Euastrum abruptum var. lagoense (Nordstedt) Willi Krieger, E. angolense var. brasiliense Willi Krieger, E. attenuatum var. brasiliense Grönblad, E. brasiliense Borge, E. ciastonii Raciborski, E. denticulatum var. rectangulare West and G.S. West, E. evolutum var. monticulosum (W.R. Taylor) Willi Krieger, E. groenbladii A.M. Scott and H. Croasdale, E. obesum Joshua, and E. westenii F.M. Costa, I.B. Oliveira and C.W.N. Moura. No taxon was registered exclusively in the rainy months (Table 2).

Fig. 4
figure 4

Number of Euastrum taxa recorded in the periphyton of three species of macrophytes collected bimonthly over a year, in the Pantanal dos Marimbus do Baiano, municipality of Andaraí, Bahia

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Table 2 Mean and standard deviation of the abiotic water variables in the Pantanal dos Marimbus in which Euastrum taxa occurred and frequency of occurrence for each species of macrophyte and occurrence in the months sampled
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Five taxa (Euastrum abruptum Nordstedt, E. abruptum var. chapadae F.M. Costa, G.J.P. Ramos and C.W.N. Moura, E. elegans var. prescottii (Förster) F.M. Costa and C.W.N. Moura, E. evolutum var. integrius West and G.S. West, and E. ornatiscrobiculatum F.M. Costa, I.B. Oliveira and C.W.N. Moura) stood out for having the highest frequency of occurrence and for being present in the three studied macrophytes (Table 2). Euastrum ansatum Ehrenberg ex Ralfs and E. praemorsum var. foersteri F.M. Costa, C.E.M. Bicudo and C.W.N. Moura were frequent in U. foliosa and E. azurea. However, we observed that most taxa studied were classified in the rare category (18), followed by the uncommon (6). Most taxa occurred in well-oxygenated waters, slightly alkaline and with an average conductivity of 80 or 90 µS cm−1. However, some were recorded in slightly acidic waters (E. abruptum var. lagoense, E. obesum, and E. westenii).

Considering all registered taxa, 19 of them occurred in the three species of macrophytes (Fig. 5, Table 2). Regarding the macrophyte-exclusive taxa, we detected only five in Utricularia foliosa (E. abruptum var. lagoense, E. angolense var. brasiliense, E. brasiliense, E. obesum, and E. westenii). On the other hand, E. ciastonii and E. attenuatum var. brasiliense Grönblad were exclusive to Cabomba caroliniana and Eichhornia azurea, respectively.

Fig. 5
figure 5

Venn diagram showing the number of common and exclusive Euastrum taxa in the three species of macrophytes collected in the Pantanal dos Marimbus (Baiano), municipality of Andaraí, Bahia

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As for morphology, the NMDS revealed the formation of two clusters that brought together most of the taxa (Fig. 6). Group I, with 19 taxa, included those smaller than 59 μm in length and with a cell wall ornamented mainly by granules and spines, and a deep apical incision; Euastrum abruptum (Fig. 7a), E. abruptum var. chapadae (Fig. 7b), E. abruptum var. lagoense (Fig. 7c), E. bidentatum var. scottii (Fig. 7h), E. ciastonii (Fig. 7j), E. denticulatum var. rectangulare (Fig. 7k), E. elegans var. prescottii (Fig. 7m), E. evolutum (Fig. 7n), E. evolutum var. integrius (Fig. 7o), E. fissum var. nordestinum (Fig. 8b), E. gemmatum (Fig. 8d), E. informe var. oculatum (Fig. 8f), E. marimbusense (Fig. 8h), E. ornatiscrobiculatum (Fig. 8j), E. praemorsum var. forsteri (Fig. 8m), E. sibiricum (Fig. 9a), E. subornatum var. brasiliense (Fig. 9c), E. westenii (Fig. 9d). Group II gathered five taxa lengths greater than 60 μm and cell wall ornamented only by scrobicules; E. ansatum (Fig. 7e), E. ansatum var. concavum (Fig. 7f), E. brasiliense (Fig. 7i), E. didelta var. quadriceps (Fig. 7l), E. subintegrum var. brasiliense (Fig. 9b).

Fig. 6
figure 6

Nonmetric multidimensional scaling (NMDS) ordination of Euastrum taxa based on their morphological characteristics. Abbreviations: S size, ID incision deep, WGS wall with granules and spines, WOS wall only with scrobicles. Numbers represent the taxa: (1) Euastrum abruptum, (2) E. abruptum var. chapadae, (3) E. abruptum var. lagoense, (4) E. angolense var. brasiliense, (5) E. ansatum, (6) E. ansatum var. concavum, (7) E. attenuatum var. brasiliense, (8) E. bidentatum var. scottii, (9) E. brasiliense, (10) E. ciastonii, (11) E. denticulatum var. rectangulare, (12) E. didelta var. quadriceps, (13) E. elegans var. prescottii, (14) E. evolutum, (15) E. evolutum var. integrius, (16) E. evolutum var. monticulosum, (17) E. fissum var. nordestinum, (18) E. gayanum var. angulatum, (19) E. gemmatum, (20) E. groenbladii, (21) E. informe var. oculatum, (22) E. luetkemuellerii var. carniolicum, (23) E. marimbusense, (24) E. obesum, (25) E. ornatiscrobiculatum, (26) E. pectinatum var. pinheirense, (27) E. platycerum var. groenbladii, (28) E. praemorsum var. forsteri, (29) E. sibiricum, (30) E. subintegrum var. brasiliense, (31) E. subornatum var. brasiliense, (32) E. westenii

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Fig. 7
figure 7

Euastrum taxa. a E. abruptum; b E. abruptum var. chapadae; c E. abruptum var. lagoense; d E. angolense var. brasiliense; e E. ansatum; f E. ansatum var. concavum; g E. attenuatum var. brasiliense; h E. bidentatum var. scottii; i E. brasiliense; j E. ciastonii; k E. denticulatum var. rectangulare; l E. didelta var. quadriceps; m E. elegans var. prescottii; n E. evolutum; o E. evolutum var. integrius. Scale Bars:10 μm

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Fig. 8
figure 8

Euastrum taxa. a E. evolutum var. monticulosum; b E. fissum var. nordestinum; c E. gayanum var. angulatum; d E. gemmatum; e E. groenbladii; f E. informe var. oculatum; g E. luetkemuellerii var. carniolicum; h E. marimbusense; i E. obesum; j E. ornatiscrobiculatum; k E. pectinatum var. pinheirense; l E. platycerum var. groenbladii; m E. praemorsum var. forsteri. Scale Bars: 10 μm

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Fig. 9
figure 9

Euastrum taxa. a E. sibiricum; b E. subintegrum var. brasiliense; c E. subornatum var. brasiliense; d E. westenii. Scale Bars:10 μm

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Seven taxa were not included in the groups above, possibly because they have distinct morphological combinations, such as length greater than 60 μm and wall ornamented by granules and spines; E. evolutum var. monticulosum (Fig. 8a) and E. platycerum var. groenbladii (Fig. 8l). And shorter than 59 μm in length with a smooth cell wall; E. angolense var. brasiliense (Fig. 7d) and E. attenuatum var. brasiliense (Fig. 7g), or ornamented by scrobicules; E. groenbladii (Fig. 8e), E. luetkemuellerii var. carniolicum (Fig. 8g) and E. pectinatum var. pinheirense (Fig. 8k).

4 Discussion

Periphyton analysis of macrophytes with different morphological and ecological characteristics revealed an interesting diversity of Euastrum taxa associated with natural substrates in the Marimbus do Baiano. Our data show that the taxonomic composition was more outstanding in the periphyton of Utiricularia foliosa when compared to that of Cabomba caroliniana and Eicchornia azurea. Recently, Santos et al. (2022) evaluated the changes in the desmid community on three macrophytes in the Marimbus do Baiano. The authors measured fractal dimension (df) of Nymphaea amazonum Mart & Zucc (df = 1.59), C. caroliniana (df = 1.65) and U. foliosa (df = 1.73). The macrophyte with high structural complexity, U. foliosa, presented the highest richness, density and diversity of desmids. In contrast, rooted macrophyte with low structural complexity, N. amazonum, registered the lowest values for these attributes. Other studies also indicate the greater richness of desmids on U. foliosa than in other macrophytes (Pellegrini and Ferragut 2012; Santos et al. 2013; Souza et al. 2015; Ramos et al. 2021). Our results can probably be attributed to the structural complexity of the plants, especially the branching of leaves, as the bigger the branch, the greater the periphytic material retaining capacity (Rovira et al. 2016; Fernandes et al. 2016; Casartelli and Ferragut 2017).

The macrophyte architecture can be a strong driver of periphytic algal structure. But our results showed that the seasonality too could have influenced the variability of Euastrum. Several registered taxa occurred only in the months with less rainfall, while the lowest richness was verified in the wettest month (March). Studies suggest that the periphytic biomass accumulation can be strongly influenced by seasonality, with the highest rate during the dry season since the water volume increase can cause the periphyton detachment from the substrates (Felisberto and Rodrigues 2005, 2010; Casartelli et al. 2016).

The analysis of abiotic factors showed that most taxa occurred in well-oxygenated, slightly alkaline, and moderately conductive waters. However, the highest richness of Euastrum was reported in May, when water was with slightly low pH. As desmids are widely reported in environments under acidic conditions (Brook 1981; Coesel 2000; Coesel and Meesters 2007), possibly such factor could be contributed to high richness in that month. Nevertheless, various studies of tropical environments have reported desmids in alkaline waters (Araújo and Bicudo 2006; Souza et al. 2015; Casartelli et al. 2016; Bicudo and Menezes 2017; Santos et al. 2022). The water transparency was somewhat low due to the high concentration of humic substances, especially in the driest months giving the brown aspect to the water. This color is typical of the most aquatic ecosystems from the Chapada Diamantina region, including the Santo Antônio River, which is considered the main river that supplies the Pantanal dos Marimbus (Ramos et al. 2021).

The studied area presents a rich diversity, with endemism of E. abruptum var. chapadae, E. fissum var. nordestinum, E. marimbusense, E. ornatiscrobiculatum, E. praemorsum var. foersteri, and E. westenii, the former variety being classified as very frequent in Marimbus do Baiano (Costa et al. 2018, 2020). Among the taxa considered uncommon or rare, E. ansatum var. concavum, E. groenbladii, and E. sibiricum had their geographic distribution expanded to the northeast region of Brazil (Costa et al. 2020). The other identified taxa, except for E. angolense var. brasiliense, had already been referred to other areas of Bahia (Bicudo and Martins 1989; Oliveira et al. 2011; Ramos et al. 2011; Oliveira et al. 2017; Ramos et al. 2018).

The traditional taxonomy, based entirely on morphological characteristics, has been deconstructed by molecular studies revealing the non-monophyly of many desmid genera (Kouwets 2008; Skaloud et al. 2012). According to Gontcharov and Melkonian (2008, 2011), Desmidiaceae consists of at least 22 independent phylogenetic lineages. However, molecular data are still insufficient for several traditional genera with distinct morphology (Hall et al. 2008).

For the Euastrum genus, molecular studies conducted by Gontcharov and Melkonian (2008, 2011) revealed two distinct strains reflecting the morphology of the taxa: strain 1, comprising large taxa (> 50–60 μm long) with porous cell surface, large bulges facials, and scrobicules; and lineage 2 (smaller than < 50 µm in length), with a varied ornate wall, and the apical lobe with a less pronounced incision, often V-shaped.

Assessing the morphology of the taxa identified in Marimbus do Baiano, we observed that most are shorter than 59 μm and have a cell wall with more than one type of ornamentation. Those larger than 60 µm are ornamented by scrobicules. Cell size is probably related to competition for space and ornamentation to the adhesion process in the periphyton, as an adaptive strategy, thus making them less susceptible to predation (Coesel 2003; Černá and Neustupa 2009; Bestová et al. 2018).

Thus, we expanded knowledge about Euastrum taxa associated with macrophytes in shallow tropical lake of Bahia State, especially in floodplains, where studies are scarce and emphasized the need to promote conservation actions in the Pantanal dos Marimbus. The results presented highlight the importance of aquatic macrophytes for periphytic communities and as repositories of new species. We agree with Ramos et al. (2021) as to expanding the limits of the APA Marimbus-Iraquara to encompass the Marimbus do Baiano, aiming to protect the local biodiversity regarding the pressures caused by touristic activities exploitation.