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Unraveling algae and cyanobacteria biodiversity in bromeliad phytotelmata in different vegetation formations in Bahia State, Northeastern Brazil

ABSTRACT

Knowledge of algal and cyanobacterial diversity of phytotelmata remains poorly-known, especially for bromeliads from different vegetation formations. We investigated the microalgae communities of four species of tank bromeliads from different vegetation formations in Bahia State, Northeast Brazil, highlighting the composition, richness and diversity of taxa. Sampling of water stored in bromeliads was carried out quarterly between 2014 and 2016, and abiotic variables and morphometric attributes of bromeliads were measured. A total of 89 taxa of algae and cyanobacteria were recorded for the four bromeliad species studied. The microalgae communities of the phytotelmata varied among vegetation formations, with one tank bromeliad, Alcantarea nahoumii, with more complex architecture (higher number of leaves and thus more cavities), being distinguished by its high species richness (73 taxa). The bromeliads exhibited little similarity in species composition, with only one species (Phacus polytrophos) occurring in all four species. Throughout the entire sampling period, classes with higher species richness, especially due to A. nahoumii, were Zygnematophyceae, Cyanophyceae and Chlorophyceae, which accounted for about 80 % of all species inventoried. Our results contribute to the knowledge of microalga communities of bromeliad phytotelmata in Brazil with regard to species richness and composition, as well as significant environmental characteristics.

Keywords:
diversity; ecology; microalgae; microhabitat; phytotelm; richness; tank bromeliads

Introduction

The term phytotelm (φυτόν, phyton = plant; τέλμα, telm = pool) refers to the small amounts of water that accumulate in plant structures, such as leaves, flowers, or tree trunk and maintain an associated biota (Varga 1928Varga L. 1928. Ein interessanter Biotop der Biocönose von Wasserorganismen. Biologisches Zentralblatt 48: 143-162.; Maguire 1971Maguire B. 1971. Phytotelmata biota and community structure determination in plant-held waters. Annual Review of Ecology and Systematics 2: 439-464.). Phytotelmata occur in almost all regions of the world, although they are most common and most diversified in the tropical region, mainly due to the high rainfall there and the large numbers of plants capable of accumulating water (Fish 1983Fish D. 1983. Phytotelmata: flora and fauna. In: Frank JH, Lounibos LP. (eds.) Phytotelmata: terrestrial plants as host for aquatic insect communities. New Jersey, Plexus. p. 1-293.).

Little is currently known about the diversity, distribution patterns, and compositions of phytotelmata microalgae communities. Among the few published studies are those of Gebühr et al. (2006Gebühr C, Pohlon E, Schmidt AR, Küsel K. 2006. Development of microalgae communities in the phytotelmata of allochthonous populations of Sarracenia purpurea (Sarraceniaceae). Plant Biology 8: 849-860.) with allochthonous populations of Sarracenia purpurea (Sarraceniaceae) in Germany, and Hernández-Rodríguez et al. (2014Hernández-Rodríguez B, Estrada-Vargas L, Novelo E. 2014. Las microalgas de Tillandsia multicaulis Steud. (Bromeliaceae) de la Reserva Ecológica “La Martinica”, Veracruz. TIP Revista Especializada en Ciencias Químico-Biológicas 17: 117-125. ) with Tillandsia multicaulis (Bromeliaceae) in Mexico. Studies of phytotelmata algae began in Brazil in the 1970s, but have only recently become more frequent, especially in Bahia State, where several taxa have been recorded for the first time for that country, including a number of species new to science (Ramos et al. 2017aRamos GJP, Bicudo CEM, Moura CWN. 2017a. Cosmarium bahianum, sp. nov. (Desmidiaceae), a new desmid species from a phytotelm habitat in the Brazilian restinga. Phytotaxa 291: 66-72. ; bRamos GJP, Bicudo CEM, Moura CWN. 2017b. Taxonomic notes on Spirotaenia (Mesotaeniaceae, Zygnematophyceae) from a Brazilian phytotelm habitat: new species and new records. Phytotaxa 309: 265-270.; cRamos GJP, Bicudo CEM, Moura CWN. 2017c. Algae in phytotelmata from Caatinga: first record of the genus Rhopalosolen Fott (Chlorophyta) for Brazil. Check List 13: 403-410.; dRamos GJP, Alves-da-Silva SM, Bicudo CEM, Moura CWN. 2017d. Euglenophyceae from bromeliad phytotelmata: new records for Bahia state and Brazil. Check List 13: 447-454. ; 2018aRamos GJP, Bicudo CEM, Moura CWN. 2018a. Some new, rare and interesting desmids from bromeliad phytotelmata in Brazil. Phytotaxa 346: 59-77.; bRamos GJP, Bicudo CEM, Moura CWN. 2018b. Diversity of green algae (Chlorophyta) from bromeliad phytotelmata in areas of rocky outcrops and “restinga”, Bahia State, Brazil. Rodriguésia (in press).).

Most phytotelmata algal studies have taken floristic approaches (morphospecies), usually addressing specific groups (Lyra 1971Lyra LT. 1971. Algumas diatomáceas encontradas em Bromeliáceas, Brasil. Memórias do Instituto Oswaldo Cruz 69: 129-139.; Sophia 1999Sophia MG. 1999. Desmídias de ambientes fitotélmicos bromelícolas. Revista Brasileira de Biologia 59: 141-150.; Ramos et al. 2011Ramos GJP, Oliveira IB, Moura CWN. 2011. Desmídias de ambiente fitotelmata bromelícola da Serra da Jiboia, Bahia, Brasil. Revista Brasileira de Biociências 9: 103-113.), or ecological approaches (Brouard et al. 2011Brouard O, Jeune A-H, Leroy C, et al. 2011. Are algae relevant to the detritus-based food web in tank-bromeliads? PLOS ONE 6: e20129. doi: 10.1371/journal.pone.0020129
https://doi.org/10.1371/journal.pone.002...
; Carrias et al. 2014Carrias JF, Céréghino R, Brouard O, et al. 2014. Two coexisting tank bromeliads host distinct algal communities on a tropical inselberg. Plant Biology 16: 997-1004. ), although they have often been published without reliable taxonomic support at the species level. Studies comparing microalgae communities from bromeliad phytotelmata found in different vegetation formations, however, have not yet been undertaken.

The principal environmental variables that regulate which algal groups will dominate in the bromeliad tanks are: light intensity (Laessle 1961Laessle AM. 1961. A micro-lirnnological study of Jamaican Bromeliads. Ecology 42: 499-517.; Sophia et al. 2004Sophia MG, Carmo BP, Huszar VL. 2004. Desmids of phytotelm terrestrial bromeliads from the National Park of “Restinga de Jurubatiba”, Southeast Brasil. Algological Studies 114: 99-119.; Brouard et al. 2011Brouard O, Jeune A-H, Leroy C, et al. 2011. Are algae relevant to the detritus-based food web in tank-bromeliads? PLOS ONE 6: e20129. doi: 10.1371/journal.pone.0020129
https://doi.org/10.1371/journal.pone.002...
), plant size (Marino et al. 2011Marino NAC, Guariento RB, Dib V, Azevedo FD, Farjalla VF. 2011. Habitat size determine algae biomass in tank-bromeliads. Hydrobiologia 678: 191-199.) and plant architecture (Carrias et al. 2014Carrias JF, Céréghino R, Brouard O, et al. 2014. Two coexisting tank bromeliads host distinct algal communities on a tropical inselberg. Plant Biology 16: 997-1004. ), rainfall (Pires et al. 2017Pires APF, Leal JS, Peeters ETHM. 2017. Rainfall changes affect the algae dominance in tank bromeliad ecosystems. PLOS ONE 12(4): e0175436. doi: 10.1371/journal.pone.0175436
https://doi.org/10.1371/journal.pone.017...
), and certain limnological characteristics (Sophia et al. 2004Sophia MG, Carmo BP, Huszar VL. 2004. Desmids of phytotelm terrestrial bromeliads from the National Park of “Restinga de Jurubatiba”, Southeast Brasil. Algological Studies 114: 99-119.; Gebühr et al. 2006Gebühr C, Pohlon E, Schmidt AR, Küsel K. 2006. Development of microalgae communities in the phytotelmata of allochthonous populations of Sarracenia purpurea (Sarraceniaceae). Plant Biology 8: 849-860.; Marino et al. 2011; Killick et al. 2014Killick SA, Blanchon DJ, Large MF. 2014. Algal communities in phytotelmata: A comparison of native Collospermum and exotic bromeliads (Monocotyledonae) in New Zealand. Telopea 17: 311-318.).

We investigated the algae and cyanobacteria communities present in four species of tank bromeliads in different vegetation formations in northeastern Brazil, emphasizing the composition, richness, and diversity of the species in those environments in order to: (1) evaluate the influence of morphometric attributes of the bromeliad tanks and the abiotic variables of the water retained in them on the richness of the algal and cyanobacterial communities; and, (2) determine the species richness and similarities of the algal and cyanobacterial communities in four tank-bromeliad species.

Materials and methods

Study sites and the bromeliads sampled

The present study was conducted in four areas with different vegetation formations in Bahia State in northeastern Brazil (Fig. 1A): (1) Fazenda Itaberaba (12°30’S, 40°04’W), in the municipality of Itaberaba, an area of caatinga (dryland) vegetation with bromeliads (Aechmea cf. lingulatoides Leme & H.E.Luther) growing on arid soils and fully exposed to the sun light; (2) Serra da Jiboia (12°51’S, 39°28’W), in the municipality of Santa Teresinha, an area of granitic rock outcrops, with bromeliads [Alcantarea nahoumii (Leme) J.R.Grant] growing at 850 m a.s.l. and fully exposed to sun light; (3) Parque das Dunas (12°55’S, 38°19’W), in the municipality of Salvador, a restinga (sandy shoreline) area with bromeliads (Hohenbergia littoralis L.B.Sm.) growing on sand dunes 600 m from ocean and fully exposed to sun light; and (4) Reserva Sapiranga (12°33’S, 38°02’W), in the municipality of Mata de São João, an area of Atlantic Forest with bromeliads (Hohenbergia stellata Schult. & Schult.f.) growing mainly in shaded forest sites (Fig. 1). Some climatic data, such as the rainfall in each study area (municipality), were obtained from the National Institute of Meteorology (INMET 2018INMET - Instituto Nacional de Meteorologia. 2018. Seção Tempo - Subseção Tempo Agora / Gráficos. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos. 10 Jan. 2018.
http://www.inmet.gov.br/portal/index.php...
); air temperatures were obtained using portable probes during collections. Those data are presented in Table 1.

Figure 1
Map of study area, showing the four municipalities in Bahia State, Brazil (A) and the bromeliads studied: Aechmea cf. lingulatoides (B) , Alcantarea nahoumii (C), Hohenbergia littoralis (D), Hohenbergia stellata (E). Please see the PDF version for color reference.

Table 1
Rainfall data of the four study areas (by municipality; INMET 2018INMET - Instituto Nacional de Meteorologia. 2018. Seção Tempo - Subseção Tempo Agora / Gráficos. http://www.inmet.gov.br/portal/index.php?r=tempo/graficos. 10 Jan. 2018.
http://www.inmet.gov.br/portal/index.php...
) between December/2014 and February/2016 and air temperature during the samplings. Values are represented by mean.

Sampling

Study material was gathered from the water retained in the cavities (tanks) formed by the leaves of the bromeliads (four species, Figs. 1B-E) in the four different vegetation formations. The accumulated water was collected using a plastic hose coupled to a 50 ml syringe. To ensure greater efficiency in collecting all biological material, that procedure was repeated several times in each tank. The water in some bromeliads was available in two kinds of phytotelmata (central and lateral), but the same collection procedures were used in both situations. Water from distinct tanks (if present), but from the same bromeliad specimen, were mixed so that each bromeliad represented a single sampling unit.

Quarterly excursions were carried out in the four study areas during 14 months, between 2014 and 2016, totaling 320 sampling units (80 bromeliads from each study area). Water from 20 tank-bromeliads were collected during each sampling period; the bromeliads sampled were randomly chosen based on the throw of a die (1 = North; 2 = East; 3 = West; 4 = South; 5 and 6 =, irrelevant), indicating the direction to follow to the next bromeliad. The distance between a sampled bromeliad and the next was always at least 5 m.

The collected material was held in properly labeled plastic containers (50 ml) and transported in a portable cooler to the Phycology Laboratory (UEFS); all collected materials were subsequently fixed in Transeau solution (Bicudo & Menezes 2017Bicudo CEM, Menezes M. 2017. Gêneros de algas de águas continentais do Brasil: chave para identificação e descrições. São Carlos, RiMa Editora.).

Environmental variables

Abiotic information concerning the tank water, such as temperature, pH, electrical conductivity, and total dissolved solids (TDS) was measured using a Hanna multiparameter probe; dissolved oxygen was measured using a portable digital Instrutherm (MO-910). All limnological variables were measured immediately after harvesting the bromeliad tank water samples. The morphometric characteristics of the bromeliads, such as height, width, and numbers of leaves were also recorded.

Identification of the microalgae and the attributes analyzed

All of the microalgae material was examined under an Olympus LX35 Optical Microscope. Taxonomic identifications were carried out to the infrageneric level whenever possible, and were mainly based on the morphological and metric characteristics of the population, consulting the specialized literature (Huber-Pestalozzi 1955Huber-Pestalozzi G. 1955. Euglenophyceen. In: Huber-Pestalozzi G. (ed.) Das Phytoplankton des Susswasser, Systematik und Biologie. Teil 4. Stuttgart, E. Schweizerbart’sche Verlangsbuchhandlung. p. 1-605.; Prescott et al. 1975Prescott GW, Croasdale HT, Vinyard HT. 1975. A synopsis of North American desmids: part II.Desmidiaceae: Placodermae. Section 1. Lincoln/ London, University of Nebraska Press.; Komárek & Fott 1983Komárek J, Fott B. 1983. Chlorophyceae - Chlorococcales. In: Huber-Pestalozzi G. (ed.) Das Phytoplankton des Süsswassers: Systematic und Biologie. Stuttgart, E. Schweizerbart’sche Verlagsbuchhandling (Nägele u. Obermiller). p. 1-1044.; Komárek & Anagnostidis 1998Komárek J, Anagnostidis K. 1998. Cyanoprokaryota I. - In: Ettl H, Gärtner G, Heynig H, Mollenhauer D. (eds.) Süßwasserflora von Mitteleuropa, Band 19/1, Stuttgart/Jena, Gustav Fischer Verlag. p.1-548.; 2005Komárek J, Anagnostidis K. 2005. Süsswasserflora von Mitteleuropa Vol. 19. Cyanoprokaryota: 2. Teil/2nd Part: Oscillatoriales. München, Elsevier Spektrum Akademischer Verlag. p. 1-759.; John et al. 2011John DM, Whitton BA, Brook AB. 2011. The Freshwater Algal flora of the British isles. 2nd edn. Cambridge, Cambridge University Press.; Wołowski 2011Wołowski K. 2011. Euglenophyta (Euglenoids). In: John DM, Whitton BA, Brook AJ. (eds.) The Freshwater Algal flora of the British isles. An identification guide to freshwater and terrestrial algae. 2nd edn. Cambridge, Cambridge University Press . p. 181-239.; Komárek 2013Komárek J. 2013. Süsswasserflora von Mitteleuropa. Vol. 19. Cyanoprokaryota: 3rd part: heterocystous genera. Heidelberg, Springer Spektrum.; Carty 2014Carty S. 2014. Freshwater dinoflagellates of North America. Ithaca/London, Comstock Publishing Associates. ).

Taxonomic richness was calculated based on the total number of species sampled in each bromeliad tank (Brower et al. 1998Brower JE, Zar JH, Ende CN. 1998. Field and laboratory methods for general ecology. 4th edn. Boston, WCB/McGraw-Hill.). The frequency of occurrence of each algae species (in each bromeliad species) was calculated considering the number of samples in which the taxa occurred in relation to the total number of samples collected. Categories of frequency followed Matteucci & Colma (1982)Matteucci SD, Colma A. 1982. Metodología para el estudio de la vegetatión. Washington, OEA.: > 70 % (quite frequent, VF); ≤ 70 % and > 40 % (frequent, F); ≤ 40 % and > 10 % (occasional, O); and ≤ 10 % (rare, R).

Microalgae community

Algae and cyanobacteria were classified according to their size class (nanoplankton: 2-20 µm, microplankton: > 20-200 µm, mesoplankton: > 200 µm-2 mm) (Reynolds 2006Reynolds CS. 2006. Ecology of phytoplankton. Cambridge, Cambridge University Press . ); and life form: unicellular flagellate (UF), colonial flagellate (CF), unicellular non-flagellated (UNF), colonial non-flagellated (including coenobia) (CNF), and filaments (Fil) (Crossetti & Bicudo 2008Crossetti LO, Bicudo CEM. 2008. Adaptations in phytoplankton life strategies to imposed change in a shallow urban tropical eutrophic reservoir, Garças Reservoir, over 8 years. Hydrobiologia 614: 91-105.).

Statistical analyses

One-way analysis of variance (ANOVA) was used to detect differences in the morphological characteristics of the bromeliads, the abiotic variables of water, and microalgae richness (dependent variables), among the different bromeliad species (independent factor). We also tested for pairwise differences, employing the Tukey post-hoc test using the multcomp package (Hothorn et al. 2008Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50: 346-363.). For this analysis, the data were log10 (x + 1) transformed to fit the assumptions of normality and homoscedasticity.

Principal Component Analysis (PCA) was performed using a variance-covariance matrix; the data was transformed by Z-score to reduce the dimensionality of the morphological and abiotic water parameters of the different bromeliads tanks sampled. All analysis were performed in R environment (R Core Team 2017R Core Team 2017. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. https://www.R-project.org/
https://www.R-project.org...
).The similarities of the algal and cyanobacterial compositions between the four bromeliad species studied were determined by using the Sørensen similarity index (Muller-Dombois, 1981Muller-Dombois D. 1981. Ecological measurements and microbial populations. In: Wicklow DT, Carroll GC. (eds.) The fungal community: Its organization and role in the ecosystem. New York, Marcel Derker. p. 173-184.): 2c/2c + A + B × 100, where A and B represent the number of species in areas A and B; and c corresponds to the number of species held in common in both areas.

A Venn diagram was prepared to illustrate the distribution of algal and cyanobacterial species richness among the different bromeliads, using software available at the Bioinformatics & Evolutionary Genomics (2017)Bioinformatics & Evolutionary Genomics 2017. Ghent, Ghent University. http://bioinformatics.psb.ugent.be/webtools/Venn/. 7 Nov. 2017.
http://bioinformatics.psb.ugent.be/webto...
site.

Results

Morphological attributes of the bromeliads, limnological conditions, and microalgae richness

In terms of the characteristics of the bromeliads sampled, Hohenbergia stellata had high mean diameter and height values while Hohenbergia littoralis had low mean values for those parameters; the other two bromeliad species showed similar measures of those same morphological characteristics. Significant differences were found in the mean numbers of leaves among the bromeliad species, especially between Alcantarea nahoumii (37.8 leaves) and H. littoralis (14.9 leaves) (Tab. 2). The waters in the bromeliad tanks of the four species were predominantly acidic, but with other significant differences between them. Aechmea cf. lingulatoides and A. nahoumii showed high mean electrical conductivities, and their total dissolved solids were two to three times greater than those observed in H. littoralis and H. stellata. The greatest mean dissolved oxygen concentration was found in A. nahoumii (7.8 mg L-1), followed by H. littoralis (6.8 mg L-1). That parameter displayed considerable variation among the different bromeliad species.

Table 2
Mean and standard deviation values (n = 80) of the morphological characteristics, abiotic water conditions, and algae richness sampled in four different bromeliads species (Superscript letter represents the Tukey test results: different letters indicate significant differences, p < 0.05).

The bromeliads studied here were organized according to their morphological characteristics and abiotic water variables in the PCA, with the first two axes explaining 55.8 % of the data variability (eigenvalues: axis 1 = 2.35, axis 2 = 2.03, permutation test = 0.009). Most individuals of H. stellata were grouped on the negative side of axis 1, and were mainly correlated with higher plant diameter (r = -0.76) and height (r = -0.61) values; most individuals of A. nahoumii were also grouped there, correlated to pH (r = -0.65) and numbers of leaves (r = -0.58). Individuals of H. littoralis were grouped on the positive side of axis 1, correlated with high water temperature (r = 0.52). Most individuals of A. nahoumii and some of A. cf. lingulatoides (mainly the ones sampled in Jan/2015) were grouped on the negative side of axis 2, and were correlated with the highest TDS (r = -0.82) and conductivity values (r = -0.81) (Fig. 2).

Figure 2
Principal component analysis based on morphological characteristics and abiotic water variables of four bromeliad species (Diam: Diameter, Heig: Height, Leav: number of leaves, T: water temperature, pH, EC: electrical conductivity, TDS: total dissolved solids, DO: dissolved oxygen).

The phytotelmata algae and cyanobacteria communities were represented by a total of 89 taxa in the four bromeliads species studied, distributed among 54 genera and nine classes: Zygnematophyceae (27 % of the species), Cyanobacteria (24 %), Chlorophyceae (21 %), Euglenophyceae (12 %), Trebouxiophyceae (7 %), Bacillariophyceae (4 %), Chrysophyceae (2 %), Dinophyceae (1 %), and Klebsormidiophyceae (1 %). Of the 320 bromeliad specimens studied, 240 individuals contained representatives of microalgae and/or cyanobacteria; all of the samples collected from Alcantarea nahoumii (80 bromeliad tanks) had microalgae; H. stellata had the lowest number of algal and cyanobacterial species, and they occurred in only 13 of the 80 bromeliads sampled.

The taxonomic richness of microalgae and cyanobacteria was highest in Alcantarea nahoumii (Serra da Jiboia - rock outcrops) with 73 taxa, followed by Hohenbergia littoralis (Parque das Dunas - restinga) (nine), Aechmea cf. lingulatoides (Fazenda Itaberaba - caatinga) (seven), and Hohenbergia stellata (Reserva Sapiranga - Atlantic Forest) (six). In terms of the species richness in the different bromeliads in the four vegetation formations studied, those on the rock outcrops containing 69 exclusive taxa, followed by restinga and caatinga vegetation (six each) and Atlantic Forest (four) (Fig. 3). Only one species, Phacus polytrophos Pochmann, occurred in all four bromeliad species studied. The most representative genus was Cosmarium (nine taxa), and it was the only desmid occurring in more than one bromeliad species.

Figure 3
Venn diagram showing the numbers of microalgae taxa found in the phytotelmata of different bromeliad species in four vegetal formations in Bahia, Brazil.

The mean species richness per individual bromeliad was significantly higher (> 12 times) in Alcantarea nahoumii (mean: 15.9) than in the other three bromeliads (mean: 1.3-0.2 species/ind.). Individual specimens of H. stellata contain the lowest mean number of species (0.2) (Tab. 2).

In terms of the entire sampling period, the microalgae classes with the highest species richness in A. nahoumii were Zygnematophyceae, Cyanophyceae, and Chlorophyceae, which contributed approximately 80 % of the total number of species inventoried. Among the bromeliads species with the lowest richness, A. cf. lingulatoides contained mainly by diatoms, whereas the most representative class in H. littoralis was Euglenophyceae (Fig. 4).

Figure 4
Relative species richness of the taxonomic classes of the microalgae communities in four bromeliad species.

Only four microalgae species (4 % of the total were considered very frequent: Enallax costatus, Parvodinium umbonatum, and Pleurotaenium trabecula, which were found in the bromeliad A. nahoumii; Oedogonium pulchrum was identified in the bromeliad H. littoralis). Most of microalgae species where considered rare (46 %), followed by occasional (35 %), and frequent (15 %). In terms of life forms, the microalgae community was dominated by unicellular non-flagellated taxa (45 %); the most common size class of organisms was microplankton (75 %) (Tab. 3).

Table 3
List of microalgae taxa and their classification by size class, life form, and frequency of occurrence in each bromeliad species. Size class: nano (nanoplankton), micro (microplankton), meso (mesoplankton). Life form: UF (unicellular flagellate), CF (colonial flagellate), UNF (unicellular non-flagellated), CNF (colonial non-flagellated, including coenobia), Fil (filaments). Areas: SB (Serra da Jiboia), PD (Parque das Dunas), Sap (Reserva Sapiranga), Ita (Itaberaba). Bromeliad species: A. nah (Alcantarea nahoumii), H. lit (Hohenbergia littoralis), H.ste (Hohenbergia stellata), A. ling (Aechmea cf. lingutaloides).

The species compositions of the microalgae communities showed low similarities among the different bromeliad species (Tab. 4). The species composition in A. nahoumii was only 3 % similar to that in A. cf. lingulatoides, 5 % similar to that in H. stellata, and 7 % similar to that in H. littoralis. The species composition in A. cf. lingulatoides was most similar to that in H. littoralis (13 %) and H. stellata (15 %).

Table 4
Sorensen's similarity index (expressed as %) applied to presence-absence matrix of microalgae species in water tanks of different bromeliad species.

Taxonomic groups - Richness and main representatives

Zygnematophyceae- Representatives were distributed among 24 taxa, with desmids being the dominant group (19 taxa). Among the most notable representatives were Cosmarium amoenum var. jiboensis, C. bahianum, C. oliveirae, Spirotaenia filiformis, and Staurastrum pseudoteliferum, which were recently described as new to science (Ramos et al. 2017aRamos GJP, Bicudo CEM, Moura CWN. 2017a. Cosmarium bahianum, sp. nov. (Desmidiaceae), a new desmid species from a phytotelm habitat in the Brazilian restinga. Phytotaxa 291: 66-72. ; bRamos GJP, Bicudo CEM, Moura CWN. 2017b. Taxonomic notes on Spirotaenia (Mesotaeniaceae, Zygnematophyceae) from a Brazilian phytotelm habitat: new species and new records. Phytotaxa 309: 265-270.; 2018aRamos GJP, Bicudo CEM, Moura CWN. 2018a. Some new, rare and interesting desmids from bromeliad phytotelmata in Brazil. Phytotaxa 346: 59-77.). Pleurotaenium trabecula was the most frequent desmid in Serra da Jiboia (F = 78 %).

Chlorophyta - Green algae were one of the most diverse groups occurring in phytotelmata in Bahia State, being represented in the present study by two classes: Chlorophyceae (19 taxa) and Trebouxiophyceae (six taxa), which occurred in all four areas, especially Serra da Jiboia (20 taxa); Monoraphidium was the most representative genus (four species). Some taxa, such as Enallax costatus, were widely distributed in the bromeliad tanks of A. nahoumii; Oedogonium pulchrum was the only species consistently encountered, often forming large and dense populations in H. littoralis tanks.

Cyanobacteria- Cyanobacteria displayed the greatest species richness in the phytotelmata at Serra da Jiboia (21 taxa), especially Hapalosiphon stuhlmannii, which was the principal species forming gelatinous masses located in the central rosette of the bromeliads. Those masses contained numerous cyanobacteria representatives including coccoid and colonial, but mainly filamentous organisms.

Bacillariophyta- Diatoms were not very common in the phytotelmata studied, with only four taxa occurring in a small number of bromeliads in Serra da Jiboia and Fazenda Itaberaba.

Dinophyta- Dinoflagellates were represented by a single species (Parvodinium umbonatum) that was restricted to bromeliads at Serra da Jiboia. Nonetheless, that species showed the greatest frequency of occurrence (F = 79 %) among all taxa encountered at Serra da Jiboia.

Euglenophyta - Euglenophytes were represented by 11 taxa; Euglena mutabilis was the most frequent species (F=56 %) of that group in the bromeliads studied.

Discussion

Microalgae richness and the influence of environmental factors

The high taxonomic richness of algae and cyanobacteria in the bromeliads at Serra da Jiboia was apparently related to the following factors: (1) plant architecture - Alcantarea nahoumii generally produces many (over 30) wide leaves that form large numbers of cavities (greater complexity) and consequently more places for water to accumulate; those leaves are also held at open angles that allow higher solar illumination; (2) the regional climate - the bromeliads grow on mountain tops, with forests on their slopes (distinct from the other three areas) - which favors the sites being constantly humid, so that the bromeliad tanks would not usually experience abrupt variations in water volumes (allowing greater community stability); (3) environmental data - the tank water was slightly acidic to neutral, with moderate conductivity and high TDS (indicative of high concentration of dissolved salts and nutrients) as compared to the other bromeliads; the usually high dissolved oxygen content probably contributed to a greater microalgae diversity.

In terms of plant architecture, Carrias et al. (2014Carrias JF, Céréghino R, Brouard O, et al. 2014. Two coexisting tank bromeliads host distinct algal communities on a tropical inselberg. Plant Biology 16: 997-1004. ) reported that greater bromeliad complexity (larger numbers of leaves - and consequently more sub-reservoirs) was associated with lower algal richness. The opposite was observed during the present study, however, mainly in A. nahoumii - the bromeliad species with the greatest number of leaves and the highest algal and cyanobacterial richness when compared to less complex bromeliads. Water volume may also directly influenced algal and cyanobacterial species richness and diversity, as the bromeliads at Serra da Jiboia usually contained large amounts of water well-distributed among the leaves in all four sampling periods.

Overall, the algal and cyanobacterial community similarities among the different bromeliads species were considered quite low (Tab. 4), and probably linked to the distinct environmental conditions in each of the four study areas. Additionally, different bromeliad species tend to host distinct algal communities (Carrias et al. 2014Carrias JF, Céréghino R, Brouard O, et al. 2014. Two coexisting tank bromeliads host distinct algal communities on a tropical inselberg. Plant Biology 16: 997-1004. ).

Recent studies have demonstrated that changes in rainfall distribution can reduce chlorophyll-a concentrations in bromeliad tanks and therefore significantly affect microalgae dominance (Pires et al. 2017Pires APF, Leal JS, Peeters ETHM. 2017. Rainfall changes affect the algae dominance in tank bromeliad ecosystems. PLOS ONE 12(4): e0175436. doi: 10.1371/journal.pone.0175436
https://doi.org/10.1371/journal.pone.017...
). Although we did not measure chlorophyll-a concentrations in the water accumulated in each bromeliad tank, it was evident that the plants from Serra da Jiboia (A. nahoumii) and Parque das Dunas (H. littoralis) contained greater volumes of water than those at Reserva Sapiranga (H. stellata) and Fazenda Itaberaba (A. cf. lingulatoides) -and the bromeliads in the former two areas showed quite different richnesses. The unevenly distributed water storage by H. littoralis leaves (with large amounts of water accumulated in the central tank and considerably smaller volumes in the lateral tanks) may affect the low species richness in that bromeliad in Parque das Dunas. The leaves forming the central tank are usually long and perpendicular to the ground, which allows less light into the bottom of the central tank; the leaves forming the lateral tanks, however, are held at more open angles, permitting greater light penetration. Additionally, the very acidic waters and lower conductivity and TDS values measured in H. littoralis may depress algal and cyanobacterial richness.

Variations in the algal and cyanobacterial communities in phytotelmata would be quite natural, with some well-established taxa and others more temporary. When comparing the desmids in A. nahoumii tanks (Serra da Jiboia) identified during this study with the 16 taxa previously identified for the same area (Ramos et al. 2011Ramos GJP, Oliveira IB, Moura CWN. 2011. Desmídias de ambiente fitotelmata bromelícola da Serra da Jiboia, Bahia, Brasil. Revista Brasileira de Biociências 9: 103-113.), nine continued to inhabit the tanks, whereas the others had disappeared. The nine taxa that persisted are widely distributed among bromeliads in the area, and well-adapted to local conditions, usually forming large populations, even with considerable external impacts (such as fires).

In terms of H. stellata (Reserva Sapiranga), only 13 out of 80 bromeliads sampled contained representatives of algae or cyanobacteria, and the numbers of species per sample were very low. Some contributing factors to that situation probably included: (1) luminosity - the bromeliads were largely shaded, but many of plants exposed to high sunlight (open areas in the forest) showed low diversity. Even in open areas, leaves from surrounding trees will fall into the tanks, often almost completely covering them; and, (2) dissolved oxygen - DO concentrations were commonly quite low (mean of 4.8 mg L-1; near 2.5 mg L-1 in some samples). According to Laessle (1961Laessle AM. 1961. A micro-lirnnological study of Jamaican Bromeliads. Ecology 42: 499-517.), algae are usually abundant in bromeliads that have high DO concentrations - a condition rarely observed in H. stellata in the present study. Additionally, many of those bromeliads held only small amounts of water (or were completely dry during some sampling periods). Among the main components found in H. stellata tanks were fungi, pollen grains, protozoa and organic matter debris.

Taxonomic groups - Richness and main representatives

Desmids are one of the main microalgae groups occurring in bromeliad phytotelmata in Brazil (Sophia 1999Sophia MG. 1999. Desmídias de ambientes fitotélmicos bromelícolas. Revista Brasileira de Biologia 59: 141-150.; Sophia et al. 2004Sophia MG, Carmo BP, Huszar VL. 2004. Desmids of phytotelm terrestrial bromeliads from the National Park of “Restinga de Jurubatiba”, Southeast Brasil. Algological Studies 114: 99-119.; Ramos et al. 2011Ramos GJP, Oliveira IB, Moura CWN. 2011. Desmídias de ambiente fitotelmata bromelícola da Serra da Jiboia, Bahia, Brasil. Revista Brasileira de Biociências 9: 103-113.). Water conditions, such as low pH and low conductivity, are typical of phytotelmata environments and favor desmid development (Sophia et al. 2004Sophia MG, Carmo BP, Huszar VL. 2004. Desmids of phytotelm terrestrial bromeliads from the National Park of “Restinga de Jurubatiba”, Southeast Brasil. Algological Studies 114: 99-119.). A number of desmid species were recently described for the first time from bromeliads in Bahia State, suggesting that those environments as important centers of desmid biodiversity (Ramos et al. 2018aRamos GJP, Bicudo CEM, Moura CWN. 2018a. Some new, rare and interesting desmids from bromeliad phytotelmata in Brazil. Phytotaxa 346: 59-77.).

In terms of the main Chlorophyta taxa, we highlight the genus Rhopalosolen, which was recently reported for the first time for Brazil (Ramos et al. 2017Ramos GJP, Bicudo CEM, Moura CWN. 2017c. Algae in phytotelmata from Caatinga: first record of the genus Rhopalosolen Fott (Chlorophyta) for Brazil. Check List 13: 403-410.c). In the bromeliads with a predominance of filamentous green algae (such as the genus Oedogonium), common predators such as rotifers, cladocerans, and copepods could be influencing the low observed algal richness.

The cyanobacteria comprise one of the most important groups found in phytotelmata in terms of taxonomic diversity and their ecological roles (Bermudes & Benzing 1991Bermudes D, Benzing DH. 1991. Nitrogen fixation in association with Ecuadorian bromeliads. Journal of Tropical Ecology 7: 531-536.). An interesting feature of the cyanobacteria identified in the bromeliad phytotelmata was their normal association with rivers, waterfalls, tree barks, rocks, even hot springs (Komárek & Anagnostidis 1998Komárek J, Anagnostidis K. 1998. Cyanoprokaryota I. - In: Ettl H, Gärtner G, Heynig H, Mollenhauer D. (eds.) Süßwasserflora von Mitteleuropa, Band 19/1, Stuttgart/Jena, Gustav Fischer Verlag. p.1-548.; 2005Komárek J, Anagnostidis K. 2005. Süsswasserflora von Mitteleuropa Vol. 19. Cyanoprokaryota: 2. Teil/2nd Part: Oscillatoriales. München, Elsevier Spektrum Akademischer Verlag. p. 1-759.; Komárek 2013Komárek J. 2013. Süsswasserflora von Mitteleuropa. Vol. 19. Cyanoprokaryota: 3rd part: heterocystous genera. Heidelberg, Springer Spektrum.) - so that bromeliad phytotelmata are important environments for cyanobacteria diversity and bring together in just one place species otherwise known from very diverse habitats.

The low diversity of diatoms encountered in bromeliad tanks was not surprising. In a study of diatoms in bromeliads in Rio de Janeiro State, however, Lyra (1971Lyra LT. 1971. Algumas diatomáceas encontradas em Bromeliáceas, Brasil. Memórias do Instituto Oswaldo Cruz 69: 129-139.) reported reduced numbers of those microalgae and attributed that result to their oligotrophic tank water conditions, as well as other environmental factors such as light intensity and temperature. According to that author, mineral element concentrations in those environments could considerably interfere with frustule development - although Pinnularia is one of the most common diatom genera inhabiting those microhabitats, and has been reported in a number of different bromeliad species (Lyra 1971Lyra LT. 1971. Algumas diatomáceas encontradas em Bromeliáceas, Brasil. Memórias do Instituto Oswaldo Cruz 69: 129-139.; 1976Lyra LT. 1976. Microflora de bromeliáceas do Estado de Pernambuco, Brasil. Memórias do Instituto Oswaldo Cruz 14: 37-50.).

Parvodonium umbonatum (the only dinoflagellate identified in the present study) have been reported as occurring in bromeliads in Rio de Janeiro State (as Peridinium umbonatum; Sophia 1999Sophia MG. 1999. Desmídias de ambientes fitotélmicos bromelícolas. Revista Brasileira de Biologia 59: 141-150.). During dry periods, spherical, reddish-brown cysts of P. umbonatum were often encountered in the bromeliads at Serra da Jiboia - possibly representing a reproductive strategy in response to unfavorable environmental conditions. That species was consistently observed forming large populations during all of the sampling periods (Ramos et al. 2016Ramos GJP, Bicudo CEM, Moura CWN. 2016. First record of Parvodinium umbonatum (Stein) Carty (Peridiniaceae, Dinophyta) for northeast Brazil. Check List 12: 1-6. ).

In terms of Euglenophytes, Carrias et al. (2014Carrias JF, Céréghino R, Brouard O, et al. 2014. Two coexisting tank bromeliads host distinct algal communities on a tropical inselberg. Plant Biology 16: 997-1004. ) reported that heterotrophic microalgae species were dominant in areas exposed to direct sunlight - but that tendency was precisely the opposite among bromeliads in Bahia - with euglenophytes appearing predominantly in shaded (or partially shaded) bromeliads. Colorless euglenophytes were encountered at Reserva Sapiranga, but chlorophyllous taxa were much more common in bromeliads exposed to direct sunlight, especially Euglena mutabilis, which commonly forms large populations (Ramos et al. 2017Ramos GJP, Bicudo CEM, Moura CWN. 2017c. Algae in phytotelmata from Caatinga: first record of the genus Rhopalosolen Fott (Chlorophyta) for Brazil. Check List 13: 403-410.d)

Although a total of nine microalgae classes were encountered in the four bromeliad species, other microalgae groups may occur in those phytotelmata, such as Xanthophyceae (Sophia 1999Sophia MG. 1999. Desmídias de ambientes fitotélmicos bromelícolas. Revista Brasileira de Biologia 59: 141-150.) and Cryptophyceae (Hernandez-Rodriguez et al. 2014Hernández-Rodríguez B, Estrada-Vargas L, Novelo E. 2014. Las microalgas de Tillandsia multicaulis Steud. (Bromeliaceae) de la Reserva Ecológica “La Martinica”, Veracruz. TIP Revista Especializada en Ciencias Químico-Biológicas 17: 117-125. ), although little is currently known about the diversity of those groups in those microhabitats, and what environmental conditions are ideal for their development.

Conclusion

The algae and cyanobacteria communities found in the phytotelmata of bromeliads growing in distinct vegetation formations were all very different, with one bromeliad species (Alcantarea nahoumii) being especially distinguished by its high taxonomic richness. We also observed low microalgae species similarity among the bromeliads studied, with only one species (Phacus polytrophos) occurring in all four bromeliad species.

Overall, the following conditions were found to be favorable to high algae and cyanobacteria richness in bromeliad phytotelmata: slightly acidic water at high temperatures, moderate conductivity, large numbers of leaves (with large amounts of water), high dissolved oxygen levels, and high environmental light intensities (Laessle 1961Laessle AM. 1961. A micro-lirnnological study of Jamaican Bromeliads. Ecology 42: 499-517.; Sophia et al. 2004Sophia MG, Carmo BP, Huszar VL. 2004. Desmids of phytotelm terrestrial bromeliads from the National Park of “Restinga de Jurubatiba”, Southeast Brasil. Algological Studies 114: 99-119.; Brouard et al. 2011Brouard O, Jeune A-H, Leroy C, et al. 2011. Are algae relevant to the detritus-based food web in tank-bromeliads? PLOS ONE 6: e20129. doi: 10.1371/journal.pone.0020129
https://doi.org/10.1371/journal.pone.002...
; Marino et al. 2011Marino NAC, Guariento RB, Dib V, Azevedo FD, Farjalla VF. 2011. Habitat size determine algae biomass in tank-bromeliads. Hydrobiologia 678: 191-199.), high rainfall (Pires et al. 2017Pires APF, Leal JS, Peeters ETHM. 2017. Rainfall changes affect the algae dominance in tank bromeliad ecosystems. PLOS ONE 12(4): e0175436. doi: 10.1371/journal.pone.0175436
https://doi.org/10.1371/journal.pone.017...
), and available nutrients (Laessle 1961Laessle AM. 1961. A micro-lirnnological study of Jamaican Bromeliads. Ecology 42: 499-517.; Marino et al. 2011Marino NAC, Guariento RB, Dib V, Azevedo FD, Farjalla VF. 2011. Habitat size determine algae biomass in tank-bromeliads. Hydrobiologia 678: 191-199.).

Combined analyses of limnological variables, bromeliad position (shade or sun), and plant morphology are important to understanding the patterns of microalgae communities in phytotelmata environments, and more detailed studies will be needed to increase our knowledge of algae and cyanobacteria distributions and their ecological relationships within that interesting microhabitat.

Acknowledgements

The authors thank CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico and FAPESB - Fundação de Amparo à Pesquisa do Estado da Bahia (Project “Flora da Bahia”, 483909/2012) for their financial support. GJPR thanks FAPESB for the doctoral fellowship (nº BOL0513/2014).

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Publication Dates

  • Publication in this collection
    Oct-Dec 2018

History

  • Received
    23 Feb 2018
  • Accepted
    17 Apr 2018
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br