ABSTRACT
The semiarid region of northeastern Brazil possesses a set of wetlands characterized by hydrographic basins with deficient drainage networks, a few large and permanent lotic systems and several permanent and temporary lagoons. Aquatic plants are widely distributed in these wetlands and the present study aims to determine if those of Ceará state have similar species compositions and differences in species richness. We hypothesized that lentic ecosystems would have more species and different growth forms of aquatic angiosperms than lotic ecosystems. A total of 1619 records of aquatic angiosperms in 43 wetland areas were analysed. The most representative families were Cyperaceae, Poaceae, Fabaceae, Alismataceae, Malvaceae, Nymphaeaceae and Pontederiaceae. Most of the species are helophytes and bottom-rooted emergent hydrophytes. Permanent lentic ecosystems had the highest number of exclusive species (27.85 %), followed by temporary lentic ecosystems (20.54 %). Contrary to our hypothesis, the different aquatic ecosystems were found to possess distinct species compositions and different proportions of growth forms, and all wetland types contributed to the macrophyte richness of the study area, although they differ in species richness. Therefore, conservation plans for the native aquatic macrophyte biota should include all wetland ecosystems in the semiarid state of Ceará.
Keywords:
biodiversity; floristic richness; hydrophytes; macrophytes; seasonal aquatic ecosystems
Introduction
Arid regions are traditionally perceived as relatively simple ecosystems, with low species diversity (McNeely 2003McNeely J. 2003. Biodiversity in arid regions: Values and perceptions. Journal of Arid Environments 54: 61-70.). However, the conclusions about the patterns of diversity in these regions can differ widely depending on the taxon analysed and the peculiarities of the geographical areas (MacKay 1991MacKay W. 1991. The role of ants and termites in desert communities. In: Polis G. (ed.) The ecology of desert communities. Tucson, The University of Arizona Press. p. 113-150.). If we consider that in temporary pools, the spatial structure of the aquatic plant community changes significantly during the rainy season according to the stage of flooding (Ferreira et al. 2015Ferreira FS, Tabosa AB, Benvindo GR. 2015. Spatiotemporal ecological drivers of an aquatic plant community in a temporary tropical pool. Journal of Arid Environments 115: 66-72.), would the diversity of aquatic plants in the semiarid region be differentiated between the lentic and lotic systems?
Wetlands in semiarid zones of northeastern Brazil are influenced by climatic seasonality and unpredictable flood pulses, which present multiannual frequency and low amplitude (Junk et al. 2014Junk W, Piedade MTF, Lourival R, et al. 2014. Brazilian wetlands: Definition, delineation and classification for research, sustainable management and protection. Aquatic Conservation: Marine and Freshwater Ecosystems 24: 5-22.). A biogeographic delineation approach of South American freshwater ecosystems considered the extreme Northeast of Brazil as the “Ecoregion Northeastern Caatinga and Coastal drainages” (Abell et al. 2008Abell R, Thieme ML, Revenga C, et al. 2008. Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58: 403-414), with a predominance of aquatic systems albeit of low water volume, but functional in terms of regulation of the regional hydrological regime and maintenance of biodiversity (Junk et al. 2014Junk W, Piedade MTF, Lourival R, et al. 2014. Brazilian wetlands: Definition, delineation and classification for research, sustainable management and protection. Aquatic Conservation: Marine and Freshwater Ecosystems 24: 5-22.). Particularly in this ecoregion, Ceará state presents the largest flood area (24,339.65 ha) and the largest number of temporary lagoons (2,930) (Maltchick et al. 1999Maltchick L, Costa MAJ, Duarte MDC. 1999. Inventory of Brazilian semi-arid shallow lakes. Anais da Academia Brasileira de Ciências 71: 801-808.). Therefore, these temporary lagoons, together with the hydrographic basins with a deficient drainage network and the permanent lentic systems of coastal formations (Claudino-Sales & Peulvast 2002Claudino-Sales V, Peulvast JP. 2002. Dune generation and ponds on the coast of Ceará State (Northeast Brazil). In: Allison RJ. (ed.) Applied Geomorphology. Chinchester, John Wiley & Sons. p. 443-460.), characterize the set of wetlands in the state.
Temporary lagoons have a cyclical nature, involving alternating rainy and dry seasons, which favours the succession of different species in processes of flooding and drought (Tabosa et al. 2012Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.). In contrast, the permanent lagoons, given the stability of the water column, have plant communities associated with the depth of the euphotic zone, as this is a determining factor for the extension of the habitats of macrophytes (Wetzel 2001Wetzel RG. 2001. Limnology. San Diego, Academic Press.). Furthermore, in artificial ecosystems like weirs, aquatic plant assemblages are more associated with nutrient concentrations than with water depth (Paiva et al. 2014Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.).
On the other hand, lotic systems in the Brazilian semiarid region are characterized by flash floods during the rainy season that can vary according to rainfall, i.e., the water can flow for weeks in small streams or months in larger rivers during the ‘wet phase’ (Maltchick & Medeiros 2006Maltchick L, Medeiros ESF. 2006. Conservation importance of semi-arid streams in north-eastern Brazil: implications of hydrological disturbance and species diversity. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 665-677.). During the dry season or “drying phase”, water flow ceases, leading to the formation of strings of disconnected temporary pools along the riverbed where the aquatic biota survives (Medeiros & Maltchick 1999Medeiros ESF, Maltchick L. 1999. The effects of hydrological disturbance on the intensity of infestation of Lernaea cyprinacea in an intermittent stream fish community. Journal of Arid Environments 43: 351-356.). In addition, due to the absence of the river-floodplain system, only the main river channel keeps the temporary pools in the dry season, resulting in less habitat availability for aquatic organisms (Maltchick & Medeiros 2006Maltchick L, Medeiros ESF. 2006. Conservation importance of semi-arid streams in north-eastern Brazil: implications of hydrological disturbance and species diversity. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 665-677.).
Along the coast of Ceará, permanent and temporary aquatic systems originate in interdune and deflated dune areas, as a result of flooding during the rainfall period or the rise of the water column in less permeable soils, and are located mainly between old Quaternary dunes and Tertiary Formations (also known as “Formação Barreiras” [Claudino-Sales & Peuvast 2002Claudino-Sales V, Peulvast JP. 2002. Dune generation and ponds on the coast of Ceará State (Northeast Brazil). In: Allison RJ. (ed.) Applied Geomorphology. Chinchester, John Wiley & Sons. p. 443-460.]). In addition to these, permanent lentic ecosystems originate from the barrage of rivers in the vicinity of their mouths due to the accumulation of sand carried by the wind (forming the “lagamares”), or by abandoned meanders and marginal lagoons located along corridors of the main rivers that reach the coast (Silva et al. 2007Silva LAC, Araujo RCP, Maia LP, et al. 2007. Zoneamento ecológico-econômico da zona costeira do Estado do Ceará. Annais do XLV Congresso da Sociedade Brasileira de Sociologia, Administração e Economia Rural. Londrina, SOBER. p. 1-20.).
Aquatic plants occur both in coastal environments (Matias et al. 2003Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.; Moro et al. 2014Moro MF, Sousa DJL, Matias LQ. 2014. Rarefaction, richness estimation and extrapolation methods in the evaluation of unseen plant diversity in aquatic ecosystems. Aquatic Botany 117: 48-55.) and in temporary and permanent aquatic systems, natural or artificial, located in the semiarid region (Paiva et al. 2014Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.; Albuquerque et al. 2020Albuquerque AC, Rodrigues-Filho CAS, Matias LQ. 2020. Influence of climatic variables on CSR strategies of aquatic plants in a semiarid region. Hydrobiologia 847: 61-74.). In shallow lagoons, plant communities occupy the entire water column, forming strata of submerged hydrophytes, overlaid by bottom-rooted emergents with floating leaves and/or stems, and by bottom-rooted emergents above the water surface (Tabosa et al. 2012Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.). In deep permanent reservoirs and lagoons, the communities occur at shallower depths and periodically flooded banks (Matias et al. 2003Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.; Paiva et al. 2014Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.). In lotic ecosystems, species richness is lower in systems with deficient drainage, and communities are influenced by the flood intensity (Pedro et al. 2006Pedro F, Maltchick L, Biachini Jr I. 2006. Hydrologic cycle and dynamics of aquatic macrophytes in two intermittent rivers of the semi-arid region of Brazil. Brazilian Journal of Biology 66: 575-585.).
Growth forms vary according to the stability of the water column, with the presence of submerged forms in permanent lentic systems being more common (Matias et al. 2003Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.; Moro et al. 2014Moro MF, Sousa DJL, Matias LQ. 2014. Rarefaction, richness estimation and extrapolation methods in the evaluation of unseen plant diversity in aquatic ecosystems. Aquatic Botany 117: 48-55.; Paiva et al. 2014Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.) while the bottom-rooted emergents and bottom-rooted emergents with floating leaves and/or stems share the water surface in temporary lentic systems (Tabosa et al. 2012Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.).
On the other hand, the dynamics of the water column in permanent lotic systems constitute a strong environmental filter to colonization by aquatic plants, which depend on marginal areas, such as an underwater banks or places with water between the spit and the shore, which are protected from strong turbulence (Sculthorpe 1967Sculthorpe CD. 1967. The biology of aquatic plants. London, Edward Arnold.). The bottom-rooted emergent and bottom-rooted submerged forms occur in these marginal habitats (Koehler & Bove 2004Koehler S, Bove CP. 2004. Alismatales from the Araguaia River Basin (MT/GO, Brazil). Brazilian Journal of Botany 27: 439-452. ), whilst haptophytes are restricted to habitats with accentuated unevenness (Silva et al. 2015Silva IC, Bove CP, Koschnistzche C. 2015. Plantas de corredeiras: reprodução e conservação de Podostemaceae. Natureza on Line (Espírito Santo) 13: 6-11.). And, in temporary lotic systems, the occurrence of two phases of hydrological disturbance (flooding and drought) exert a strong influence so that angiosperms with bottom-rooted submerged or free-floating forms are observed in the areas of river resurgences or permanent river puddles (Maltchick & Medeiros 2006Maltchick L, Medeiros ESF. 2006. Conservation importance of semi-arid streams in north-eastern Brazil: implications of hydrological disturbance and species diversity. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 665-677.; Maltchick & Bianchini 2006Maltchick L, Bianchini I. 2006. Hydrologic cycle and dynamics of aquatic macrophytes in two intermittent rivers of the semi-arid region of Brazil. Brazilian Journal of Biology 66: 575-585.).
Considering that aquatic plants are widely distributed in wetlands, the present study analyses if aquatic systems of Ceará state tend to show similarity in species composition and differences in species richness and growth forms. We hypothesize I) that lentic ecosystems, natural or artificial, will exceed lotic ecosystems in the number of species (richness). However, as rivers present drainage deficiency and discontinuity (having stability of the water column for only a few months), we expect that II) lentic and lotic ecosystems present similarity in species composition and differences in the proportions of growth forms.
Materials and methods
Data source
All records of angiosperms (number of species in each area) from wetlands of Ceará state were obtained through systematic inventories carried out in the state, collections were performed during the wet seasons from 2000 to 2020 and are published elsewhere and we also included data (number of species) from Iguatu wetlands from unpublished studies (Tab. 1). In the case of these unpublished studies, all species were sampled in Iguatu wetlands along the shoreline of the lagoons using three transects 50 m apart, from the margin to the furthermost area of the macrophyte stand, close to the limnetic zone. Plants were sampled in a belt transect ca. 1 m wide using traditional plant sampling tools (scissors, shovels and hoes), given that the depth of the water column (less than 1 m) did not require any other apparatus.
Nomenclatural data were updated based on IPNI (http://www.ipni.org/), Flora do Brasil 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/. 11 Mar. 2020.
http://reflora.jbrj.gov.br/...
(http://reflora.jbrj.gov.br), Tropicos (http://tropicos.org) and The Plant List (http://theplantlist.org). Identifications made by specialists were considered and others had their identifications updated based on the specific literature for each family. The new records and origin status (native or exotic) were based on Flora do Brasil 2020 (2020)Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/. 11 Mar. 2020.
http://reflora.jbrj.gov.br/...
, in order to highlight the main invasive species, we annotated this information after each scientific name in the species list (Moro et al. 2012Moro MF, Souza VC, Oliveira-Filho AT, et al. 2012. Alienígenas na sala: o que fazer com espécies exóticas em trabalhos de taxonomia florística e fitossociologia? Acta Botanica Brasilica 26: 991-999.). Growth forms were classified following Cook (1990)Cook CDK. 1990. Aquatic Plant Book. Amsterdam, New York, SPB Academic Publishing. as the following: (1) Hydrophytes: bottom-rooted submerged (RS), bottom-rooted emergent (RE), bottom-rooted emergent with floating leaves and/or stems (RLF), free-swimming submerged (FS), free-floating emergent (FE), and (2) Helophytes (Hel).
For the similarity analysis, the following 43 wetland habitats were selected: 9 Permanent Lentic (PLE), 11 Temporary Lentic (TLE), 8 Permanent Lotic (PLO), 7 Temporary Lotic (TLO) and 8 Artificial Lentic (ALE) ecosystems (Fig. 1, Tab. S1 in supplementary material).
Map of the localization of the 43 selected wetland areas. ALE = Artificial Lentic ecosystem; PLE = Permanent Lentic ecosystem; PLO = Permanent Lotic ecosystem; TLE = Temporary Lentic ecosystem; TLO = Temporary Lotic ecosystem.
Statistical analyses
To compare the richness among the five different ecosystems (PLE, TLE, PLO, TLO and ALE) we used the extrapolation approach based on the Hill number with q = 0 (Chao et al. 2014Chao A, Gotelli NJ, Hsieh TC, et al. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45-67.), using the iNEXT package (Hsieh et al. 2013Hsieh TC, Ma KH, Chao A. 2013. iNEXT online: interpolation and extrapolation (Version 1.0) [Software]. http://chao.stat.nthu.edu.tw/blog/software-download/. 13 Mar. 2020.
http://chao.stat.nthu.edu.tw/blog/softwa...
) in R software (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. 25 May 2020.
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). We performed 1000 randomizations and calculated the confidence interval at 95 %.
We calculated the distance of species composition among the 43 ponds and rivers with the Jaccard dissimilarity index. The distance matrix was related to their features (lentic or lotic and permanent, temporary or artificial) with a PERMANOVA approach, which is a multivariate analysis of variance for dissimilarity data with permutations (Anderson 2001Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32 46.; McArdle & Anderson 2001McArdle BH, Anderson MJ. 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290-297.). PERMANOVA does not have the assumption of normal distribution, being characterized as a non-parametric analysis more powerful than the analysis of similarity (ANOSIM) and the Mantel test in detecting differences in real communities (Anderson & Walsh 2013Anderson MJ, Walsh DCI. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs 83: 557-574.). PERMANOVA also assumes independent observations, it can use categorical or continuous independent variables, and it uses a permutation test (Anderson 2001). We used the “adonis” function with 10,000 replications, followed by the “betadisper” function in the “vegan” package (Oksanen et al. 2019Oksanen J, Blanchet FG, Friendly M, et al. 2019. Vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan. 10 May 2020.
https://CRAN.R-project.org/package=vegan...
) in R software (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. 25 May 2020.
https://www.R-project.org/...
).
To understand the proportion of growth forms, considering the interaction of lotic/lentic and temporary/artificial/permanent ecosystems, we calculated the Scheirer-Ray-Hare test, which is a non-parametric test analogous to the two-way ANOVA when their assumptions are not met (Sokal & Rohlf 1995Sokal RR, Rohlf FJ. 1995. Biometry. 3rd. edn. New York, W. H. Freeman and Company.). We used the proportion of growth forms because the number of sampled units of Permanent Lentic (9), Temporary Lentic (11), Permanent Lotic (8), Temporary Lotic (7) and Artificial Lentic (8) were different and, thus, not comparable concerning the absolute number of species in each growth form.
Additionally, we performed the post-hoc pairwise Dunn test (Sokal & Rohlf 1995Sokal RR, Rohlf FJ. 1995. Biometry. 3rd. edn. New York, W. H. Freeman and Company.). The Scheirer-Ray-Hare test was calculated with the “rcompanion” package (Mangiafico 2019Mangiafico S. 2019. rcompanion: functions to support extension education program evaluation. R package version 2.2.1. https://CRAN.R-project.org/package=rcompanion. 04 Mar. 2020.
https://CRAN.R-project.org/package=rcomp...
) and the Dunn test with the “FSA” package (Ogle et al. 2020Ogle DH, Wheeler P, Dinno A. 2020. FSA: fisheries stock analysis. R package version 0.8.30. https://github.com/droglenc/FSA. 20 May 2020.
https://github.com/droglenc/FSA...
), both in R software (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. 25 May 2020.
https://www.R-project.org/...
).
Results
Our sampling of aquatic angiosperms is represented by 44 families, 108 genera and 219 species (Tab. 1). The most representative families were Cyperaceae (23 %), Fabaceae (10 %), Poaceae (9 %), Alismataceae (5 %), followed by Araceae, Nymphaeaceae and Pontederiaceae (4 % each) (Fig. 2A). Most of the species are helophytes (58 %) and bottom-rooted emergent hydrophytes (22 %) (Fig. 2B). Of the species in this study, 21 are new records for Ceará state (Flora do Brasil 2020 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/. 11 Mar. 2020.
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), most representatives of Poaceae (7 spp.).
Floristic list of species collected in aquatic ecosystems in Ceará state, northeastern Brazil. The growth forms (GF) were classified following Cook (1990)Cook CDK. 1990. Aquatic Plant Book. Amsterdam, New York, SPB Academic Publishing.: (1) Hydrophytes: bottom-rooted submerged (RS), bottom-rooted emergent (RE), bottom-rooted emergent with floating leaves and/or stems (RLF), free-swimming submerged (FS), free-floating emergent (FE), haptophytes (HAP), and (2) Helophytes (Hel). PLE - Permanent Lentic ecosystem; TLE - Temporary Lentic ecosystem; PLO - Permanent Lotic ecosystem; TLO - Temporary Lotic ecosystem; ALE - Artificial Lentic ecosystem. (*) New record for Ceará state.
A. Percentage of species richness per family in the study areas. B. Percentage of growth forms (Cook 1990Cook CDK. 1990. Aquatic Plant Book. Amsterdam, New York, SPB Academic Publishing.) of aquatic angiosperms in the study areas. (Hel) Helophytes; (RE) Bottom-rooted emergent; (RLF) Bottom-rooted emergent with floating leaves and/or stems; (RS) Bottom-rooted submerged; (FE) Free-floating emergent; (FS) Free-swimming submerged; (HAP) Haptophytes.
The greatest values for species richness were found in permanent (162 spp.) and temporary lentic (107 spp.) ecosystems, followed by artificial lentic ecosystems (86 spp.). Temporary (32 spp.) and permanent lotic (51 spp.) ecosystems presented the lowest richness (Fig. 3). Six species occurred in all five ecosystems: Echinodorus subalatus, Pistia stratiotes, Neptunia plena, Nymphaea amazonum, Ludwigia helminthorrhiza and Ludwigia leptocarpa. Permanent lentic ecosystems showed the largest number of exclusive species (61 or 27.85 %), followed by temporary lentic (45 or 20.54 %), artificial lentic (14 or 6.39 %), permanent lotic (12 or 5.47 %) and temporary lotic (8 or 3.65 %). Most of the species (123 or 56.16 %) occurred exclusively in non-artificial lentic ecosystems.
Rarefied and extrapolated (black symbols) number of species in the five ecosystems analysed. Confidence interval at 95% after 1000 randomizations (grey symbols, with the same shape of the correspondent rarefied and extrapolated number of species). The filled symbols are the observed number of species and have the same shape as the rarified and extrapolated number of species. The left side of the observed richness is the rarified and the right side is the extrapolated number of species. ALE = Artificial Lentic ecosystem; PLE = Permanent Lentic ecosystem; PLO = Permanent Lotic ecosystem; TLE = Temporary Lentic ecosystem; TLO = Temporary Lotic ecosystem.
The five ecosystems have different species compositions (F = 1.25; R² = 0.03; P = 0.03), but no significant dispersion (F4.38 = 0.87; P = 0.48), indicating that the difference among the five ecosystems is greater than the difference within the ecosystems (Fig. 4; Tab. 2). Temporary aquatic systems tend to have higher proportions of free-swimming submerged and bottom-rooted emergents with floating leaves and/or stems (Fig. 5A and B, Tab. S2 in supplementary material), whereas lentic ecosystems tend to have higher proportions of bottom-rooted submerged forms than lotic ecosystems (Fig 5C, Tab. S2 in supplementary material). On the other hand, helophytes tend to show different proportions among the different ecosystems (Fig. 5D, Tab. S2 in supplementary material).
Nonmetric Multidimensional Scaling (NMDS) representing the grouping of the wetlands and their corresponding ecosystems. The PERMANOVA indicated the difference among the five ecosystems (F = 1.25; R² = 0.03; P = 0.03; Table 1). ALE = Artificial Lentic ecosystem; PLE = Permanent Lentic ecosystem; PLO = Permanent Lotic ecosystem; TLE = Temporary Lentic ecosystem; TLO = Temporary Lotic ecosystem. The stress of the NMDS is 0.29.
Permutational Multivariate Analysis of Variance Using Distance Matrices (PERMANOVA) results considering the five different habitats. The interaction is related the two factors: temporary/permanent/artifical and lotic/lentic. ALE = artificial lentic; PLE = permanent lentic; PLO = permanent lotic; TLE = temporary lentic; TLO = temporary lotic wetland.
Boxplots showing the distribution of the proportion of growth forms among the aquatic ecosystems. A-B. Artificial, permanent, temporary; C. lentic and lotic; D. different combinations of both. We show only the significant results in Table S2 in supplementary material. ALE = Artificial Lentic ecosystem; PLE = Permanent Lentic ecosystem; PLO = Permanent Lotic ecosystem; TLE = Temporary Lentic ecosystem; TLO = Temporary Lotic ecosystem. Grey points: the proportions of the life-form in the aquatic ecosystems.
Discussion
Our hypothesis that lentic ecosystems present more species of aquatic angiosperms was confirmed. However, our results show that the different aquatic ecosystems present distinct species composition and different proportions of sets of growth forms (bottom-rooted submerged, bottom-rooted emergent, bottom-rooted emergent with floating leaves and/or stems, free-swimming submerged, free-floating emergent, haptophytes and helophytes) according to the ecosystem. This result does not corroborate the hypothesis that in permanent lentic ecosystems there would be a greater diversity of growth forms compared to the others.
Cyperaceae and Poaceae were the most representative families in the wetlands of Ceará state. These plant families also constitute the greatest richness of monocotyledons in the world (Bouchenak-Khelladi et al. 2014Bouchenak-Khelladi Y, Muasya AM, Linder HP. 2014. A revised evolutionary history of Poales: origins and diversification Botanical Journal of the Linnean Society 175: 4-16.) and exhibit strong dominance in several wetlands worldwide (Sieben 2010Sieben EJ, Morris CD, Kotze DC, et al. 2010. Changes in plant form and function across altitudinal and wetness gradients in the wetlands of the Maloti-Drakensberg, South Africa. Plant Ecology 207: 107-119.; Rodríguez-Arias & Benavides 2016Rodríguez-Arias CE, Benavides AMS. 2016. Vegetación acuática de los humedales de la microcuenca alta de la quebrada Estero, San Ramón de Alajuela, Costa Rica. Brenesia 85/86: 9-20.; Oliveira et al. 2019Oliveira LS, Andrade BO, Boldrini II, Moço CC. 2019. Aquatic vascular plants of South Brazil: checklist and a comparative floristic approach. Acta Botanica Brasilica 3: 709-715.). Furthermore, the initial diversification of these plant groups occurred in the Paleogene (Bremer 2002Bremer K. 2002. Gondwanan evolution of the grass alliance of families (Poales). Evolution 56: 1374-1387.), a period of intense rainfall and open landscapes (Cerling et al. 1998Cerling TE, Ehleringer JR, Harris JM. 1998. Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philosophical Transactions of the Royal Society Series B 353: 159-171.), probably in wetlands (Givnish et al. 2010Givnish TJ, Ames M, McNeal JR, et al. 2010. Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Annals of the Missouri Botanical Garden 97: 584-616.). In addition, some Poales are restricted to aquatic ecosystems, such as Typhaceae, Xyridaceae and some genera of Eriocaulaceae (Bouchenak-Khelladi et al. 2014Bouchenak-Khelladi Y, Muasya AM, Linder HP. 2014. A revised evolutionary history of Poales: origins and diversification Botanical Journal of the Linnean Society 175: 4-16.), which are also found in Ceará state.
Species of Cyperaceae, Poaceae, Fabaceae, Alismataceae and Malvaceae predominate in the wetland flora of Ceará and are mostly helophytes and bottom-rooted emergent hydrophytes. These growth forms stand out in lotic systems and the margins of lentic systems, habitats usually associated with primary succession. Notably, Cyperaceae and Poaceae species present efficient long-distance dispersal mechanisms and underground systems that allow for effective vegetative propagation (Goetghebeur 1998Goetghebeur P. 1998. Cyperaceae. In: Kubitzki K. (ed.) The families and genera of vascular plants. Volume IV: Flowering Plants - Monocotyledons: Alismatanae and Commelinanae (except Gramineae). Berlin, Heidelberg, Springer. p. 141-190.). Both families usually have the largest number of representatives in aquatic environments (Matias et al. 2003Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.; Tabosa et al. 2012Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.; Oliveira et al. 2019Oliveira LS, Andrade BO, Boldrini II, Moço CC. 2019. Aquatic vascular plants of South Brazil: checklist and a comparative floristic approach. Acta Botanica Brasilica 3: 709-715.).
The greatest species richness was found in permanent and temporary lentic ecosystems with the largest number of exclusive species (56.16 %). The stability of the water column contributed to species with different growth forms being able to colonize these ecosystems, resulting in local dominance of one or a few species and evident zonation patterns along environmental gradients from shoreline to limnetic zone border as a function of the variation in water depth (Spence 1982Spence DHN. 1982. The zonation of plants in freshwater lakes. Advances in Ecological Research 12: 37-126.; McCreary 1991McCreary NJ. 1991. Competition as a mechanism of submersed macrophyte community structure. Aquatic Botany 41:177-193.).
In the shallow coastal zone, the co-occurrence of helophytes and bottom-rooted hydrophytes constitute a stratified vegetation (Den Hartog & Segal 1964Den Hartog C, Segal S. 1964. A new classification of water-plant communities. Acta Botanica Neerlandica 13: 367-393.), related to the typically strong competition among aquatic plant species (Gopal & Goel 1993Gopal B, Goel U. 1993. Competition and allelopathy in aquatic plant communities. Botanical Reviews 59: 155-210.). And, as a greater number of species tend to co-occur at shallower depths in lentic systems of Ceará (Matias et al. 2003Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.), helophytes and bottom-rooted emergent hydrophytes, represented by the Cyperaceae, Poaceae, Fabaceae, Alismataceae and Malvaceae families, predominate along the banks of the aquatic ecosystems of the state. In the limnetic region, assemblages tend to constitute strata of free-swimming submerged forms according to a gradient of light intensity as a function of water depth (Rørslett & Agami 1987Rørslett B, Agami M.1987. Downslope limits of aquatic macrophytes: a test of the transient niche hypothesis. Aquatic Botany 29: 83-95.) and occasionally, free-floating and bottom-rooted submerged forms in the extremes of the water column (Spence 1982Spence DHN. 1982. The zonation of plants in freshwater lakes. Advances in Ecological Research 12: 37-126.).
The free-floating species showed no significant difference in the proportion of records among the aquatic ecosystems, but the proportion of free-swimming submerged and bottom-rooted emergents with floating leaves and/or stems was different between the artificial and natural lentic systems, and between natural lentic and lotic ones. Submerged plants interact intrinsically with the functioning of aquatic ecosystems, mobilizing nutrients and providing habitats for smaller dominant omnivore-planktivores (Meerhoff et al. 2003Meerhoff M, Mazzeo N, Moss B, Rodríguez-Gallego L. 2003. The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquatic Ecology 37: 377-391.). Bottom-rooted emergents with floating leaves and/or stems can occupy the entire water column, especially in shallow lakes, resulting in the vanishing of submerged plants by accumulation of organic matter in the sediment and eutrophication of the environment due to the high production of floating leaf blades (Klok & Velde 2017Klok PF, Velde G. 2017. Plant traits and environment: floating leaf blade production and turnover of Waterlilies. Peer J-the Journal of Life and Environmental Sciences 5: e3212. doi: 0.7717/peerj.3212
https://doi.org/0.7717/peerj.3212...
). Thus, these species assemblages affect, among other factors, the trophic levels of lentic ecosystems (Barko et al. 1986Barko JW, Adams MS, Clesceri NL. 1986. Environmental factors and their consideration in the management of submersed aquatic vegetation: a review. Journal of Aquatic Plant Management 24:1-10.), resulting in a wide variation of growth forms.
The assemblages that compose the artificial aquatic systems include Utricularia foliosa and Ceratophyllum demersum, both free-swimming species. The shift in water flow allows submerged plants to form extensive vegetation banks that influence the dynamics of nutrients between water and sediment (Barbosa et al. 2020Barbosa VV, Severiano JS, Oliveira DA, Barbosa JEL. 2020. Influence of submerged macrophytes on phosphorus in a eutrophic reservoir in a semiarid region. Journal of Limnology 79: 138-150.), constituting a common aspect in reservoirs of the Brazilian semiarid region. Other plants like Ludwigia helminthorrhiza, Neptunia oleracea, N. plena, Nymphaea amazonum, N. lasiophylla, N. lingulata and Nymphoides humboldtiana compose the assemblages of these systems as bottom-rooted emergents with floating leaves and/or stems. These species share a fast rate of vegetative reproduction, either by rhizomes or by stolons, so that in formations mixed with submerged macrophytes they present a pattern of relationship alternat ing between negative and positive interactions (Lycarião & Dantas 2017Lycarião TA, Dantas EW. 2017. Interactions between different biological forms of aquatic macrophytes in a eutrophic tropical reservoir in Northeastern Brazil. Revista de Biologia Tropical 65: 1095-1104.). Additionally, they are generalists, except for N. ligulata (Sousa & Matias 2013Sousa DJL, Matias LQ. 2013. A família Nymphaeaceae no Estado do Ceará. Rodriguésia 64: 049-059.), and are found in most Brazilian regions (Flora do Brasil 2020 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/. 11 Mar. 2020.
http://reflora.jbrj.gov.br/...
). Furthermore, there are fewer species in artificial systems than in natural lentic systems in Ceará state (14 or 6.39 % are common species).
On the other hand, the proportion of bottom-rooted submerged forms was different between the lentic and lotic systems, with records of the following species limited to lentic ecosystems: Eriocaulon setaceum, Cabomba haynesii, Hydrothrix gardneri, Potamogeton pusillus and all Hydrocharitaceae species, with restricted occurrence of Najas marina in permanent lentic ecosystems. Species with this growth form were not recorded in lotic systems, probably due to their vulnerability to complete their life cycle due to abiotic factors such as water currents (Power et al. 2016Power ME, Stout RJ, Cushing CE, et al. 2016. Biotic and Abiotic Controls in River and Stream Communities. Journal of the North American Benthological Society 7: 456-479.).
Aquatic plant richness is related to other environmental factors in lentic systems (Alahuhta et al. 2014Alahuhta J, Kaninen A, Hellsten S, et al. 2014. Variable response of functional macrophyte groups to lake characteristics, land use, and space: implications for bioassessment. Hydrobiologia 737: 201-214.; Ferreira et al. 2015Ferreira FS, Tabosa AB, Benvindo GR. 2015. Spatiotemporal ecological drivers of an aquatic plant community in a temporary tropical pool. Journal of Arid Environments 115: 66-72.), which makes it difficult to generalize about the diversity of these ecosystems (Bubíková & Hrivnák 2018Bubíková K, Hrivnák R. 2018. Relationships of macrophyte species richness and environment in different water body types in the Central European region Annales de Limnology-International Journal of Limnology 54: 35. doi: 10.1051/limn/2018027
https://doi.org/10.1051/limn/2018027...
). However, it is possible to observe that there is a set of exclusive species that are evolutionarily associated with these ecosystems. In this study, representatives of Nymphaeales (Cabombaceae, Nymphaeaceae), Monocotyledons (Alismataceae, Araceae, Hydrocharitaceae, Marantaceae, Potamogetonaceae, Pontederiaceae, Thyphaceae) and a few Eudicotyledons (Lentibulariaceae, Menyanthaceae, Hydroleaceae) have records limited to lentic ecosystems. Some of these families (Alismataceae, Araceae, Hydrocharitaceae, Lentibulariaceae, Pontederiaceae) have species with progressive adaptation to the aquatic environment, an evolutionary trend in monocots that is associated with vegetative differentiation more than in any other angiosperm group (Kremer & Andel 1995Kremer P, Andel J. 1995. Evolutionary aspects of life forms in angiosperm families. Acta Botanica Neerandica 44: 469-479).
In temporary lentic ecosystems, different growth forms colonize the entire water column in a space-time dynamic, i.e., these ecosystems have high species turnover (Tabosa et al. 2012Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.). Thus, the species have not only overlapping niches, but are also phylogenetically related species and tend to compete among themselves (Ferreira et al. 2015Ferreira FS, Tabosa AB, Benvindo GR. 2015. Spatiotemporal ecological drivers of an aquatic plant community in a temporary tropical pool. Journal of Arid Environments 115: 66-72.). In these environments, few families did not have records, either because they are not associated with habitat specificity or because the populations are restricted to permanent lentic ecosystems (Araliaceae, Burmanniaceae, Linderniaceae, Potamogetonaceae, Xyridaceae), reflected by a considerable number of exclusive species (45 or 20.54 % are exclusive to temporary lentic ecosystems). This shows that natural temporary lentic ecosystems contribute to the maintenance of aquatic plant richness in Ceará state, being recognized that natural ponds contributed most to regional biodiversity, supporting significantly many more species, more unique species and more rare species than other waterbody types (Williams et al. 2003Williams P, Whitfield M, Biggs J, et al. 2003. Comparative biodiversity of rivers, streams, ditches and ponds in an agricultural landscape in Southern England. Biological Conservation 115: 329-341.).
The hydrophytes that have records restricted to these ecosystems were Eichhornia heterosperma, Eichhornia paradoxa, Heteranthera rotundifolia, Heteranthera seubertiana, Lemna minuta, Utricularia hydrocarpa, and the species endemic to northeastern Brazil, Echinodorus palaefolius and Echinodorus pubescens.
In contrast, the movement of the water column in lotic ecosystems is considered a significant driver of macrophytes diversity (Lacoul & Freedman 2006Lacoul P, Freedman B. 2006. Environmental influences on aquatic plants in freshwater ecosystems. Environmental Reviews 14: 89-136; Bornette & Puijalon 2011Bornette G, Puijalon S. 2011. Response of aquatic plants to abiotic factors: a review. Aquatic Sciences 73: 1-14.) because water speed selects species with morphological adaptations like streamlined shapes, strap-like leaves or flat shoots (Chambers et al. 1991Chambers PA, Prepas EE, Hamilton HR, et al. 1991. Current velocity and its effect on aquatic macrophytes in flowing waters. Ecological Applications 1: 249-257.).Other adaptations include those that allow plants to attach firmly to the rocky substrate in rapid streams and waterfalls by specialized structures, such as disk-like holdfasts (haptera) found in Podostemaceae (Rutishauser et al. 2005Rutishauser R, Pfeifer E, Alejandro Novelo R, et al. 2005. Diamantina lombardii - an odd Brazilian member of the Podostemaceae. Flora-Morphology, Distribution, Functional Ecology of Plants 200: 245-255.), so that only Apinagia gardneriana and Mourera aspera have records limited to these ecosystems (Bubíková & Hrivnák 2018Bubíková K, Hrivnák R. 2018. Relationships of macrophyte species richness and environment in different water body types in the Central European region Annales de Limnology-International Journal of Limnology 54: 35. doi: 10.1051/limn/2018027
https://doi.org/10.1051/limn/2018027...
). In the present study, lotic ecosystems showed low values of richness and a low number of exclusive species (12 or 5.47 %).
The rivers of the semiarid region present wide variation in the water column due to rainfall irregularity, selecting species with high resistance and resilience in response to hydric disturbances (Maltchick & Pedro 2001Maltchick L, Pedro F. 2001. Responses of Aquatic Macrophytes to Disturbance by Flash Floods in a Brazilian Semiarid Intermittent Stream. Biotropica 33: 566-572.). This may influence the low number of exclusive species, which tend to present mechanisms for survival in temporary environments based on ruderal strategies, due to the desiccation of the habitat and the consequent loss of biomass during the dry season (Albuquerque et al. 2020Albuquerque AC, Rodrigues-Filho CAS, Matias LQ. 2020. Influence of climatic variables on CSR strategies of aquatic plants in a semiarid region. Hydrobiologia 847: 61-74.).
In temporary lotic systems, floods and droughts cause disturbances with different intensity, frequency and duration, determining the occurrence of aquatic communities. Therefore, species richness was lower in the puddles of the rivers and streams subject to flood events when compared to ponds (Pedro et al. 2006Pedro F, Maltchick L, Biachini Jr I. 2006. Hydrologic cycle and dynamics of aquatic macrophytes in two intermittent rivers of the semi-arid region of Brazil. Brazilian Journal of Biology 66: 575-585.). This dynamic can explain the low richness found in the temporary rivers of Ceará, with the lowest number of exclusive species (8 or 3.65 %).
Artificial lentic ecosystems showed species richness (86 spp.) close to the richness of lotic systems (83 spp.), and lower than natural lentic systems (359 spp.). Considering only the hydrophytes, the species that occupy these systems tend to be generalists (Echinodorus subalatus, Nymphaea amazonum, Neptunia plena, Ludwigia helminthorrhiza and L. leptocarpa) or species with predominant occurrence in natural lentic ecosystems with free-floating growth form (Lemna aequinoctialis, Pistia stratiotes, Spirodela intermedia, Wolffiella welwitschii), free-swimming submerged (Utricularia foliosa), bottom-rooted submerged (Cabomba haynesii, Apalanthe granatensis, Egeria densa, E. najas, Najas arguta, N. conferta, Potamogeton pusillus ) and bottom-rooted emergent forms (Echinodorus subalatus, Helanthium tenellum, Bacopa aquática, Stemodia foliosa, S. marítima, Polygonum ferrugineum and P. hispidum). These artificial systems exhibit irregular water level fluctuations related to the modifications of the reservoirs by human activity, being considered a special type of lentic environment (Hutchinson 1957Hutchinson GE. 1957. A Treatise on Limnology. New York, John Wiley & Sons.), so that only a few species with free-floating forms have records from these environments in Ceará state: Eichhornia crassipes, Lemna aequinoctialis and Spirodela intermedia. The free-floating macrophytes tend to be limited by stream speed, being common in slow-flowing streams (Grinberga 2011Grinberga L. 2011. Macrophyte species composition in streams of Latvia under different flow and substrate conditions. Estonian Journal of Ecology 60: 194-208.), or when intercepted, tend to predominate in reservoirs (Paiva et al. 2014Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.) mainly during the dry season (Lycarião & Dantas 2017Lycarião TA, Dantas EW. 2017. Interactions between different biological forms of aquatic macrophytes in a eutrophic tropical reservoir in Northeastern Brazil. Revista de Biologia Tropical 65: 1095-1104.).
Among the species that occur in all five ecosystems, P. stratiotes has a pantropical distribution, while E. subalatus, N. amazonum, N. plena, L. helminthorrhiza and L. leptocarpa are of wide distribution in Brazil (Flora do Brasil 2020 2020Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/. 11 Mar. 2020.
http://reflora.jbrj.gov.br/...
) and in the American continent (Tropicos® 2020Tropicos® - The tropics database. 2020. Missouri Botanical Garden. http://www.tropicos.org. 23 Apr. 2020.
http://www.tropicos.org...
). Some aquatic plants with wide distribution tend to present high levels of polymorphism and phenotypic plasticity related to environmental variables, allowing them to occur over a wide range of conditions (Lacoul & Freedman 2006Lacoul P, Freedman B. 2006. Environmental influences on aquatic plants in freshwater ecosystems. Environmental Reviews 14: 89-136). Wide morphological variability in populations occurring in Ceará has been described for E. subalatus (Matias 2007Matias LQ. 2007. O gênero Echinodorus (Alismataceae) no domínio da Caatinga brasileira. Rodriguésia 62: 887-900.), N. amazonum (Sousa & Matias 2013Sousa DJL, Matias LQ. 2013. A família Nymphaeaceae no Estado do Ceará. Rodriguésia 64: 049-059.) and P. stratiotes (Andrade et al. 2013Andrade IM, Mayo SJ, Silva MFS, Sousa DJL, Matias LQ, Ribeiro TA. 2013. The Araceae in Ceará, Brazil: humid forest plants in a semi-arid region. Rodriguésia 64: 445-477.), which explains how these species tend to occupy different aquatic environments.
Helophytes predominated in the aquatic systems of Ceará state, accounting for 65 % of the species. Vegetative reproduction is a predominant trait in this group, which may assure population maintenance at the ecological time scale (Li 2014Li W. 2014. Environmental opportunities and constraints in the reproduction and dispersal of aquatic plants. Aquatic Botany 118: 62-70.). These species colonize the margins of aquatic systems forming assemblages that are affected by the dynamic of the substrate and the water (Deil et al. 2011Deil U, Freiburg IBr, Germany MA, et al. 2011.The vegetation of seasonal wetlands in extratropical and orotropical South America. Phytocoenologia 41: 1-34.). In addition to cryptophytic species, annual species occupy the margins of these systems, declining when the margins are little impacted by abiotic factors (e.g. waves) or when nutrients in substrate favour an increase in biomass and establishment of perennial rhizomatous helophytes (Hernández & Rangel 2009Hernández J, Rangel JO. 2009. La vegetación del humedal de Jaboque (Bogotá, D.C.). Caldasia 31: 355-379.).
An unusual finding in this study was that only the proportions of helophytic species differed in relation to the five types of aquatic systems. Among all the factors, the interactions between terrestrial and aquatic environments can explain the distribution and abundance of aquatic plants in many interaction scenarios (Lacoul & Freedman 2006Lacoul P, Freedman B. 2006. Environmental influences on aquatic plants in freshwater ecosystems. Environmental Reviews 14: 89-136). Moreover, the organization of plant assemblages, regardless of the aquatic system type, may be influenced by biotic unpredictability, given that in arid regions ecological variability in life cycles is influenced by highly variable and unpredictable flow regimes and the impacts of land use and water resources (Choy et al. 2002Choy SC, Thomson CB, Marshall JC. 2002. Ecological condition of central Australian arid-zone rivers. Water Science and Technology 45: 225-232.).
The results showed that all waterbody types contributed to the macrophytes richness in the state, although lentic ecosystems have the highest richness values and exclusive species. So that the preservation of this flora must be considered not only for a specific type of aquatic ecosystem but for all possible types of freshwater habitats in Ceará state.
Acknowledgements
We acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for the fellowships granted to Hugo Pereira do Nascimento and Felipe Martins Guedes through the Programa Institucional de Bolsas de Iniciação Científica (PIBIC) of the Universidade Federal do Ceará.
References
- Abell R, Thieme ML, Revenga C, et al 2008. Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58: 403-414
- Alahuhta J, Kaninen A, Hellsten S, et al 2014. Variable response of functional macrophyte groups to lake characteristics, land use, and space: implications for bioassessment. Hydrobiologia 737: 201-214.
- Albuquerque AC, Rodrigues-Filho CAS, Matias LQ. 2020. Influence of climatic variables on CSR strategies of aquatic plants in a semiarid region. Hydrobiologia 847: 61-74.
- Anderson MJ, Walsh DCI. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs 83: 557-574.
- Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32 46.
- Andrade IM, Mayo SJ, Silva MFS, Sousa DJL, Matias LQ, Ribeiro TA. 2013. The Araceae in Ceará, Brazil: humid forest plants in a semi-arid region. Rodriguésia 64: 445-477.
- Barbosa VV, Severiano JS, Oliveira DA, Barbosa JEL. 2020. Influence of submerged macrophytes on phosphorus in a eutrophic reservoir in a semiarid region. Journal of Limnology 79: 138-150.
- Barko JW, Adams MS, Clesceri NL. 1986. Environmental factors and their consideration in the management of submersed aquatic vegetation: a review. Journal of Aquatic Plant Management 24:1-10.
- Bornette G, Puijalon S. 2011. Response of aquatic plants to abiotic factors: a review. Aquatic Sciences 73: 1-14.
- Bouchenak-Khelladi Y, Muasya AM, Linder HP. 2014. A revised evolutionary history of Poales: origins and diversification Botanical Journal of the Linnean Society 175: 4-16.
- Bremer K. 2002. Gondwanan evolution of the grass alliance of families (Poales). Evolution 56: 1374-1387.
- Bubíková K, Hrivnák R. 2018. Relationships of macrophyte species richness and environment in different water body types in the Central European region Annales de Limnology-International Journal of Limnology 54: 35. doi: 10.1051/limn/2018027
» https://doi.org/10.1051/limn/2018027 - Cerling TE, Ehleringer JR, Harris JM. 1998. Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philosophical Transactions of the Royal Society Series B 353: 159-171.
- Chambers PA, Prepas EE, Hamilton HR, et al 1991. Current velocity and its effect on aquatic macrophytes in flowing waters. Ecological Applications 1: 249-257.
- Chao A, Gotelli NJ, Hsieh TC, et al 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45-67.
- Choy SC, Thomson CB, Marshall JC. 2002. Ecological condition of central Australian arid-zone rivers. Water Science and Technology 45: 225-232.
- Claudino-Sales V, Peulvast JP. 2002. Dune generation and ponds on the coast of Ceará State (Northeast Brazil). In: Allison RJ. (ed.) Applied Geomorphology. Chinchester, John Wiley & Sons. p. 443-460.
- Cook CDK. 1990. Aquatic Plant Book. Amsterdam, New York, SPB Academic Publishing.
- Deil U, Freiburg IBr, Germany MA, et al 2011.The vegetation of seasonal wetlands in extratropical and orotropical South America. Phytocoenologia 41: 1-34.
- Den Hartog C, Segal S. 1964. A new classification of water-plant communities. Acta Botanica Neerlandica 13: 367-393.
- Ferreira FS, Tabosa AB, Benvindo GR. 2015. Spatiotemporal ecological drivers of an aquatic plant community in a temporary tropical pool. Journal of Arid Environments 115: 66-72.
- Flora do Brasil 2020. 2020. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/ 11 Mar. 2020.
» http://reflora.jbrj.gov.br/ - Givnish TJ, Ames M, McNeal JR, et al 2010. Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Annals of the Missouri Botanical Garden 97: 584-616.
- Goetghebeur P. 1998. Cyperaceae. In: Kubitzki K. (ed.) The families and genera of vascular plants. Volume IV: Flowering Plants - Monocotyledons: Alismatanae and Commelinanae (except Gramineae). Berlin, Heidelberg, Springer. p. 141-190.
- Gopal B, Goel U. 1993. Competition and allelopathy in aquatic plant communities. Botanical Reviews 59: 155-210.
- Grinberga L. 2011. Macrophyte species composition in streams of Latvia under different flow and substrate conditions. Estonian Journal of Ecology 60: 194-208.
- Guedes FM, Nascimento HP, Matias LC. 2016. Ambientes aquáticos diferenciados agregam específicas comunidades de plantas aquáticas?. Revista Encontros Universitários da UFC. http://www.periodicos.ufc.br/eu/article/view/17346 23 Mar. 2020.
» http://www.periodicos.ufc.br/eu/article/view/17346 - Guedes FM, Matias LQ. 2020. Flora do Ceará, Brasil: Lentibulariaceae. Rodriguésia 70: e01892018. doi: 10.1590/2175-7860202071140
» https://doi.org/10.1590/2175-7860202071140 - Hernández J, Rangel JO. 2009. La vegetación del humedal de Jaboque (Bogotá, D.C.). Caldasia 31: 355-379.
- Hsieh TC, Ma KH, Chao A. 2013. iNEXT online: interpolation and extrapolation (Version 1.0) [Software]. http://chao.stat.nthu.edu.tw/blog/software-download/ 13 Mar. 2020.
» http://chao.stat.nthu.edu.tw/blog/software-download/ - Hutchinson GE. 1957. A Treatise on Limnology. New York, John Wiley & Sons.
- Ibiapina-Santos L. 2016. Diversidade filogenética e fatores estruturantes de comunidades de plantas aquáticas em lagoas temporárias. MSc Thesis, Universidade Federal do Ceará, Fortaleza.
- Junk W, Piedade MTF, Lourival R, et al 2014. Brazilian wetlands: Definition, delineation and classification for research, sustainable management and protection. Aquatic Conservation: Marine and Freshwater Ecosystems 24: 5-22.
- Klok PF, Velde G. 2017. Plant traits and environment: floating leaf blade production and turnover of Waterlilies. Peer J-the Journal of Life and Environmental Sciences 5: e3212. doi: 0.7717/peerj.3212
» https://doi.org/0.7717/peerj.3212 - Koehler S, Bove CP. 2004. Alismatales from the Araguaia River Basin (MT/GO, Brazil). Brazilian Journal of Botany 27: 439-452.
- Kremer P, Andel J. 1995. Evolutionary aspects of life forms in angiosperm families. Acta Botanica Neerandica 44: 469-479
- Lacoul P, Freedman B. 2006. Environmental influences on aquatic plants in freshwater ecosystems. Environmental Reviews 14: 89-136
- Li W. 2014. Environmental opportunities and constraints in the reproduction and dispersal of aquatic plants. Aquatic Botany 118: 62-70.
- Lycarião TA, Dantas EW. 2017. Interactions between different biological forms of aquatic macrophytes in a eutrophic tropical reservoir in Northeastern Brazil. Revista de Biologia Tropical 65: 1095-1104.
- MacKay W. 1991. The role of ants and termites in desert communities. In: Polis G. (ed.) The ecology of desert communities. Tucson, The University of Arizona Press. p. 113-150.
- Maltchick L, Bianchini I. 2006. Hydrologic cycle and dynamics of aquatic macrophytes in two intermittent rivers of the semi-arid region of Brazil. Brazilian Journal of Biology 66: 575-585.
- Maltchick L, Pedro F. 2001. Responses of Aquatic Macrophytes to Disturbance by Flash Floods in a Brazilian Semiarid Intermittent Stream. Biotropica 33: 566-572.
- Maltchick L, Costa MAJ, Duarte MDC. 1999. Inventory of Brazilian semi-arid shallow lakes. Anais da Academia Brasileira de Ciências 71: 801-808.
- Maltchick L, Medeiros ESF. 2006. Conservation importance of semi-arid streams in north-eastern Brazil: implications of hydrological disturbance and species diversity. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 665-677.
- Mangiafico S. 2019. rcompanion: functions to support extension education program evaluation. R package version 2.2.1. https://CRAN.R-project.org/package=rcompanion 04 Mar. 2020.
» https://CRAN.R-project.org/package=rcompanion - Matias LQ, Amado RE, Nunes E. 2003. Macrófitas aquáticas da lagoa de Jijoca de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 17: 623-631.
- Matias LQ, Gonzalez HHS, Oliveria WR. 2017. Flora do Ceará: Hydrocharitaceae e as fanerógamas marinhas: Cymodoceaceae, Ruppiaceae. Rodriguésia 68: 1333-1346.
- Matias LQ, Nunes E. 2001. Levantamento florística da Área de proteção Ambiental de Jericoacoara, Ceará, Brasil. Acta Botanica Brasilica 15: 35-43.
- Matias LQ, Sousa DJL. 2011. Alismataceae no estado do Ceará, Brasil. Rodriguésia 62: 887-900.
- Matias LQ. 2007. O gênero Echinodorus (Alismataceae) no domínio da Caatinga brasileira. Rodriguésia 62: 887-900.
- McArdle BH, Anderson MJ. 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290-297.
- McCreary NJ. 1991. Competition as a mechanism of submersed macrophyte community structure. Aquatic Botany 41:177-193.
- McNeely J. 2003. Biodiversity in arid regions: Values and perceptions. Journal of Arid Environments 54: 61-70.
- Medeiros ESF, Maltchick L. 1999. The effects of hydrological disturbance on the intensity of infestation of Lernaea cyprinacea in an intermittent stream fish community. Journal of Arid Environments 43: 351-356.
- Meerhoff M, Mazzeo N, Moss B, Rodríguez-Gallego L. 2003. The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquatic Ecology 37: 377-391.
- Moro MF, Sousa DJL, Matias LQ. 2014. Rarefaction, richness estimation and extrapolation methods in the evaluation of unseen plant diversity in aquatic ecosystems. Aquatic Botany 117: 48-55.
- Moro MF, Souza VC, Oliveira-Filho AT, et al 2012. Alienígenas na sala: o que fazer com espécies exóticas em trabalhos de taxonomia florística e fitossociologia? Acta Botanica Brasilica 26: 991-999.
- Nascimento HP, Matias LQ. 2021. Flora do Ceará, Brasil: Onagraceae. Rodriguésia 72: e01732019. doi: 10.1590/2175-7860202172029
» https://doi.org/10.1590/2175-7860202172029 - Normando LRO. 2011. Fatores espaço-temporais e riqueza de macrófitas aquáticas de lagoas temporárias do semiárido do Brasil. MSc Thesis, Universidade Federal do Ceará, Fortaleza.
- Ogle DH, Wheeler P, Dinno A. 2020. FSA: fisheries stock analysis. R package version 0.8.30. https://github.com/droglenc/FSA 20 May 2020.
» https://github.com/droglenc/FSA - Oksanen J, Blanchet FG, Friendly M, et al 2019. Vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan 10 May 2020.
» https://CRAN.R-project.org/package=vegan - Oliveira LS, Andrade BO, Boldrini II, Moço CC. 2019. Aquatic vascular plants of South Brazil: checklist and a comparative floristic approach. Acta Botanica Brasilica 3: 709-715.
- Paiva JRA, Matias LQ, Martins FR, Becker H. 2014. Does distance between aquatic plant assemblages matter in defining similarity between them during high water-level periods. Lakes and Reservoirs: Research and Management 19: 37-45.
- Pedro F, Maltchick L, Biachini Jr I. 2006. Hydrologic cycle and dynamics of aquatic macrophytes in two intermittent rivers of the semi-arid region of Brazil. Brazilian Journal of Biology 66: 575-585.
- Power ME, Stout RJ, Cushing CE, et al 2016. Biotic and Abiotic Controls in River and Stream Communities. Journal of the North American Benthological Society 7: 456-479.
- R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ 25 May 2020.
» https://www.R-project.org/ - Rodríguez-Arias CE, Benavides AMS. 2016. Vegetación acuática de los humedales de la microcuenca alta de la quebrada Estero, San Ramón de Alajuela, Costa Rica. Brenesia 85/86: 9-20.
- Rørslett B, Agami M.1987. Downslope limits of aquatic macrophytes: a test of the transient niche hypothesis. Aquatic Botany 29: 83-95.
- Rutishauser R, Pfeifer E, Alejandro Novelo R, et al 2005. Diamantina lombardii - an odd Brazilian member of the Podostemaceae. Flora-Morphology, Distribution, Functional Ecology of Plants 200: 245-255.
- Sculthorpe CD. 1967. The biology of aquatic plants. London, Edward Arnold.
- Sieben EJ, Morris CD, Kotze DC, et al 2010. Changes in plant form and function across altitudinal and wetness gradients in the wetlands of the Maloti-Drakensberg, South Africa. Plant Ecology 207: 107-119.
- Silva IC, Bove CP, Koschnistzche C. 2015. Plantas de corredeiras: reprodução e conservação de Podostemaceae. Natureza on Line (Espírito Santo) 13: 6-11.
- Silva LAC, Araujo RCP, Maia LP, et al 2007. Zoneamento ecológico-econômico da zona costeira do Estado do Ceará. Annais do XLV Congresso da Sociedade Brasileira de Sociologia, Administração e Economia Rural. Londrina, SOBER. p. 1-20.
- Sokal RR, Rohlf FJ. 1995. Biometry. 3rd. edn. New York, W. H. Freeman and Company.
- Sousa DJL, Campelo MJA, Matias LQ. 2018. Flora do Ceará: Pontederiaceae. Rodriguésia 69: 1641-1657.
- Sousa DJL, Matias LQ. 2013. A família Nymphaeaceae no Estado do Ceará. Rodriguésia 64: 049-059.
- Spence DHN. 1982. The zonation of plants in freshwater lakes. Advances in Ecological Research 12: 37-126.
- Tabosa AB, Matias LQ, Martins FR. 2012. Live fast end die young: The aquatic macrophyte dynamics in a temporary pool in the Brazilian semiarid region. Aquatic Botany 102: 71-78.
- Tropicos® - The tropics database. 2020. Missouri Botanical Garden. http://www.tropicos.org 23 Apr. 2020.
» http://www.tropicos.org - Wetzel RG. 2001. Limnology. San Diego, Academic Press.
- Williams P, Whitfield M, Biggs J, et al 2003. Comparative biodiversity of rivers, streams, ditches and ponds in an agricultural landscape in Southern England. Biological Conservation 115: 329-341.
Publication Dates
-
Publication in this collection
16 Aug 2021 -
Date of issue
Jan-Mar 2021
History
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Received
19 May 2020 -
Accepted
19 Nov 2020