Plant Distribution in Freshwater Wetlands of the Brazilian Subtropical Highland Grasslands

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Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands

Article in Brazilian Journal of Botany · March 2016 DOI: 10.1007/s40415-015-0226-y

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Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands

1 1 Tatiana Lobato de Magalhaes • Roseli Lopes da Costa Bortoluzzi • Adelar Mantovani1

Received: 8 May 2015 / Accepted: 1 October 2015 Ó Botanical Society of Sao Paulo 2015

Abstract Wetlands are heterogeneous environments that Keywords Aquatic macrophytes Á Banhados Á harbor several species. In spite of playing a key role in Biodiversity conservation Á Inner and outer zones Á aquatic ecosystems, macrophytes are the most neglected Protected areas group in limnological studies. In the Brazilian subtropical highland grasslands, freshwater wetlands occur intermingled with native grasslands. Our objective was to assess Introduction species richness and variation in floristic composition along transects. We sampled 324 units to compare floristic Wetlands represent an interface between aquatic and ter- similarity between and within areas based on non-metric restrial systems, as they harbor species adapted to both multidimensional scaling (NMDS). We recorded plants of environments and have high biodiversity (Baptista et al. 40 families, 88 genera, and 133 species, out of which 17 2012). Their biota includes endangered, endemic, and eco- are endangered. The richest families were Poaceae, nomically important species (Pott and Pott 2000). Although Cyperaceae, and Asteraceae. The life forms found included freshwater wetlands cover only 0.01 % of the Earth’s sur- amphibious, emergent, and fixed submerged types. The face, they harbor approximately 10 % of all animal species NMDS pointed to dissimilarity between and within areas. and 1 % of all described vascular plant species (Balian et al. We observed the formation of two zones. In the outer zone, 2008). Approximately 20 % of tropical South America is we detected seven indicator species and 17 exclusive spe- estimated to be occupied by freshwater wetlands, including cies. In the inner zone, we detected five indicator species flooded forests and grasslands (Junk 1993). Brazil has one of and 29 exclusive species. Our study suggests that wetlands the largest hydrologic networks in the world, which includes are species-rich, heterogeneous environments characterized permanent, seasonal, lacustrine, and fluvial aquatic ecosys- by different zones. The knowledge of biodiversity and tems (Bove et al. 2003). presence of indicator species is key to the elaboration of Aquatic environments are usually heterogeneous (San- strategies for the restoration and conservation of freshwater tamaria & Van Vierssen 1997). This heterogeneity is wetlands. associated with water filtering and retention and also with plant species diversity (Junk 2002). In spite of playing a key role in aquatic ecosystems, by providing food and habitat for many organisms (Balian et al. 2008), aquatic macrophytes are the most neglected group in limnological studies (Esteves 1998). In general, they are species with broad geographic distribution (Santamaria and Van Viers- & Tatiana Lobato de Magalhaes sen 1997) that have different levels of flooding tolerance. [email protected] Adaptations to aquatic environment determine the life form of aquatic macrophytes and may explain the formation of 1 Graduate School in Plant Production, Santa Catarina State University, Av. Luis de Camo˜es, 2090, Lages, different ecological niches in wetlands (Rocha and Martins Santa Catarina, Brazil 2011). 123 T. L. de Magalhaes et al.

The region of Brazilian subtropical highland grasslands and 324 sampling units. To assess the location of plants, we is locally known as campos de cima da serra. This region is set up inward transects, length = 30 cm (Fig. 1). We car- located between the states of Santa Catarina and Rio ried out the floristic inventory in 1 9 1 m sampling units Grande do Sul, southern Brazil, and harbors highly diverse arranged on the transects and systematically moved to the wetlands (Baptista et al. 2012) and endemic species (Iganci right and left of the central line of the transect. The et al. 2011). The wetlands of this region are locally known beginning of the wetland was delimited by the occurrence as banhados and occur intermingled with native grasslands of aquatic plants and the presence of hydromorphic soils. (Schaefer-Santos et al. 2013). They are very common in the We photographed plants in the field, collected, and region and, sometimes, occur associated with forest frag- identified them, and later deposited the vouchers in the ments, forming a heterogeneous mosaic. Wetlands are Lages Herbarium (LUSC) at the Santa Catarina State systems of conservation concern (Baptista et al. 2012). University. We identified plant species by consulting the However, they are susceptible to anthropogenic action specialized literature and specialists in different taxonomic (drainage, damming, and burn), especially due to the groups. Then, we confirmed species identification in her- expansion of agriculture and livestock farming in the baria of southern Brazil: Barbosa Rodrigues Herbarium region. Information on vegetation biodiversity and spatial (HBR), Federal University of Rio Grande do Sul Herbar- distribution in those wetlands is fundamental for the ium (ICN), and Federal University of Santa Catarina Her- establishment of conservation strategies, as well as for barium (FLOR). Nomenclature followed the Species List planning their sustainable use. Hence, our objective was to of the Brazilian Flora (Lista de Espećies da Flora do Brasil assess species richness and variation in floristic composi- 2014). The classification of life forms of aquatic macro- tion along transects in three wetlands located in the phytes followed Irgang et al. (1984): amphibious (lives on Southern Plateau of Santa Catarina, within the Brazilian the bank and tolerates dry seasons), emergent (is rooted to subtropical highland grasslands. the substrate with a vegetative/reproductive part emerging from the water), epiphyte (grows on another plant), fixed Materials and methods floating (floats on the surface, but is rooted in the substrate), fixed submerged (a submerged plant, rooted in the The region of the Brazilian subtropical highland grasslands substrate), free floating (floats on the surface, but is not belongs to the Atlantic Forest (Iganci et al. 2011, Boldrini rooted in the substrate), and free submerged (is submerged, et al. 2009). Its altitudes vary between 800 and 1600 m but not rooted in the substrate). We analyzed species a.s.l. The local vegetation is predominantly composed of conservation status from two perspectives: extinction risk grasses and classified as campos de altitude (montane grasslands), but also includes remnants of a mixed rain- forest, also known as arauca´ria forest. The average tem- peratures in winter and summer are 10.5 and 17.5 °C, respectively, and the climate is classified as a subtropical, type Cfb in the Ko¨ppen system. The average annual rainfall of 1600 mm is evenly distributed throughout the year (Andrade et al. 2008, INMET 2014). The banhados, classified as wetlands by several bota- nists, occur within natural grasslands and are considered permanently protected areas (Santa Catarina 2009). The predominant soils in these wetlands are Gleysols and Organosols, which are hydromorphic soils, typical of areas with water saturation that retain large deposits of organic matter (Almeida et al. 2007). We selected three wetlands areas: Area 1, in Bom Jardim da Serra (28°1905400S– 49°4004600W; 1213 m a.s.l.); Area 2, in Lages, locality of Coxilha Rica (28°1701800S–50°3204600W; 989 m a.s.l.); and Area 3, in Painel (27°5900800S-50°0505800W; 1252 m a.s.l.). The three study areas are located within private properties, where natural grasslands occur, and the water depth in the wetlands varies between 0–20 cm. Data collection was carried out in January and February 2012 (blossom season). In total, we sampled 12 transects Fig. 1 Example of the inward transect 123 Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands and species listed as indicators of preserved environments. and Juncus L. (four species). The life forms found among We analyzed the conservation status of each species based aquatic macrophytes were amphibious (91 species), emer- on the National Official List of Threatened Flora Species gent (28), and fixed submerged (14). We observed 17 (MMA 2014) and the Red List of Threatened Species threatened species in the National Official List of Threat- (IUCN 2015). For species listed as indicators of preserved ened Flora Species, in the categories ‘‘least concern’’ (7), environments, we used the official lists of the Brazilian ‘‘endangered’’ (4), ‘‘vulnerable’’ (2), and ‘‘near threatened’’ environmental agencies (Santa Catarina 2009, Brasil (1). We also observed three species listed in the IUCN 2010). categories of The International List of Threatened Species We analyzed floristic composition with descriptive (Table 1). statistics, using the data gathered by family, genus, and The three studied areas showed similar richness indexes: species. We analyzed species richness using total number 67 (Area 1), 68 (Area 2), and 58 species (Area 3). Forty- of species, number of species per sampling unit, diversity three species occurred simultaneously in two areas, and 17 indices (Shannon, Simpson, and Log-Alpha), and richness species occurred simultaneously in three areas. These 17 estimators (Jack1, Jack2, Chao, and Boot indices), fol- species belong to the families Cyperaceae (four species), lowing Borcard et al. (2011). We measured abundance as Asteraceae (three species), Poaceae, Juncaceae (two spe- the total number of individual plants inside the sampling cies each), Araliaceae, Lythraceae, Mayacaceae, Poly- units. We did not measure abundance for clonal individu- galaceae, Valerianaceae, and Verbenaceae (one species als. We considered clonal the species that formed clumps each). The three areas showed similar values of Shannon or that had no isolated occurrence (e.g., species of Poaceae, diversity index. The minimum richness per sampling unit Cyperaceae, Juncaceae, and bryophytes in general). We was 21 species, and the maximum, 32 species (Table 2). calculated relative density based on the total number of The rarefaction curves tended to stabilization and individuals of each species in the sampling units, and rel- reached a low increment rate (Fig. 2), which indicates ative frequency as the occurrence of species in the sam- sufficient sampling. The species abundance distribution pling units (Krebs 1999). We analyzed floristic similarity showed an exponentially decreasing curve for all three between areas with a non-metric multidimensional scaling studied areas. The most frequent families were Cyperaceae (NMDS), based on the Sorensen distance, as proposed by and Poaceae, whereas the most frequent species were Borcard et al. (2011). We used the same ordination analysis Floscopa glabrata (Kunth) Hassk., Leptostelma maxima D. to compare floristic composition among study areas and Don, Pycreus niger (Ruiz and Pav.) Cufod, and Rhyn- within each area, by assessing variation in inward transects. chospora corymbosa (L.) Britton. We calculated the indicator species index (Indval) The NMDS (k = 3) evidenced a clear difference in (Dufrene and Legendre 1997) to detect indicator species of floristic composition among areas (Fig. 3a), which we also outer and inner zones. We considered indicator species any observed when analyzing species abundance data using the biological species that defines a trait or characteristic of the same method. In the NMDS (k = 2) within areas, we environment and whose relationship between species observed species grouping after seven meters of sampling occurrence/abundance and groups of sites is significant. and the formation of two zones: inner and outer. The outer All analyzes were carried out in the open source soft- zone comprises the initial sampling units up to the seventh ware R, version 2.13.1, using the Biodiversity, Indic- meter, and the inner zone comprises the sampling units species, and Vegan packages (Borcard et al. 2011;R allocated from the seventh meter on (Fig. 3b–d). Development Core Team 2013). Among the indicator species (P \ 0.001; IndVal [ 0.5), seven were considered indicators of the outer zone and five of the inner zone. Seventeen species were exclusive to the Results outer zone and 29 to the inner zone. In the outer zone, we observed eight species of preserved environments (seven Our floristic inventory resulted in 133 species: five bryo- exclusive and one indicator) and three threatened species phytes, two pteridophytes, and 116 angiosperms of 40 (two exclusive and one indicator). In the inner zone, we families and 88 genera. The richest families were Poaceae observed nine typical species of preserved environments, (25 species), Cyperaceae (21 species), and Asteraceae (20 five threatened, and one endemic to the Brazilian Sub- species). Most families (48 %) and genera (60 %) were tropical Highland Grasslands (all species exclusive to the represented by a single species. The genera that comprised inner zone) (Table 3). the largest number of species belonged to the families The species identified as indicators of the outer zone Cyperaceae, Asteraceae, Iridaceae, and Juncaceae. They showed emergent (two) and amphibious life forms (five), were Eleocharis R. Br. (seven species), Rhynchospora whereas those identified as indicators of the inner zone Vahl., Baccharis L., Sisyrinchium L. (five species each), showed fixed submerged (four) and amphibious life forms 123 T. L. de Magalhaes et al.

Table 1 List of presence (bold) and absence (empty cell) of species according to site (Area 1 = Bom Jardim da Serra, Area 2 = Lages, Area 3 = Painel), life form (LF life form, E emergent, A amphibious, FS Fixed submerged), conservation status (CS conservation status, LC least concern, EN endangered, NT nearly threatened, VU vulnerable, IUC IUCN’s Red List of Threatened Species), and occurrence parameters (RD relative density, RF relative frequency) Family Taxon Voucher LF CS Area 1 Area 2 Area 3 RD RF RD RF RD RF

Alismataceae Echinodorus grandiflorus (Cham. & Schltr.) Micheli 112 E 1.73 41.1 Alismataceae Echinodorus tenellus (Mart.) Buchenau 113 E 1.35 12.5 Apiaceae Eryngium floribundum Cham. & Schltdl. 118 A 0.63 12.5 Apiaceae Eryngium mesopotamicum Pedersen 116 A 0.06 1.79 3.37 46.4 Araliaceae Hydrocotyle ranunculoides L. f. 121 FS – 16.1 – 19.6 – 23.2 Asteraceae Achyrocline alata (Kunth) D. C. 161 E 0.22 5.36 Asteraceae Achyrocline satureioides (Lam.) D. C. 150 A 0.17 3.57 Asteraceae Baccharis breviseta D. C. 162 A 4.01 67.9 Asteraceae Baccharis crispa Spreng. 143 A 0.36 12.5 2.57 51.8 0.51 10.71 Asteraceae Baccharis megapotamica Spreng. 139 A LC 2.42 48.2 0.12 3.57 0.67 14.3 Asteraceae Baccharis cf. organensis Baker 153 A 0.72 16.1 Asteraceae Baccharis spicata (Lam.) Baill 146 A 0.18 1.79 Asteraceae Campovassouria cruciata (Vell.) R. M. King & H. Rob 395 A 0.05 1.79 Asteraceae Chrysolaena simplex (Less.) Dematt. 130 A 0.05 1.79 Asteraceae Eupatorium serratum Spreng. 133 A 0.18 7.14 0.78 21.4 3.14 44.6 Asteraceae Gamochaeta americana (Mill.) Wedd. 149 A 0.24 7.14 Asteraceae Leptostelma catharinensis (Cabrera) A. Teles & Sobral 127 A EN 1.12 25.0 Asteraceae Leptostelma maxima D. Don 124 A 8.48 88.9 1.74 25.0 Asteraceae Lessingianthus glabratus (Less.) H. Rob. 131 A 0.09 3.57 Asteraceae Senecio brasiliensis (Spreng.) Less. 398 A 0.06 1.79 Asteraceae Solidago chilensis Meyen 154 A 0.04 1.79 Asteraceae Stevia veronicae D. C. 156 A 0.94 19.6 0.06 1.79 1.80 21.4 Asteraceae Symphyotrichum graminifolium (Spreng.) G. L. Nesom 160 A 0.22 7.14 Asteraceae Trixis lessingii D. C. 126 A 1.50 33.9 Bartramiaceae Breutelia subtomentosa (Hampe) A. Jaeger 389 FS – 1.79 Begoniaceae Begonia cucullata var. cucullata Willd. 164 A 0.01 1.79 Blechnaceae Blechnum schomburgkii (Klotzsch) C. Chr. 330 A 0.05 1.79 Campanulaceae Lobelia hederacea Cham. 367 FS NT 2.09 17.9 Campanulaceae Siphocampylus verticillatus (Cham.) G. 358 E LC 0.73 35.7 Commelinaceae Floscopa glabrata (Kunth) Hassk. 167 A 5.68 73.2 Cyperaceae Ascolepis brasiliensis (Kunth) Benth. ex C.B. Clarke 206 A – 10.7 – 7.14 – 62.5 Cyperaceae Carex polysticha Boeckeler 201 A – 39.3 Cyperaceae Carex purpureovaginata Boeckeler 377 A – 1.79 Cyperaceae Cyperus haspan L. 168 A – 51.8 – 26.8 – 35.7 Cyperaceae Cyperus reflexus Vahl 171 A – 3.57 Cyperaceae Eleocharis contracta Maury 185 E – 41.1 Cyperaceae Eleocharis maculosa (Vahl) Roem. & Schult 209 E – 35.7 Cyperaceae Eleocharis montana (Kunth) Roem. & Schult 183 E – 35.7 – 10.7 Cyperaceae Eleocharis niederleinii Boeckeler 211 E – 23.2 Cyperaceae Eleocharis rabenii Boeckeler 210 E – 1.79 Cyperaceae Eleocharis sellowiana Kunth 180 E IUC – 8.93 Cyperaceae Eleocharis subarticulata (Nees) Boeck 181 E – 14.3 Cyperaceae Lipocarpha humboldtiana Nees 198 A – 16.1 – 5.36 Cyperaceae Pycreus niger (Ruiz & Pav.) Cufod 177 A – 91.1 – 35.7 – 16.1 Cyperaceae Pycreus unioloides (R. Br) Urb 173 A – 44.6 – 8.93 – 7.50

123 Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands

Table 1 continued Family Taxon Voucher LF CS Area 1 Area 2 Area 3 RD RF RD RF RD RF

Cyperaceae Rhynchospora corymbosa (L.) Britton 191 A IUC – 7.14 – 80.4 Cyperaceae Rhynchospora emaciata (Nees) Boeckeler 194 A – 3.07 Cyperaceae Rhynchospora marisculus Lindl. & Nees 189 A – 16.7 – 10.7 Cyperaceae Rhynchospora rugosa sub. americana (Vahl) Gale 187 A – 5.36 – 10.7 Cyperaceae Rhynchospora tenuis Link 195 A LC – 1.79 Cyperaceae Sclerial leptostachya Kunth 196 A – 7.14 Dicranaceae Atractylocarpus brasiliensis (Mu¨ll. Hal.) R. S. Williams 361 FS – 1.79 – 7.14 Dicranaceae Campylopus occultus Mitt. 385 FS – 1.79 Eriocaulaceae Eriocaulon ligulatum (Vell.) L. B. Sm 212 A 0.63 14.3 3.59 60.7 Eriocaulaceae Syngonanthus caulescens var. caulescens (Poir.) 215 A LC 0.90 8.93 Ruhland Hydrolaceae Hydrolea spinosa var. paraguayensis (Chodat) L. 166 E 0.66 14.3 J. Davenp. Hypericaceae Hypericum rigidum A. St.-Hil. 266 A 0.42 12.5 Hypnaceae Isopterygium tenerifolium Mitt. 363 FS – 5.36 Iridaceae Phalocallis coelestis (Lehm.) Ravenna 224 E 1.07 28.6 Iridaceae Sisyrinchium cf. luzula Klotzsch ex Klatt 218 A 0.73 16.1 Iridaceae Sisyrinchium cf. pachyrhizum Baker 222 A 0.18 3.57 Iridaceae Sisyrinchium cf. pendulum Ravenna 219 A 0.49 8.93 Iridaceae Sisyrinchium micranthum Cav. 223 A 0.28 5.36 Iridaceae Sisyrinchium vaginatum cf. var. marchioden Spreng. 221 A 0.06 1.79 Juncaceae Juncus effusus L. 229 E IUC – 25.0 Juncaceae Juncus microcephalus Kunth 226 E – 62.5 – 41.1 – 37.7 Juncaceae Juncus ramboi Barros 230 E – 7.14 Juncaceae Juncus scirpoides Lam. 380 E – 41.1 – 28.6 – 28.6 Lamiaceae Cunila galioides Benth. 237 A 0.36 7.14 Lamiaceae Hyptis lappulacea Mart. ex Benth. 236 A 0.28 5.36 Lamiaceae Prunella vulgaris L. 234 A 0.36 8.93 Lamiaceae Salvia procurrens Benth. 240 A 0.09 3.57 2.93 66.1 Lentibulariaceae Utricularia tridentata Sylveń 242 FS VU 0.24 3.57 0.17 3.57 Lythraceae Cuphea ingrata Cham. & Schltdl. 248 A 0.63 17.9 3.53 58.9 0.56 14.3 Lythraceae Cuphea lindmaniana Bacig. 251 A EN 0.13 3.57 0.73 14.3 Mayacaceae Mayaca sellowiana Kunth 254 FS – 17.9 – 5.36 – 25.0 Melastomataceae Tibouchina cerastifolia Cogn. 260 A 0.06 1.79 Melastomataceae Tibouchina gracilis (Bonpl.) Cogn. 257 A 0.96 21.4 0.84 10.7 Myrsinaceae Lysimachia filiformis (Cham. & Schltdl.) U. Manns & 369 FS – 21.4 Anderb. Onagraceae Ludwigia longifolia (D. C.) H. Hara 261 A 4.52 64.3 Onagraceae Ludwigia sericea (Cambess.) H. Hara 264 A 5.08 64.3 1.29 25.0 Onagraceae Ludwigia sp. L. 115 E 0.31 7.14 Orchidaceae Habenaria macronectar (Vell.) Hoehnell 274 E 0.12 3.57 Orchidaceae Habenaria montevidensis Spreng. 269 E 0.22 7.14 Orchidaceae Habenaria repens Nutt. 272 E 0.40 8.93 0.90 8.93 Orobanchaceae Buchnera longifolia Kunth 348 E LC 0.05 1.79 Orobanchaceae Stemodia stricta Cham. & Schltdl. 346 E 0.05 1.79 Plantaginaceae Mecardonia procumbens var. flagellaris (Cham. & 364 FS – 12.5 Schltdl.) V. C. Souza Poaceae Agrostis hygrometrica Nees 307 A – 14.3 – 10.71

123 T. L. de Magalhaes et al.

Table 1 continued Family Taxon Voucher LF CS Area 1 Area 2 Area 3 RD RF RD RF RD RF

Poaceae Agrostis lenis Roseng. et al. 304 A VU – 10.7 – 14.3 – 3.57 Poaceae Andropogon lateralis Nees 287 A – 64.3 – 46.4 – 41.1 Poaceae Andropogon macrothrix Trin 295 A – 12.5 Poaceae Andropogon virgatus Desv. 290 A – 8.93 Poaceae Axonopus compressus (Sw.) P. Beauv. 284 A – 3.57 Poaceae Axonopus fissifolius (Raddi) Kuhlm 283 A – 1.79 – 8.93 Poaceae Axonopus ramboi G. A. Black 278 A EN – 1.79 Poaceae Briza calotheca (Trin.) Hack. 317 A – 26.8 – 30.4 Poaceae Calamagrostis longiaristata (Wedd.) Hack. Ex Sodiro 308 A – 8.93 – 17.9 Poaceae Deschampsia caespitosa (L.) P. Beauv. 313 A EN – 33.9 Poaceae Dichanthelium sabulorum var. polycladum (Ekman) 282 A – 41.1 Zuloaga Poaceae Eriochrysis cayennensis P. Beauv. 299 E – 8.93 – 21.4 Poaceae Eriochrysis villosa Swallen 300 E – 35.7 Poaceae Glyceria multiflora Steud. 310 A – 48.2 Poaceae Holcus lanatus L. 298 A – 5.36 Poaceae Panicum schwackeanum Mez. 280 A – 28.6 Poaceae Paspalum dilatatum var. dilatatum Poir. 277 A – 1.79 Poaceae Paspalum exaltatum J. Presl. 276 A – 5.36 Poaceae Paspalum urvillei Steud. 279 A – 3.57 Poaceae Saccharum asperum (Nees) Steud. 294 A – 1.79 Poaceae Saccharum villosum Steud. 291 A – 1.79 Poaceae Sacciolepis vilvoides (Trin.) Chase 303 A – 21.4 – 12.5 Poaceae Sorghastrum nutans (L.) Nash 296 A – 5.36 Poaceae Sporobolus indicus (L.) R. Br. 312 A – 16.1 Polygalaceae Monnina tristaniana A. St.-Hil. & Moq. 319 E – 12.5 Polygonaceae Polygala linoides Poir. 321 A – 23.2 – 1.79 – 5.36 Polygonaceae Polygonum acuminatum Kunth 328 A – 3.57 Polygonaceae Polygonum meisnerianum Cham. 324 A – 1.79 – 28.6 –– Pottiaceae Leptodontium viticulosoides (P. Beauv.) Wijk & Marg. 392 FS 0.05 1.79 Ranunculaceae Ranunculus flagelliformis Sm. 373 FS 1.79 16.1 Rubiaceae Galianthe centranthoides (Cham. & Schltdl.) E. 335 A 0.63 21.4 L. Cabral Rubiaceae Galium equisetoides (Cham. & Schltdl.) Standl. 332 A LC 0.22 7.14 1.08 26.8 Rubiaceae Galium humile Cham. & Schltdl. 334 A LC 0.04 1.79 Rubiaceae Hedyotis thesiifolia (A. St.-Hil.) K. Schum. 370 FS 2.86 19.6 Sphagnaceae Sphagnum recurvum P. Beauv. 337 FS – 1.79 – 14.3 Thelypteridaceae Thelypteris interrupta (Willd.) K. Iwats. 357 E 1.44 28.6 Thelypteridaceae Thelypteris opposite var. rivolorum (Vahl) Ching 356 E 0.81 14.3 Valerianaceae Valeriana salicariifolia Vahl 339 A 2.19 51.8 1.67 32.1 1.74 32.1 Verbenaceae Glandularia corymbosa (Ruiz and Pav.) O’Leary and P. 232 A 0.27 8.93 Peralta Verbenaceae Glandularia hassleriana (Briq.) Tronc. 344 A 0.04 1.79 Verbenaceae Verbena alata Otto ex Sweet 233 A 0.90 19.6 0.06 1.79 0.22 5.36 Xyridaceae Xyris jupicai Rich. 352 A 0.22 7.14 2.36 39.3 Xyridaceae Xyris laxifolia Mart. 350 A 0.42 10.7

123 Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands

Table 2 Estimated richness, Area Estimated richness Observed richness Diversity maximum and minimum richness per sampling unit 2 2 1 Jack 1 67.9 Smallest (1 m )21Shannon 3.32 (1 m ), and diversity index per 2 study area Jack 2 68.0 Largest (1 m )31Simpson 0.94 Chao 65.0 Total (area) 67 Logalpha 11.8 Boot 65.3 2 Jack 1 65.9 Smallest (1 m2)23Shannon 3.53 Jack 2 67.9 Largest (1 m2)30Simpson 0.96 Chao 63.3 Total (area) 58 Logalpha 11.7 Boot 61.8 3 Jack 1 67.9 Smallest (1 m2)23Shannon 3.62 Jack 2 69.0 Largest (1 m2)32Simpson 0.96 Chao 66.1 Total (area) 68 Logalpha 12.7 Boot 65.8 Global Jack 1 144.9 Smallest (1 m2)21Shannon 4.09 Jack 2 149.9 Largest (1 m2)32Simpson 0.97 Chao 141.9 Total (area) 133 Logalpha 23.92 Boot 138.0

zone are important to help characterize the boundaries of wetlands. This information will be useful for the conservation of protected areas and land-use planning in agree- ment with the environmental law. We consider our sampling sufficient based on rarefaction curves, which tended to stabilization, and richness estimate calculations, which resulted in similar values as observed in the field. The global diversity index found can be considered high (Shannon = 4.09). Eugenio et al. (2011) published similar data (Shannon = 3.81 and 3.57), in the wetlands of western Brazil. The species accumula- tion curves showed classic concave forms, hollow curves, or inverted ‘‘J.’’ Many families (40 %) and genera (64 %) were represented by single species, which is a common pattern for preserved areas. Moreira et al. (2011) found similar results (51.6 and 65.3 %) in a savanna vegetation that grows in riparian forests. That vegetation has hydromorphic soils and palm trees within a shrubby-herbaceous Fig. 2 Rarefaction curve of the sampling vegetation surrounded by grasslands and is locally known as vereda. According to Prado (2009), the dominance of few species is one of the laws of ecology, and to understand (one; Fig. 4a). We observed a similar difference between species abundance distributions we need to look into the the outer and inner zones in terms of the life forms of non- causes of rarity. This type of abundance distribution occurs exclusive species: most were amphibious, followed by in preserved areas or areas that suffer few impacts, where emergent and fixed submerged (Fig. 4b). the vegetation is in balance. The occurrence of species of the genera Sphagnum, Habenaria, and Blechnum is typical of preserved environments (Brasil 2010, Magalhaes et al. Discussion 2013). In addition, the occurrence of endangered species is also typical of preserved areas, which we observed in the Our study pointed out that wetlands show floristic varia- outer and inner zones. tion, with outer and inner zones. Some species are zone The families Asteraceae, Cyperaceae, and Poaceae indicators, some others are typical of preserved areas, and scored the largest number of species occurrence in other some are threatened. The indicator species of the outer wetlands’ studies (Ferreira et al. 2010, Rolon et al. 2010,

123 T. L. de Magalhaes et al.

Fig. 3 NMDS ordination a among areas 1, 2, and 3; b between the outer and inner zones of Area 1; c between the outer and inner zones of Area 2; and d between the outer and inner zones of Area 3

Alves et al. 2011, Moreira et al. 2011). In our study, species were found in the outer zone (B7 m from the outer Cyperaceae and Poaceae were not only the richest families, limit). Alves et al. (2011) and Murray-Hudson et al. (2012) but also the most abundant. Many species of Cyperaceae obtained similar results in other wetlands. The species are typical of wetlands and show morphological adapta- found in the outer zone represented 74 % of the total of tions to survive in flooded environments (Rocha & Martins species sampled in our study. In studies carried out in 2011). wetlands of Florida, USA, Murray-Hudson et al. (2012) Santamaria and Van Vierssen (1997) proposed that established as the outer zone the area comprised by the first aquatic species tend to have broader distribution than ter- five meters of the wetland. They observed that inward restrial plants. Three species recorded in the present study transects reached sampling sufficiency, as the outer and were listed as semi-cosmopolitan: Juncus effusus L., intermediate zones concentrated most species. Rhynchospora corymbosa (L.) Britton, and Thelypteris Alves et al. (2011) stated that this heterogeneity results interrupta (Willd.) K. Iwats (Irgang and Gastal Juńior from water-level variation. They explain that the occurrence 2003). They were also included in the international list of of amphibious species is higher in the outer zone because this threatened species (IUCN 2015). Furthermore, Baccharis zone works as an interface between aquatic and terrestrial spicata (Lam.) Baill was cited as a macroendemic species environments. We observed this pattern in our study, as most (Irgang and Gastal Juńior 2003), whereas Calamagrostis indicator species of the outer zone showed the fixed sub- longiaristata (Wedd.) Hack. ex Sodiro, Leptostelma merged life form. This pattern probably occurs because the catharinensis (Cabrera) A.Teles & Sobral, and Syngonan- species occurring in the outer zone have higher phenotypical thus caulescens (Poir.) Ruhland were listed as endemic to plasticity and can adapt themselves to hydromorphic envi- the Brazilian Subtropical Highland Grasslands (Iganci et al. ronments. The indicator species of the inner zone were 2011). mostly short-sized (\10 cm in height), such as Hedyotis The comparison among sampling units located on thesiifolia (A. St.-Hil.) K. Schum., Lysimachia filiformis transects through NMDS showed the formation of clusters (Cham. and Schltdl.) U. Manns and Anderb., Mayaca sel- in the units located in the center of the wetland, in the three lowiana Kunth, and Ranunculus flagelliformis Sm. This study areas. The accumulated richness showed that most pattern can be related to a greater submersion due to the

123 Plant distribution in freshwater wetlands of the Brazilian subtropical highland grasslands

Table 3 Indicator and Species Outer zone Inner zone Life form Habit Conservation status exclusive species of the outer zone and inner zone associated Achyrocline alata Exclusive E SS PA with the site of occurrence, life form (A amphibious, Achyrocline satureioides Exclusive A SS PA E emergent, FS Fixed Agrostis lenis Exclusive A H PA/VU submerged), habit (S shrubby, Andropogon virgatus Exclusive A H PA H herbaceous, SS subshrub), and Ascolepis brasiliensis Exclusive A H conservation status (PA indicator of preserved area, End Atractylocarpus brasiliensis Exclusive FS H endemic to the Brazilian Axonopus compressus Exclusive A H PA Subtropical Highland Axonopus fissifolius Exclusive A H Grasslands, threatened species in the categories: LC least Axonopus ramboi Exclusive A H PA/EN concern, EN endangered, VU Blechnum schomburgkii Exclusive A S PA vulnerable, IUC IUCN’s Red Chrysolaena simplex Exclusive A S List of threatened species) Cunila galioides Exclusive A H PA Cuphea ingrata Indicator A SS Cuphea lindmaniana Exclusive A H Cyperus reflexus Exclusive A H Eleocharis montana Exclusive E H Eleocharis rabenii Exclusive E H Eleocharis sellowiana Exclusive E H IUC Eryngium floribundum Exclusive A H PA Eryngium mesopotamicum Indicator A H Galium humile Exclusive A H LC Gamochaeta americana Exclusive A H PA Glandularia hasslerana Exclusive A SS Hedyotis thesiifolia Indicator FS H Holcus lanatus Exclusive A H Hydrolea spinosa Exclusive E H Juncus microcephalus Indicator E H PA Juncus scirpoides Indicator E H Leptostelma catharinensis Exclusive A H End/EN Leptostelma maxima Exclusive A H Lessingianthus glabratus Exclusive A H Ludwigia longifolia Indicator A S Ludwigia sericea Exclusive A S Lysimachia filiformis Indicator FS H Mayaca sellowiana Ind. and Exc. FS H Monnina tristaniana Exclusive E SS Paspalum dilatatum Exclusive A H Paspalum exaltatum Exclusive A H Paspalum urvillei Exclusive A H Phalocallis coelestis Exclusive E H Polygala linoides Exclusive A H PA Polygonum acuminatum Exclusive A H Polygonum meisnerianum Exclusive A H PA Prunella vulgaris Exclusive A H PA Ranunculus flagelliformis Indicator FS H Rhynchospora corymbosa Indicator A H IUC Rhynchospora rugosa Exclusive A H Rhynchospora tenuis Exclusive A H LC Saccharum asperum Exclusive A H PA Salvia procurrens Indicator A H

123 T. L. de Magalhaes et al.

Table 3 continued Species Outer zone Inner zone Life form Habit Conservation status

Sisyrinchium cf. pachyrhizum Exclusive A H Sisyrinchium vaginatum Exclusive A H PA Solidago chilensis Exclusive A S PA Sporobolus indicus Indicator A H Tibouchina cerastifolia Exclusive A S Utricularia tridentata Exclusive FS H VU Xyris jupicai Exclusive A H

distance from the outer limit. Species distribution in wetlands can be associated with environmental factors, such as water depth and distance from the outer limit (Jiao and Zhou 2013), as well as other factors, such as pH, temperature, and sun incidence. Eugenio et al. (2011) observed that wetlands show changes in floristic and structural composition influ- enced by soil moisture. Pinheiro et al. (2012) observed that the shallower the lake, the higher its vegetation amount. Jiao and Zhou (2013) observed that water depth and distance from the water body explain 70 % of the spatial distribution of the genus Carex in humid areas. Higuchi et al. (2014) observed that the spatial variation in soil drainage influences the heterogeneity of the floristic composition in forest physiognomies. Although the study areas have high floristic turnover, they show the same richness and diversity patterns, as evidenced by their species distribution, species accumula- tion curves, total richness, richness of outer and inner zones, family and genus composition, and formation of outer and inner zones. This complexity of habitat composition is important to determine plant distribution, as well as the occurrence of associated fauna (birds, reptiles, invertebrates, and other taxa). The vegetation composition of wetlands is susceptible to temporal changes in the environment, due to natural factors (mainly rainfall and temperature) and human interferences. Hence, the knowledge of biodiversity and presence of zone indicator species is key to the elaboration of strategies for the restoration and conservation of freshwater wetlands.

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