Plants associated with aquatic and marshy environments in the state of Paraíba, northeastern Brazil

We present a list of aquatic and wetland plant species from the state of Paraíba, Brazil, based on the collections deposited in national and international herbaria. We identified 290 species belonging to 61 families. The checklist includes habit, localities of the collections in the state of Paraíba, and geographic distribution of each species. The amphibious habit was the most prevalent and the Sertão (semiarid inland region) was the region with the greatest collection effort. New occurrences have been registered for the state (14 species). Although our data reveal a high plant richness, we relate this richness to increased field expeditions.


Introduction
Aquatic plants comprise lifeforms from macroscopic algae to submerged, floating, emergent or amphibious tracheophytes, the latter capable of surviving in the water, in swampy places or withstand periodic soil soaking (Chambers, Lacoul, Murphy & Thomaz, 2008;Padial, Bini & Thomaz, 2008). With this variety of lifeforms, this group presents several anatomical and functional adaptations, the result of great diversification from a taxonomic point of view (Sculthorpe, 1967;Esteves, 2011), and which draw the attention of researchers to carry out ecological and floristic studies.
The inventories related to aquatic/marshy environments are relatively recent, compared with typically terrestrial ecosystems, besides the majority of these studies are occasional (Machado-Filho, Cabral, Melo, Zickel & Moura, 2014). With the increase in knowledge about these floristic assemblies, in the first two decades of the 21st century, there has been a recognition of the ecological and economic importance of these organisms for water ecosystems (Chambers et al., 2008), and these studies are clarifying patterns of structure and composition of these floras.
Faced with scientific advances, Brazil still strives to quantify the floristic richness of its aquatic ecosystems, and there is already, for example, general preliminary list for the Northeast region of Brazil (Moura-Júnior et al., 2013). However, scientific publications based on fieldwork, involving research on aquatic/marshy environments of plants for the state of Paraíba, are still scarce. (Araújo, Sabino, Cotarelli, Silva-Filho & Campelo, 2012;Lima, Machado-Filho & Melo, 2013;Torres, Fernando & Lucena, 2016). In addition, the research that has been published does not even cover the entire territorial dimensions of the state. In view of these limitations, it is important to explore the collections deposited in herbaria, in order to complement these data and synthesize the regional list of species from aquatic/marshy environments in Paraíba. Such an effort is recommended not only for the purpose of organizing a checklist, based on richness data, but to qualitatively assess the data, for possible recognition of new occurrences or the identification of species with potential lifeforms in water or swampy conditions. Thus, it is expected that when exploring herbarium collections, it will be possible to ascertain a more accurate number of species of aquatic/marshy environment plants collected for the state. Previous collection expeditions, presumably, lacked any intention of generating information about these floristic assemblies by their collectors, and thus, this information ended up marginalized.
Therefore, this work aims to expand information about plants associated with aquatic and marshy environments in the Northeast region of Brazil. A list of tracheophyte species, occurring in aquatic and swampy environments collected in the state of Paraíba is presented based on the examination of indexed herbarium collections. With this floristic list, data on habit, lifeforms and phytogeography of the registered species are also presented.

Materials and Methods
A preliminary survey was conducted in the collections of the herbaria JPB, EAN, ACAM and CSTR (acronyms according to Thiers, 2017, continuously updated). In addition, the database of the INCT Brazilian Virtual Herbarium of Plants and Fungi -INCT-HVFF (http://inct.splink.org.br) was consulted to find samples of aquatic plants from Paraíba deposited in other herbaria (ALCB, ASE, BHCB, CEN,  CEPEC, CESJ, EAC, FCAB, FLOR, FUEL, HCDAL, HUCP,   HUEFS, HUNI, HUTO, HVASF, HST, HTSA, HURB,  HUFU, ICN, IAN, INPA, IPA, MAC, MBM, MOSS,  NYBG, OBIS-BR, PACA, PEUFR, R, RBR, SP, SPF, SPSF,  UESC, UFP, US, V and VIC). To save space only one  voucher was highlighted in the table. All specimens whose labels had collection records inside or on the shores of lakes, springs, rivers, streams, estuaries, floodplains, reservoirs and marshy environments were listed and different habits (submerged fixed, submerged free, emergent, floating fixed, floating free or amphibious) were determined according to Veloso et al. (1992). However, when the type of habit was not included in the exsiccatae, floristic-taxonomic articles or surveys of aquatic plants were consulted.
The species presented in Table 1 were recorded as identified in the herbarium, excluding those with doubtful identification ("cf." or "aff."). Families that presented a high number of specimens identified only up to genus level were highlighted in the text.
The taxonomic validation of the samples was based on a pre-existing identification on the exsiccate label by an expert in the group. When identification was doubtful, samples were identified based on the specific literature for each botanical group.
The correct spelling of each species name was verified through consultations of the online databases Flora do Brasil 2020 and The Plant List (2019). The delimitation of families followed the Angiosperm Phylogeny Group (APG IV, 2016).
The mesoregions in the territory of Paraíba (Figure 1) were listed according to Brasil (2007), and include the following: Mata (coastal region of hot-humid climate, in the Atlantic Forest domain and over the Barreiras Formation), Agreste (transition zone between the Atlantic Forest and the Caatinga, dominated by a hot-humid climate, preceding the Borborema Plateau), Borborema (region predominantly occupied by the Borborema Plateau) and Sertão (in the Caatinga domain, in a semiarid climate, with crystalline and sedimentary soils of the "Rio do Peixe" basin.  Machado-Filho, et al. -Aquatic plants of Paraíba, Brazil To determine the geographic distribution of each species, the following sources were consulted: literature in aquatic plants (Hoehne, 1948;Irgang and Gastal-Jr, 1996;Pott and Pott, 2000;Amaral, Bittrich, Faria, Anderson & Aona, 2008;Lorenzi, 2008), regional Floras and the online databases of the Global Biodiversity Information Facility (2020), Global Invasive Species Data Base (2019), Tropicos (Mobot, 2019) and the Flora do Brasil 2020.
The species were classified into one of the following geographic distribution categories: Endemic (Caatinga, with connections between Cerrado and/or Atlantic Forest), Neotropical (distributed from Mexico to Argentina), American (restricted to the American continent), Gondwanian (encompassing the South American, African and Australian continents), Paleotropical (scattered in the African continent), Pantropical (those of the tropical climatic range), and Palearctic (associated with European continent), cultivated and with uncertain distribution.

Results and Discussion
From the herbaria, 483 exsiccatae that complied with the established criteria were cataloged. Another 91 specimens were recorded in the INCT-HVFF (2017), totaling 574 exsiccatae registered as "aquatic" or "marshy" collected in the state of Paraíba. Of these, 151 exsiccates were identified only to genus, 12 to family, and one remains undetermined.
In relation to the regions of the state of Paraíba, 192 specimens were collected in the Sertão, 98 in the Agreste, 91 in the Borborema and 61 in the Mata. Probably, the greater collection effort in the interior of Paraíba may be associated with the expansion of universities to the interior of Brazil at the beginning of the 20th century (Barros, 2015).
Few aquatic and marshy ecosystems have been the targets of scientific research in Paraíba. The Sertão presents the greatest collection effort due probably to the concern associated with water availability and the quality of its sources. On the other hand, the fact that the Mata region has fewer records could be related to the urbanization process that has intensified in recent years, de-characterizing the landscape and, consequently, causing the loss of habitats and local floristic diversity, including aquatic species.
We recorded 290 tracheophyte species, and 61 families (Table 1) associated with aquatic and marshy environments in Paraíba.
Of the species identified, only three of them are cultivated: Bryophyllum pinnatum (weed with potential for invasion of new areas, according to Giulietti et al, 2018), Syzygium cumini (tree with potential for invasion of new areas, according to Dias, Baptista, Mantoani, Holdefer & Torezan, 2013) and Ocimum americanum. Some selected species are shown in Figure 2.
Although the data collection efforts are different, comparing the data obtained here with the results presented by Moura-Júnior et al. (2013), who registered 261 species of aquatic plants in the state of Paraíba, this study found 10% more species (another 29 spp.). However, the actual species richness is probably still underestimated due to the low collection effort in the aquatic ecosystems of Paraíba in general.
The predominance of Cyperaceae species corroborates the findings of Lima et al. (2009), who examined herbarium collections in the state of Pernambuco. In floristic studies, the predominance of this family in aquatic and swampy ecosystems is also confirmed, whether in areas of high altitudes (Díaz et al. 2008), subtropical (Rolon, Homem & Maltchik, 2010;Kafer, Colares & Hefler, 2011) or wet-todry transition regions (França et al., 2003;França et al., 2010;Meyer and Franceschinelli, 2011;Lima et al., 2013). According to Bove, Gil, Moreira & Anjos (2003), Cyperaceae is a perennial family that develops spatial dominance in environments, especially in dry periods. This fact is related to the cryptophytic biological spectrum of this group, which involves the development of structures that favor vegetative reproduction, such as tubers, rhizomes or stolons (Pott, Bueno, Pereira, Sallis & Vieira, 1989).
In relation to the lifeform, amphibious species predominated with 69,3% of the species (Figure 5), followed by emergent (12%), fixed submerged (10%), free floating (5,7%) and fixed floating (3%). In relation to amphibious lifeforms, there is a lack of conclusive studies that point out characteristics common to families, or if there are convergent adaptations. Some researchers have already started investigations in this regard, such as Leite, França & Scatena (2009), who analyzed the anatomy of the amphibious representatives of Cyperaceae and found that the presence of air gaps, buliform cells on the adaxial surface of the leaf epidermis, reduced number of xylem elements and low lignification in the cell walls of the tissues in the different organs studied. For these researchers, these characteristics are important for amphibious plants to adapt to the seasonal variations of transition between the aquatic/marshy environments.
Aquatic plants sensu stricto include emergent, floating or submerged lifeforms, and represent 26% of the total species. In this subgroup there is a greater diversity of the botanical families Alismataceae, Lentibulariaceae, Pontederiaceae, Xyridaceae, Nymphaeaceae, Araceae, Onagraceae, Hydrocharitaceae and Salviniaceae. It is noticed that aquatic plants sensu stricto increase in terms of phylogenetic diversity towards the center of the aquatic body. Aquatic plants sensu lato are restricted to the edge of the reservoir and are more related to the surrounding matrix.
Endemic species accounted for 4% of the total, showing that these species of aquatic/marshy environments plants are more widely distributed than expected. The endemic species recorded were restricted to Caatinga or were related to connections between Caatinga -Cerrado or Caatinga -North Atlantic Forest.
Our results corroborate the findings of Schultorpe (1967), who reported that the assemblages of plants associated with aquatic or malaria environments, in general, are comprised of flora approximately 40% endemic to their own continent, the rest being species of transcontinental, pantropical or cosmopolitan distribution. Regarding this wide distribution, Schultorpe (1967), Hutchinson (1975), Charalambidou and Santamaria (2002) and Les, Crawford, Kimball, Moody & Landolt (2003) highlight that anemochory and zoochory are important to understand this pattern in the composition of species.
These plants also have phenotypic plasticity and wide ecological tolerance, when compared to typically terrestrial plants. Thus, variations in temperature and rainfall in tropical regions, such as the state of Paraíba, do not cause such dramatic effects in this group (Santamaría, 2002).
In addition, Esteves (2011), states that the large-scale occurrence of this group can also be influenced by the anthropization process (homogenization of habitats, water or soil pollution), to which aquatic environments are strongly subject. The biological relationships established among species (competition, allelopathy, herbivory, parasitism) can also affect these groups (Lacoul and Freedman, 2006). Most of the water bodies for human supply in the Northeast are eutrophic, due to the conditions of high average temperatures and sunshine throughout the year (Chorus and Bartram, 1999). This characteristic favors the development of aquatic plants, regardless of their way of life. This trophic state is closely related to species composition, in which more generalist species prefer eutrophic ecosystems. This type of situation must also have influenced our data, but in the collections of these plants, it is difficult to find data associated with the trophic state of the water bodies.

Conclusion
There is still a huge gap in Brazil to be filled when it comes to knowledge about the aquatic or swampy floras of its territory. Thus, studies performing a floristic survey of aquatic and swampy environments deposited in botanical collections collaborate to quantify the regional biodiversity in a country.
The State of Paraíba has 290 species of plants registered in aquatic or swampy environments. This data update brought an increase of 11% more species than in previous surveys. In addition, new occurrences were recorded (14 species). This flora comprises mainly herbaceous, amphibious species with wide geographic distributions (the majority occurring in the intratropical zone).
These data need to be updated in the future, with the publication of new field studies, as it was noticed that there are few floristic studies for the state.