Aquatic macrophytes of Northeastern Brazil : Checklist , richness , distribution and life forms

Species richness in Pernambuco should be 369, not 370. Page 310 within Table 2: 1 Graduate student (PhD) in Plant Biology, Universidade Federal de Minas Gerais, Biology Department. Av. Antônio Carlos, 6627. CEP 31270-901. Belo Horizonte, MG, Brazil. 2 Graduate student (PhD) in Botany, Universidade Federal Rural de Pernambuco, Biology Department. Av. Dom Manoel de Medeiros, s/n°, Dois Irmãos. CEP 52171-900. Recife, PE, Brazil. 3 Graduate student (MSc) in Natural Resource, Universidade Federal de Roraima, Biology Department. Av. Capitão Ene Garcez, 2413, Aeroporto, Boa Vista. CEP 69304-000. Roraima, RR, Brazil. 4 Universidade Federal do Mato Grosso do Sul, Program in Plant Biology, Center for Biological Sciences and Health, Biology Department. Cidade Universitária, s/n CEP 79070-900. Campo Grande, MS, Brazil. 5 Universidade Federal Rural de Pernambuco, Program in Botany, Biology Department. Av. Dom Manoel de Medeiros, s/n°, Dois Irmãos. CEP 52171-900. Recife, PE, Brazil. * Corresponding Author. E-mail: zickelbr@yahoo.com Edson Gomes de Moura-Júnior 1, Liliane Ferreira Lima 1, Simone Santos Lira Silva 2, Raíssa Maria Sampaio de Paiva 3, Fernando Alves Ferreira 4, Carmen Silvia Zickel 5* and Arnildo Pott 4 Aquatic macrophytes of Northeastern Brazil: Checklist, richness, distribution and life forms


Introduction
Wetlands represent one of the vital components in the maintenance of the global balance, considering the high diversity of species found in these ecosystems (Gopal and Junk 2000).Part of this biodiversity can be explained by the presence of aquatic plants, which are known to exert large structural and metabolic influences on the environment.These plants participate in the production of organic matter and nutrient cycling in the water, constitute the base of the food chain as the primary source of energy, protect the margins of rivers, ponds and lakes against erosion, and serve as shelter and protection for aquatic and/or amphibious organisms (Pott and Pott 2000;Murphy et al. 2003;Thomaz and Cunha 2010).On the other hand, the excessive growth of aquatic vegetation (mostly ruderal species) can become a problem for water use (navigation and electric power generation), contributing to loss of diversity of submersed plants and phytoplankton (Lembi 2009;Thomaz and Cunha 2010).
Throughout the world, the first studies on aquatic macrophytes were performed in temperate ecosystems and only later began to be performed in the tropics (Thomaz and Bini 2003;Pompêo and Moschini-Carlos 2003).Due to this geographic bias, the existing literature on aquatic plants of tropical regions does not correlate with the biodiversity of the group.Even now, few works address the biodiversity of aquatic macrophytes in African (Raynal-Roques 1980;Obot and Mbagwu 2008) and Asian countries (Subramanyam 1962).In the Americas, studies have been performed in Mexico (Ramos and Novelo 1993;Bonilla-Barbosa and Novelo 1995), in Argentina (Neiff Abstract: Aquatic plants have great influence on the structure and dynamics of aquatic ecosystems, thereby contributing considerably to biodiversity.In Brazil, knowledge of the biodiversity of aquatic macroflora is still limited.We present a checklist of aquatic macrophytes occurring in the northeastern region of Brazil through a bibliographic search.We recorded a total of 412 species, 217 genera and 72 families.The most representative families were Cyperaceae (70 species), Poaceae (38), Fabaceae (27) and Asteraceae (20).The States with highest number of species were Pernambuco (370), Bahia (360), Ceará (267) and Paraíba (261).The best-represented life forms were amphibious (193 species) and emergent (100).The aquatic flora of Northeastern Brazil exhibits high species richness; however, there is a scarcity of records of aquatic macrophytes for the States of Alagoas, Rio Grande do Norte, Maranhão, Sergipe and Piauí.
of aquatic macrophytes in congresses, symposia and scientific journals, there are few professionals that are currently fully dedicated to study this community in Brazil.
Although they have yet to cover the diversity of aquatic macrophytes, the floristic studies carried out in Brazil are important because they contribute to the quantification and qualification of the flora of aquatic ecosystems, as well as to the knowledge of geographic distribution of species.In such a context, obtaining a global vision of the quantity of records and of the species richness of aquatic macrophytes can serve as subsidy for ecological studies, can help visualize patterns related to biodiversity and can help elucidate the relation of flora with environmental factors.
Therefore, our study aims to produce a checklist of aquatic macrophytes occurring in the Northeast of Brazil through a bibliographic survey based on inventories in this region.Thereafter, we want to answer the following questions: (i) What is the number of species recorded for the Northeast of Brazil?(ii) What is the number of existing records for each State of the region?(iii) What are the life forms?(iv) What is the floristic similarity between the states?and (v) Which species are considered ruderal or opportunistic?

Study site
Distinguished from other tropical regions by certain peculiar aspects, the Northeast region of Brazil occupies an area of 1,554,257 km 2 (18.25% of Brazil) and contains nine states: Alagoas, Bahia, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, Rio Grande do Norte and Sergipe (IBGE 2002) (Figure 1).This region is characterized by strikingly distinct phytogeographic zones (forest, subhumid and semiarid Caatinga, and middle North palmlands) and an annual regime of rain irregularly distributed between March and August, with the peak in May and June, the dry period being between September and February (IBGE 2002;Silva et al. 2002).
Covering a large drainage area of the Northeast region of Brazil, there are important Brazilian hydrographic basins, among which we note the following: São Francisco Basin, which has an area of 643,000 km² and covers 521 municipalities of seven states (Bahia, Minas Gerais, Pernambuco, Alagoas, Sergipe, Goiás and Distrito Federal); Parnaíba Basin, which occupies 344,112 km² nearly covering the whole state of Piauí and part of the states of Maranhão and Ceará; Oriental Northeastern Atlantic Basin, basically situated in the state of Maranhão and in a small oriental portion of the state of Pará, has an area of 254,100 km²; and the Eastern Atlantic Basin, with an area of 374,677 km², within two states of the Northeast (Sergipe and Bahia) and two of the Southeast (Minas Gerais and Espírito Santo) (ANA 2012).

Data Collection
The checklist was created by a bibliographic search of studies on aquatic plants performed in the Northeast of Brazil, published between August 2000 and 2010.
To accomplish these objectives, we adopted the conceptualization of aquatic macrophytes proposed by Cook (1996), in which the author includes plants in which photosynthetically active organs are either permanently or for several months of the year totally or partially submersed in freshwater or floating in aquatic habitats.More recently, Chambers et al. (2008) also included charophytes within the definition of macrophytes.
Aquatic macrophytes have been grouped according to their life forms into submerged, free floating, rooted floating, emergent and amphibious (Irgang et al. 1984), and epiphyte (Tur 1972).Usually, life form zoning occurs according to water depth: amphibians on the littoral, emergents on the shallow belts, and others in the deeper zones (Pott et al. 2011).
We consulted floristic and/or taxonomic work such as book chapters and national and international scientific articles, as well as theses and dissertations made available by graduate programs in Botany and Ecology (Table 1).You can see the locations studied in some states (Figure 1, Table 1), except those related to study of Matias et al. (2010), who were not available.Based on those publications, we compiled the floristic data (including ruderal taxa) of life forms of the aquatic macrophytes by state.
To consolidate the checklist, in addition to the referred bibliography, we verified the species records for each state of Northeast of Brazil and consulted the biological collections on the data system of "speciesLink" (SPLINK 2011), which has information from the main Brazilian herbaria.
The species list followed the classification of families proposed by APG III (2009) for angiosperms, by Smith et al. (2006) for pteridophytes, Buck and Goffinet (2000) for bryophytes, and Wood and Imahori (1964) for macroalgae.Plant names and respective authors were checked by consulting the data bank of the Missouri Botanical Garden (MOBOT 2011).The characterization of species as ruderal was based on "Plantas daninhas do Brasil" (Lorenzi 2008), which considers species ruderal if they are the first to colonize disturbed wetlands.

Data analyses
The evaluation of the floristic similarity between the records of different states was accomplished through a cluster analysis.The date of floristic composition was subjected to an analysis of similarity by the Jaccard index (Magurran 2004) and ordered by the WPGMA method, using the software PRIMER 6.0 (Clarke and Gorley 2006).
To identify significantly similar groups (p <0.05), we used the Simprof method of randomization with 1000 replications, using the software PRIMER 6.0 (Clarke and Gorley 2006).
We compiled all records of aquatic macrophytes in a matrix of presence and absence of species.The frequency of occurrence of each species (F) was estimated through the equation: where: n i = number of sites where the species i was found, and N = number of sampled sites

Results and Discussion
We compiled 412 species of 217 genera and 72 families (Table 2).According to Agostinho et al. (2005), the vascular aquatic flora of wetlands in Brazil is estimated to 600 species, which makes the number of taxa identified in our study somewhat representative.The high richness of aquatic macrophytes for the Northeast can be attributed to seasonal and hydrological influence on the aquatic ecosystems of the region (França et al. 2003;Neves et al. 2006;Moura-Júnior et al. 2009;Campelo et al. 2012) The families with highest richness of aquatic macrophytes in the Northeast of Brazil were Cyperaceae, with 70 species, Poaceae (36 spp.), Fabaceae (27 spp.), Alismataceae (23 spp.) and Asteraceae (20 spp.) (Table 2).The floristic representativeness of Cyperaceae and Poaceae was also recorded in studies on aquatic macrophytes of the other Brazilian regions, including the North (Junk and Piedade 1993), South (Irgang and Gastal-Jr. 1996;Mormul et al. 2010) andSoutheast (Ferreira et al. 2010).The present estimate is ca.700 species of Cyperaceae and 1500 of Poaceae in Brazil (Souza and Lorenzi 2008).According to Goetghebeur (1998), the taxonomic abundance of these families must be related to their efficiency in vegetative propagation, with underground systems formed by rhizomes or stolons.The richness of Asteraceae and Fabaceae in our study converged with the result reported by Lima et al. (2009) in the checklist of aquatic macrophytes of the state of Pernambuco, wherein both of these families as well as the two previous families are the four richest.It is known that species of Asteraceae are particularly common in several vegetation types in Brazil (Souza and Lorenzi 2008), likely due to the morphological adaptations of the fruits, which have a persistent pappus transformed into a dispersal structure, primarily for anemochory and zoochory (Heiden et al. 2007).Considering Fabaceae, we believe that the morphological, ecophysiological and reproductive plasticity of the sub-families Faboideae, Caesalpinioideae and Mimosoideae can explain the wide specific richness of the family in ecotonal areas and in wetlands of the Northeast.As was discussed for Cyperaceae, Poaceae, Fabaceae and Asteraceae, the high representation of floristic Alismataceae in northeastern Brazil may also be related to morphological adjustments of their representatives.According to Matias (2010), individuals of Echinodorus and Sagittaria (the most common representative of Alismataceae in the study area) have an underground system composed of perennial rhizomes with buds that can withstand long periods of drought and thus can colonize aquatic ecosystems permanently and/or intermittently until ecotone environments (swamps) are created.
According to Magurran (1988), the number of inventoried species in an area invariably increases with the size of sampled area and/or the sampling effort.Therefore, the scarce record of aquatic macrophytes for the states of Alagoas, Rio Grande do Norte, Maranhão, Sergipe and Piauí compared to the other states of the Northeast might have been caused by the low number of inventoried areas and by a small range of studied areas.Although some states in the Northeast presented a negative bias regarding the record of aquatic plant species, Pernambuco and Bahia showed similar species richness to that observed in the Amazon region, where 388 species were identified (Junk and Piedade 1993), and higher than the richness of 273 species found in the Pantanal (Pott and Pott 2000).
According to the Simprof test, macrophyte communities that had Jaccard (S) scores above 54% were considered significantly similar in floristic structure (Figure 2).Thus, groups of species of aquatic plants in the states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco and Sergipe can be considered similar (S = 55%) (Figure 2).However, within the group of those six states, there was the formation of three clusters whose similarity indices were the highest recorded in the analysis: the first included the aquatic macrophytes of the states of Bahia and Pernambuco (S = 79.8% ), the second was represented by macrophytes of Ceará and Paraíba (S = 69.3%),and third was formed by hydrophytes of Alagoas and Sergipe (S = 58.5%)(Figure 2).Some studies have shown that the composition and distribution of species of aquatic plants in tropical ecosystems are primarily explained by their hydrological (e.g., elevation, flow) and/or limnological characteristics (e.g., turbidity, conductivity, transparency, pH, temperature and concentration of oxygen, nitrogen and dissolved phosphorus) (Thomaz et al. 2003;Murphy et al. 2003;Pedro et al. 2006;Souza et al. 2009;-Moura Júnior et al. 2011).Most of these researchers concede that changes in hydrological characteristics and/or limnological ecosystem changes, in short, the processes of interaction between species (e.g., competition, facilitation), modify the structure of aquatic communities.In this context, the similarity in the species composition of hydrophytes of Alagoas, Bahia, Ceará, Paraíba, Pernambuco and Sergipe can be explained by similarities in the hydrological and limnological conditions of aquatic ecosystems in these states.Similarly, the floristic dissimilarity of macrophytes of Maranhão, Piauí and Rio Grande do Norte in relation to other states of Northeastern Brazil is most likely related to the differences in hydrological and limnological ecosystem states.Moreover, the lack of information about the species of aquatic plants in the states of Maranhão, Piauí and Rio Grande do Norte may also explain the differences for these flora with the rest of the Northeast, which implies the need for floristic and taxonomic studies for these three states.
Regarding the aquatic macrophytes, which are restricted to only one of the life forms of the Northeast, the most representative groups were amphibious and emergent, with 193 and 100 of the species, respectively.Next, there appeared rooted submersed (22 spp.), free floating (18 spp.), rooted floating (16 spp.), free submersed (eight spp.) and a single species of epiphyte.Relative to the plasticity of life forms, 47 species stood out for being amphibious as well as emergent.As for the results of the life forms per state, we also observed a higher number of species categorized as amphibious and emergent when compared to other analyzed categories (Figure 3).The other categories of life forms contained two species (amphibious/rooted floating) and only one species each (emergent/epiphyte/amphibious, emergent/free floating, emergent/rooted floating, emergent/rooted submerged and free floating/rooted floating).The predominance of species that presented amphibious and/or emergent life forms (for the nine states of Northeastern Brazil) was similar to results obtained in various aquatic environments of tropical regions (Pott and Pott 2000;Ferreira et al. 2011).We attribute the representativeness of these species to their morphophysiological adjustments, which allow them to survive in the interface between aquatic and terrestrial environments (Sculthorpe 1967;Matias et al. 2003).We further suggest that the high richness of amphibious and/ or emergent aquatic plants in tropical ecosystems may be related to the number of species of Cyperaceae and Poaceae (Ribeiro et al. 2011).
In our list, 141 species were considered ruderal or opportunistic, corresponding to 34.2% of the number of aquatic macrophytes cited for the Northeast.Such species are grouped into 44 families, of which Poaceae (with 23 species), Asteraceae (14), Cyperaceae (14), Fabaceae (12) and Pontederiaceae (6) had the highest number of species (Table 2).Some studies have reported that the proliferation of aquatic ruderal weeds is primarily related to the dumping of industrial, urban and agricultural nutrient-rich nitrogen and phosphate (anthropogenic eutrophication) in rivers, lakes, ponds and reservoirs (Pott and Pott 2000;Esteves 2011).It is also known that eutrophication is an agent that interferes with interspecific interactions of natural selection, causing a decline in the biodiversity of aquatic communities (Tundisi and Tundisi 2008;Bicudo et al. 2010;Esteves 2011).From this perspective, the growing process of deterioration in the quality of aquatic limnological ecosystems in Northeastern Brazil (Cyril et al. 2010;Silva and Zickel 2010) can be considered to be a factor threatening the aquatic biodiversity of the region, especially if academic studies and/or governmental strategies for the conservation of these resources are not developed.
The occurrence of ruderal species per state was the following: Maranhão (43.85%),Sergipe (42.85%),Alagoas (42.78%),Rio Grande do Norte (41.96%),Ceará (41.04%),Piauí (39.87%),Paraíba (39.31%),Bahia (36.16%) and Pernambuco (35.58%).It is worth pointing out that of the 71 species common to all states of the Northeast, 39 species were considered ruderal, while of the 41 taxa considered restricted, i.e., that occurred only in a single state, six were ranked as ruderal (Table 2).As we observed in our study, other researchers also recorded a large percentage of ruderal species, e.g., Kita and Souza (2003) for the floodplain of the upper Paraná, Bove et al. (2003) in a temporary aquatic environment of the coastal plain in Rio de Janeiro, and Henry- Silva et al. (2010) for the hydrographic basin of Apodi/Mossoró, at 29%, 23% and 47.5%, respectively.The high representativeness of species considered ruderal or oportunistic can be attributed to some features favoring dispersion and survival, such as high adaptation and resistance, as well as longevity and good seed dispersion (Souza and Lorenzi 2008).In addition, the major weedy species of aquatic macrophytes that occur in Brazil spread vegetatively (plus via seed).This factor facilitates the proliferation and exaggerated abundance of some species in many aquatic environments.Many species thus become an ecological problem (Lembi 2009;Thomaz and Cunha 2010).Moura et al. (2009) cited the weedy species Egeria densa, Ceratophyllum demersum, Brachiaria mutica, B. subquadripara, Eichhornia crassipes, Pistia stratiotes, Polygonum lapathifolium, Echinochloa polystachya and Salvinia auriculata as the species that have the most impact in the State of São Paulo because they can hinder multiple uses of water resources, such as the generation of electricity, irrigation, navigation, fishing and recreation.These species, except Urochloa arrecta (above cited as Brachiaria subquadripara, although not a synonym) and Polygonum lapathifolium, have all been recorded in Northeastern Brazil.
We verified that the existing aquatic flora in Northeastern Brazil exhibits high species richness, a fact that is easily observed by the number of recorded taxa.The record of species varied among states and among categories of life forms according to the amount of sampled areas and/or collection effort in each state.Although the Northeast presented a high richness of aquatic plants (34,2% of which were classified as ruderal), we observed a scarcity in the records of aquatic plants for the states of Alagoas, Rio Grande do Norte, Maranhão, Sergipe and Piauí.We detected a need for more data collection and research directed at the aquatic community.We suggest efforts on floristic and taxonomic work be performed in the Northeast of Brazil to gather information to better determine the contribution of aquatic macrophytes present in wetlands of this region.

Figure 1 .
Figure 1.Hidrographic map of the Northeast region of Brazil, with the inventoried sites (in red).AL = State of Alagoas; BA = State of Bahia; CE = State of Ceará; MA = State of Maranhão; PB = State of Paraiba; PE; State of Pernambuco; PI = State of Piauí; RN = State of Rio Grande do Norte; SE = State of Sergipe.

Figure 3 .
Figure 3. Life forms of aquatic macrophytes by state in Northeast Brazil.AL = State of Alagoas; BA = State of Bahia; CE = State of Ceará; MA = State of Maranhão; PB = State of Paraiba; PE; State of Pernambuco; PI = State of Piauí; RN = State of Rio Grande do Norte; SE = State of Sergipe.

Table 1 .
List of the studies used to elaborate the checklist.AL = State of Alagoas; BA = State of Bahia; CE = State of Ceará; MA = State of Maranhão; PB = State of Paraiba; PE; State of Pernambuco; PI = State of Piauí; RN = State of Rio Grande do Norte; SE = State of Sergipe; NO = Northeastern.