List of Angiosperm species of the riparian vegetation of the Apodi-Mossoró river , Rio Grande do Norte , Brazil

Complete lists of species of the riparian forests of Rio Grande do Norte were not found. The work of Tavares et al. (1975), although referring to the vegetation of the Piranhas-Açu basin, did not focus on the riparian vegetation. For other northeastern states knowledge of riparian vegetation is also rare. Noteworthy are the work of Nascimento et al. (2003), along the São Francisco river, and Lacerda et al. (2005), expanded by Lacerda and Barbosa (2006) for Taperoá river basin in Paraiba. In Pernambuco, there are studies on riparian vegetation of the river Pajeú (Souza and Rodal 2010), and an ethnobotanical study on the riparian vegetation of the river Navio, both in the Floresta municipality (Ferraz et al. 2006). This study was conducted primarily to list the richness of Angiosperm taxa of the riparian vegetation of the Apodi-Mossoró river and discuss general aspects of this vegetation type, providing subsidies for its restoration and management.


Introduction
The Apodi -Mossoró river basin, with an area of 14,268 km 2 (corresponding to 26.8% of the estimated area of the Rio Grande do Norte State), occurs in the Caatinga biome where the climate is very hot and semi-arid (SEMARH 1998), BSw'h' according to Köppen classification, being surrounded by the Araripe mountains and Borborema plateau (Rocha et al. 2009). The source and mouth of the river Apodi Mossoró are in the Rio Grande do Norte and it has 618 dams (Henry-Silva 2010), with a total water volume of 469.714.600m3 .
The course of the river was the main route of Portuguese penetration into the interior of Rio Grande do Norte in the eighteenth century and its margins were already used for the establishment of corrals and gardens (Monteiro 2002). Currently, the major activities that interfere directly in the river are irrigated fruit growing, family agriculture, salt production, mineral exploration and oil production, which environmental and economic impacts focus entirely on the river basin (Rocha et al. 2009). Logging of riparian vegetation is also intense and is documented below.
With early deforestation and salinization of large areas downstream, little is left of the original riparian flora of the temporary rivers in the semi-arid Northeast and is curious to note that the descriptions of these vegetation types are contradictory. For Ab 'Sáber (1999a, b; these "matinhas beiradeiras" of the northeastern rivers may be called "forests of craiba" (Tabebuia aurea (Silva Manso) Benth. and Hook. F. ex Moore). Andrade- Lima (1981) on the other hand characterizes them a palm forest, where the dominant taxa are Copernicia prunifera (Mill.) H.E. Moore, Licania rigida Benth. and Geoffroea spinosa Jacq., and he does not mention craiba. The descriptions of Ab'Saber and Andrade Lima refer only to dominant taxa, and the riparian northeastern forests have been misinterpreted in that they contain a small number of species.
Abstract: This article describes the riparian vegetation of a river in the Rio Grande do Norte state for the first time. This is a seasonal river in the semiarid region of the Caatinga biome. The study is based on data from herbarium collections and new expeditions from July 2007 to October 2008. Two hundred and forty seven taxa were recorded and of these, 116 are herbs and three of which are epiphytes, 25 sub-shrubs, 77 shrubs or trees, 26 lianas, one parasite, and two palms. This list of species of riparian vegetation in the river Apodi-Mossoró was compared with only two available lists from rivers in the northeast with similar environmental characteristics and showed a low similarity. This study points to the need for preservation of the species and remnants of riparian vegetation of the river Apodi-Mossoró and to increase efforts in the study of this vegetation type.
The southern half of the basin consists of a Depression, a relief with predominantly flat plateau and Planaltos Residuais, which surfaces are delimited by erosional scarps with flat tops and sedimentary origin. The north-central portion of the basin is characterized by karst surface and in the far north, there is the coastal strip, according to data from SEMARH (1998) which presents more detail.
The floristic survey was based on the analysis of specimens deposited in the MOSS herbarium (acronym available in Thiers 2012) and new collections undertaken. Samples were collected monthly and some every two weeks, during the period from July 2007 to October 2008 (see Figure 1): 1) in the region of springs, in the municipality of Luís Gomes, 2) in preserved fragments in the municipality of Felipe Guerra, representing the middle portion of the river, and 3) in Mossoró, with estuarine characteristics. Additional collections were made in Governor Dix-Sept Rosado, Apodi, Riacho de Santana and Areia Branca.
The herbarium analysis showed species that were not found in the systematic field collection points. These species were then relocated based on the label information and with the aid of local informants.
The collections were made randomly within the area or directed by local informants. We sampled only fertile material, however a few tree species were only found  sterile and their names were included in the list presented in Table 1. We included species occurring in small grassland patches and aquatic herbs, associated with riparian forests. Identifications were made using literature, by comparison in the herbaria and sending material to specialists. The vouchers were incorporated into the MOSS herbarium and duplicates distributed to EAC, UFRN and others. Popular names were provided by local informants. Information provided by the riverside communities was the main source for determining the location of endangered species. The scientific names are in accordance to the list of species in the flora of Brazil (Forzza et al. 2012).
We compared the similarity of the tree and shrub flora of the river Apodi-Mossoró with lists published in Lacerda et al. (2005) and Souza and Rodal (2010), due to their geographic proximity and similarities in environmental factors. Table 1 presents the environmental characteristics of the regions occupied by the rivers whose floristic lists were used in this comparison. The unidentified taxa were considered exclusive or distinct. Sub-shrubs from Apodi Mossoró river vegetation were included in the comparison if those species were considered shrubs or trees in the other two published lists. The similarity between the flora of these areas was based on Sørensen index (Mueller-Dombois and Ellenberg 1974).

Results and Discussion
A total of 247 taxa were recorded in the Apodi-Mossoró riparian vegetation (Table 2), which represents the largest number of species records occurring along rivers in the Northeast. Of the species found, 116 are terrestrial or aquatic herbs and three epiphytes, 25 sub-shrubs, 77 shrubs or trees, 26 lianas, one parasite and two palm trees.
Non arboreal taxa: 119 species were found from this stratum (Table 1), represented in 28 families and 74 genera. Some taxa are illustrated in Figure 2. The Poaceae and Cyperaceae account for 41% of the herbaceous flora found in the riparian vegetation of this river. This large number of herbs is also due to sampling species from temporary ponds and associated pioneer taxa.
The most diverse genera were Cyperus L. with 14 species, followed by Eragrostis Wolf, Paspalum L. and Ludwigia L. with four species each. Tillandsia Wilbr., Eleocharis R. Br, Panicum L., Spermacoce L. and Lippia L. had three species each and all other genera were represented by one or two species.
The species Tarenaya spinosa (Jacq.) Raf., Cyperus compressus L., Croton heliotropiifolius Kunth., Chloris barbata Sw., Apalanthe granatensis (Bonpl.) Planch., Echinochloa colona (L.) Link, Heteranthera seubertiana Solms and Eleocharis geniculata (L.) Roem. and Schult. were recorded in all the collecting areas. Araújo et al. (2005) compared the herbaceous diversity in flat, rocky and riparian microhabitats in the Caatinga biome. The richness, diversity and uniqueness of the herbaceous species in riparian habitat were higher than the others. The similarity between the occurrence of non-arboreal taxa from this study compared to the list of Araújo et al. (2005) is extremely low. The species that occurred in both lists are Bomarea edulis (Tussac.) Herb. (under B. salsilloides (Mart.) Benth. and Hook), Dalechampia cf. scandens L., Heliotropium angiospermum Murray, Herissantia crispa (L.) Briziky, Panicum trichoides Sw., Panicum venezuelae Hack, Ruellia asperula (Mart. and Nees) Lindau and Tragia volubilis L. Dactyloctenium aegyptium (L.) P. Beauv. and Enteropogon mollis (Nees) Clayton appear in the list of Araújo et al. (2005), but are not related to the riparian habitat. The low similarity of the herbaceous layer between the Apodi-Mossoró and Olaria stream may be related to the heterogeneity of the riparian vegetation of the northeastern rivers (discussed below in greater detail), but also due to differences between the phytogeographic subzones occupied by rivers.
The three phytogeographic subzones of the Northeast are called "Zona da Mata", "Agreste" and "Sertão". According to Barbosa et al. (2006), the Zona da Mata extends from the coast in a strip of approximately 100km wide and has humid tropical climate, fertile soil and occupied by atlantic rainforest. The Agreste is a transition area between the more humid Zona da Mata and the semi arid Sertão. Araújo et al. (2005) worked in an area of the Olaria stream located in the Agreste, called dry tropical forest by the authors. Works that deal with the distribution pattern of taxa in Pernambuco show that species richness varies between the subzones, with exclusive taxa occurring in each subzone. The Agreste has higher richness of taxa and exclusive species, when compared with the Sertão. Among others, the work of Barros et al. (1988) and Abreu et al. (2008) illustrate this distribution pattern by analysis of distant taxonomic groups, such as Pteridophytes and Oxalis L. (Oxalidaceae) respectively, with the higher number of taxa in the Agreste than in the Sertão and emphasize the occurrence of exclusive species, characteristic of each subzone. Maciel et al. (2010) showed that Agreste is populated with all the species of Paspalum L. (Poaceae) occurring in Pernambuco and that this subzone is the richest in exclusive species when compared with the Sertão, which, in turn, also has exclusive species. The Apodi-Mossoró river is restricted to the Sertão and Olaria stream to the Agreste.
The time of year can also be the cause of low similarity, since Araújo et al. (2005) sampled only those species that occurred in the rainy season, with no data collected during the dry season. Eragrostis hypnoides (Lam.) Britton, for example, was only found in the dry season, occurring in the shrinking lake margins, which was also observed by Ferreira et al. (2009). Reis et al. (2006) and Lima et al. (2007) showed that due to variations in total rainfall between years, characteristic of northeastern climate, the herbaceous community structure can be changed and many populations can show drastic reductions in size, even disappearing completely from the area. Lima et al. (2007) evaluating the phenological differences between microhabitats in an area of caatinga, concluded that spatial variations in the microhabitats conditions associated with interannual variations in total rainfall may change the flowering period and recruitment of herbaceous plants. They also showed that a short time series may not be sufficient to describe the plasticity that exists within populations and infer the geographical distribution of some herbaceous species of the caatinga.
We sampled 30 species of lianas belonging to 25 genera, 14 families with one undetermined species. The families Fabaceae (seven species), Cucurbitaceae (five species) and Sapindaceae (four species) showed the highest species richness, accounting for 50% of the liana species found. Moreover, ten families (37%) were represented by a single liana species. The genera of higher species richness were Luffa Mill., Cardiospermum L. and Paullinia L., with two species each, and the remaining 20 genera (74%) had only one. Remarkably, 18 (66%) of the 27 species found occurred only in the Luís Gomes region, where the river sources were found. As previously mentioned, the source of the Apodi-Mossoró river is located in the Serra dos Minhuns, which has semi-deciduous vegetation. The occurrence of a significant number of lianas in a semi-  Udulutsch et al. (2004) highlighted this high liana species richness as attributes of these seasonally semi-deciduous forest fragments. No published data on the occurrence of lianas in riparian forests of the Northeast temporary rivers was found.
Tree-shrub taxa: The family with the highest number of taxa was Fabaceae, with 19 genera and 30 species, followed by Euphorbiaceae, with four genera and five species. Figure 3 shows the illustration of tree-shrub taxa. Fabaceae and Euphorbiaceae also were cited as the richest families in species numbers in other surveys of the tree-shrub layer in areas of caatinga (Lemos et al. 2004;Amorim et al. 2005;Gomes et al. 2006;Santana and Souto 2006) and the seasonally semi-deciduous forests (Rodal et al. 2005). Table 3 compares the number of tree taxa from the rivers Taperoá in Paraiba (Lacerda et al. 2005) and Pajeú in Pernambuco (Souza and Rodal 2010)  This same table shows that the number of unique tree taxa, or those quoted in only one of the three surveys is high. There are 18 species cited for Taperoá which did not occur in the other two areas, six were unique to the river Pajeú and 40 to the Apodi Mossoró river. The Sørensen index shows a low similarity between the tree-shrub flora of the river areas and Taperoá river shares more species in common with the Apodi Mossoró river (Table 3).
The large number of exclusive species in the riparian vegetation of the Apodi-Mossoró is probably due to sampling along the entire length of the river, which did not occur in the other two surveys. Thus, species occurring in the mangrove penetrated into the riparian vegetation, as is the case Laguncularia racemosa (L.) C.F. Gaertn., Avicennia spp. and Lycium martii Sendtn. collected in Mossoró, site with a strong estuarine influence. The same occurs in the region of springs in Luiz Gomes, which was surrounded by semi deciduous forest species, as is the case Myrciaria tenella (DC.) O.Berg (Pereira et al. 2002) and Thiloa glaucocarpa (Mart.) Eichler, Copaifera sp. among others. Figure 4 illustrates the various environments found in this work.
The description given by Ab'Sáber (2001) of a riparian vegetation of seasonal rivers in the Northeast, being dominated by "craiba" (Tabebuia aurea), could not be applied in any of the remaining sections of the river Apodi-Mossoró at least not today. No records of "craiba" were found along the Apodi-Mossoró river.
The rarity of "craiba" may be due to human influence. There are indications of a more frequent occurrence of this species, such as the name of a municipality in the watershed Apodi-Mossoró as Caraúbas, which is an obvious reference to "craiba" which is also called "caraúba" (Braga 1976). Another interesting fact that can aid the discussion, is that "craiba" showed higher use value in the study by Ferraz et al. (2006) in a creek in Pernambuco. However, according to these authors, the current use by the local population is not consistently associated with positive or negative impacts on the conservation of the species.
In Andrade- Lima (1982) characterization there is no reference to "craibeira" and the riparian vegetation of the Rio Grande do Norte, Ceará and Piauí seasonal rivers is a "forest of palms" with predominantly Copernicia prunifera, Licania rigida ( Figure 3F) and Geoffroea spinosa. Interestingly, none of the dominant species considered by Ab'Saber (2001) or Andrade Lima (1982) were found in the list of species shared between the three areas.
The lack of "craiba" in the riparian vegetation of Apodi Mossoró today could be explained by human action, but the lack of "carnauba" in the Taperoá river (Lacerda et al. 2005;Lacerda and Barbosa 2006) is more complicated and seems to demonstrate that the riparian vegetation of the Northeast rivers is extremely heterogeneous and that the descriptions of Andrade-Lima and Ab'Sáber are not conflicting, but refer to different distinct contexts. The description given by Andrade- Lima (1981) demonstrates better the vegetation more frequently found in the small remnants along the Apodi-Mossoró river: great proliferation of "carnaúba" and "oiticicas" of considerable size and the frequent presence of "marizeiro" or "umarizeiro".
Ab'Sáber (1999b) refers to "ariscos" which are grassy fields with groups of "carnaúbas". Formations that approach this description can be found in the Mossoró municipality, except for the presence of "craibeira", as mentioned in the previous paragraph. In these formations, Cyperus articulatus L. (Cyperaceae), locally known as "junco", covers the areas flooded and Paspalum vaginatum Sw. (Poaceae), surround the "junco ponds" in the drier portions of these wetlands. At the edges of these areas, the "joazeiro" (Zizyphus joazeiro) is very frequent.
In addition to differences in the composition of riparian vegetation between the rivers of the Northeast, there is a floristic heterogeneity of riparian forests conditioned by ecotonal nature of the border, which is occupied by more than one type of vegetation or distinct physiognomic formations, as emphasized by Rodrigues and Nave (2001). The fragments of the riparian vegetation studied along the Apodi-Mossoró river were shown to be heterogeneous in physiognomic and floristic terms. According to Fernandes (2005), the influence of mountain forests in the composition of the riparian vegetation of the rivers of northeast is broad, since species have originated from the adjacent mountains. Similar proposition was made and substantiated by Oliveira Filho and Ratter (2001) to explain the extraordinary richness of the riparian vegetation of the Cerrado, and they suggest that elements of riparian vegetation were "imported" from neighboring forest formations.
Besides eliminating the riparian vegetation as a whole, selective pressure on certain species is also likely to occur. Species considered typical and frequent (Andrade-Lima 1981), as Geoffrea spinosa, the popular "umarizeiro", have reduced populations today, even though the cooked fruit is well appreciated by riverine communities. Sapindus saponaria L. is also represented by a few individuals, located in Apodi.
Only two individuals of Vitex gardneriana Schauer, popularly called "jarimataia" and Trichilia hirta L., "barandão", were relocated and could be prioritized in recuperation programs to maintain these taxa in riparian vegetation of the Apodi-Mossoró river or at least in Apodi. The distribution of these species seems never to have been continuous along the length of the river, since the previous collection records are concentrated only in Apodi and communities of the source regions apparently did not know these species. According to reports from the riverside community of Apodi, stems from "jarimataia" and "barandão" are extracted to manufacture tool handles and fence posts.
Besides the removal of the riparian vegetation of the Apodi-Mossoró river, biological invasion by exotic species is common. The "algarroba" (Prosopis juliflora (Sw.) DC.) mixed with the native pioneer "jurema preta" (Mimosa tenuiflora (Willd.) Poir.), forms large tracts of vegetation along the river, especially in Mossoró. Another concern is the invasion by "unha-de-cão" (Cryptostegia grandiflora R.Br., Figure 3C), a species endemic to Madagascar and naturalized in tropical regions of the world (Vieira et al. 2004), which forms dense, impenetrable forests in floodplains. To a lesser extent, we observed the invasion of riparian vegetation by Parkinsonia aculeata L., whose impact in areas of the Northeast has been documented (Fabricante 2009).
The results of this study point to a small similarity between areas of riparian vegetation, as reported for other regions (Rodrigues and Nave 2001), but the small number of available studies do not provide a comprehensive view of the distribution of species in the seasonal rivers of semiarid region of Brazil.