Checklist of Angiosperms in the Restingas of Pará state, Brazil, with comments on floristic affinities and phytophysiognomies

Abstract Pará state has one of the longest coastal in Brazil. However, floristic surveys have been conducted in few regions and only one study has comprehensively evaluated the coastal flora of the state. The objective of this study was to create an updated and certified checklist of the angiosperms in the restingas of Pará. The list was made using literature, floristic and taxonomic revisions, herbaria specimens from HBRA, IAN, MFS and MG, and collections made between 2014 and 2018. Overall, 470 species, 279 genera and 92 families were recorded. Of this total, 11 species are new records for coastal Pará. The families with the greatest number of species are Fabaceae, Cyperaceae, Poaceae, Myrtaceae, Rubiaceae, Asteraceae, Apocynaceae, Polygalaceae, Convolvulaceae and Melastomataceae, which correspond to 52% of the species. Cyperus, Eugenia, Rhynchospora, Eleocharis and Ipomoea are the most representative genera. For life forms, herbs and shrubs are predominant. Dune fields, restinga forest and herbaceous swamp are the phytophysiognomies with the greatest number of species. A comparison with restingas of northeastern Brazil showed that the flora surveyed is most similar to that of Maranhão, since many species of the Amazonian flora also occur in restingas in this state.


Introduction
Approximately 70% of coastal Brazil is occupied by dune and restinga formations, which are discontinuous due to characteristics of the soil and topography (Rizzini 1979;Silva et al. 2010). In Amazonia, this pioneer ecosystem occurs in northeastern Pará and is formed by plant communities on sandy Quaternary plains under marine influence, with small elevations and distinct phytophysiognomies in the direction of the ocean to the continent (Bastos 1996;Silva et al. 2010).
According to Flora of Brazil 2020 (BFG 2015), the largest gap in the knowledge about the vegetation of the country is still in Amazonia. This includes restingas, which have been studied more in the Northeast Zickel et al. 2007;Silva et al. 2008;Santos-Filho et al. 2011Oliveira et al. 2014) and Southeast Souza et al. 2016) coastal regions of Brazil.
Brazilian restingas have been destroyed due to urban expansion and illegal extractivism (Scarano et al. 2004), and studies of this ecosystem have advanced at a slower rate compared to the increase in this degradation (Scherer et al. 2005). In Pará, the main threats are the illegal extraction of material for civil construction, tourism and fire (Silva et al. 2010;Amaral et al. 2016).
Since the work of Pires (1973), which proposed a classification for Amazonian plant formations, a little over 60 studies have been conducted in restingas in Pará, including abstracts, scientific articles, theses and dissertations. Some of these works focus on species aspects of the vegetation: floristics/phytosociology (Bastos 1996;Santos et al. 2003;Silva et al. 2010;Quaresma & Jardim 2015); relationships of plant communities and environmental factors Silva et al. 2018); and taxonomic groups (Vicente et al. 1999;Rocha 2000;Rocha et al. 2001a,b;Rocha & Bastos 2004;Rosário et al. 2005;Margalho et al. 2009;Sousa et al. 2009; Barbosa et al. 2013;Mesquita et al. 2013;Abreu et al. 2014;Lima et al. 2014;Falcão-da-Silva et al. 2015a, b;Schneider et al. 2017). In addition, Bastos et al. (2003) covers botanical and medicinal use aspects and a book by Bastos et al. (2014) is about flowers and fruits that are part of the beauty of these environments.
The diversity of angiosperms in Amazonian restingas was evaluated by Amaral et al. (2008). This publication lists 365 species for coastal Pará and Amapá and is based on determinations on herbarium collections; however, it does not cite specimens. After a decade, this is still the only comprehensive work about the coastal flora of Pará. Considering the possible increase in herbarium collections and new determinations of species, as a result of a growth in knowledge about the flora of Brazil in recent years (BFG 2018), this work provides a certified checklist of the angiosperms in the restingas of Pará.

Study area
The areas of restinga in Pará are concentrated in the northeastern part of the state (approximately 598 km), including the municipalities of Bragança and Augusto Corrêa (Bragantina region) and Curuçá, Maracanã, Marapanim, Salinópolis, São Caetano de Odivelas and São João de Pirabas (Salgado region) (Fig. 1). In addition to the restingas on the mainland, in an eastern part of Marajó Island (Salvaterra and Soure municipalities) there are areas of this ecosystem associated with areas transitioning to Amazonian savanna (Amaral 2016).
Restinga vegetation in Pará is generally formed of different complex physiognomies on a sandy plain, including areas with herbaceous halophiles or rhizomatous psammophiles, herbaceous swamps, dune fields, open formations with bushes and restinga forest, as described by Bastos (1996). The soil is sandy, poor in clay and organic material, and has a low capacity to retain water and nutrients . The climate is the Am type based on the Köpen classification (Alvares et al. 2013). The annual rainfall is 2,500-3,100 mm, the average annual temperature is 27 °C and the relative humidity of the air is around 80-85% (Sudam 1984;Martorano et al. 1993;Alvares et al. 2013).

Data sampling and analysis
The list of species that occur in the restingas of Pará was obtained from two main sources: (i) reference literature about the restinga flora of coastal Pará (Santos & Rosário 1988;Bastos 1988;Amaral et al. 2008Amaral et al. , 2016 and floristic-taxonomic revisions of groups that are known to occur in restingas of the state; and (ii) specimens deposited in herbaria that concentrate on records of the state (HBRA, IAN, MFS and MG). Acronyms according to Thiers (continuously updated).
Expeditions were also made between 2014 and 2018. While collecting, the random walk method was adopted, as described by Filgueiras et al. (1994), with the goal of sampling the majority of the restinga phytophysiognomies; fertile material was collected and processed based on the methods used in plant taxonomy (Bridson & Forman 1998).
The samples collected, and undetermined herbarium specimens, were identified based on taxonomic revisions, regional floras, comparison with collections determined by specialist and literature about each family. The collections were deposited in MG at the Museu Paraense Emílio Goeldi.
The classification of families follows APG IV (2016), except for Turneraceae that is treated as independent of Passifloraceae. The information about life forms and phytophysiognomies (habitats) is based on field observations, specimen labels and the literature. The classification for the phytophysiognomies follows Bastos (1996) and the classification for the life forms follows IBGE (2012), except species of climbers, which is based on the definitions of liana and herbaceous vine by Queiroz (2009
Among the families with mainly species of shrubs and trees, Fabaceae (23 spp.), Myrtaceae (21 spp.), Rubiaceae (14 spp.) and Sapotaceae (7 spp.) are notable for being the most representative in number of species, mainly in the restinga forest phytophysiognomy. Cyperaceae (52 spp.), Poaceae (32 spp.) and Fabaceae (19 spp.) are the most representative families of terrestrial herbs, which is due to the high occurrence of individuals of these families in open dune formations and flooded areas, especially those of Cyperaceae that dominate these swampy environments.
The group of climbers is mostly represented by individuals of Fabaceae, which are mainly herbaceous vines; however, Apocynaceae, Bignoniaceae, Convolvulaceae and Dilleniaceae have numerous species with a lianescent life form.
There is a considerable difference in the richness recorded for the different phytophysiognomies. Dune fields and restinga forest are the richest, with up to 39.4% of the angiosperm flora in the restingas of Pará.  mainly Rhynchospora Vahl (7 spp.) and Xyris Gronov. ex L. (4 spp.).
Even with a small increase in sampling effort, together with advances in taxonomic knowledge, it is not uncommon for checklists and broader floristic studies to record new occurrences for many plant groups.
The present survey of restingas in Pará found 11 new records for the state, including

Discussion
In a survey conducted by Amaral et al. (2008), 365 species were recorded for the restingas of coastal Pará and Amapá, which corresponds to only 77.8% of the species listed here. In addition, these authors also included five species of ferns and lycophytes in their checklist.
The analysis of the flora of restingas of Pará indicates relatively low richness in relation to the coastal extension of the state, which is similar to the richness recorded in studies of restingas in states of the Northeast Region of Brazil when taking into account the differences in the length of the coastline of each state and the collection effort and inclusion criteria of the flora (vascular flora or only angiosperms  ; and 831 spp. for Sergipe (168 km) (Oliveira et al. 2014).
The difference in the richness between the restingas in Pará and those of the Northeast Region of Brazil also indicates a heterogeneous distribution of the records of the flora in these environments in the state, which is probably because the large coastal extension has resulted in collecting in the most accessible points compared to more expensive expeditions to less accessible areas. This can be seen when mapping the existing collections from restingas in the state, since a large part of the records are from the municipalities of Bragança, Marapanim and Macaranã, of which the latter two are geographically close (Fig. 1).
Based on expeditions conducted for this study, 11 species were confirmed that had never been cited for restingas of Pará (Tab. S1, available on supplementary material <https:// doi.org/10.6084/m9.figshare.13681750.v1>). However, new studies are still important to confirm the true floristic richness of coastal Pará, since they will fill knowledge gaps and directly affect the development of research about restinga species in different areas, resulting in a better understanding of the ecological dynamics of these environments.
The richest families recorded in this study are also the most relevant in lists of the restinga flora of the Northeast Region of Brazil, in which Fabaceae, Cyperaceae, Poaceae, Myrtaceae and Rubiaceae are always cited as having the greatest number of species Santos-Filho et al. 2011Gomes & Guedes 2014;Oliveira et al. 2014Oliveira et al. , 2015Almeida Jr. et al. 2017). Gentry (1988) cites Fabaceae as the dominant family in different Amazonian formations.
When comparing restingas of Pará to those of the Northeast Region, it is important to consider the variety and diversity of physiognomic typologies in each area. This factor directly influences not only species richness but also structural and taxonomic composition, resulting in differences in the composition of the richest families. For example, few floristic studies of restingas in the Northeast and Southeast regions of Brazil mention Polygalaceae among the 10 families with the greatest number of species (Souza et al. 2016;Almeida Jr. et al. 2017;Castelo & Braga 2017), indicating a peculiar difference exhibited by Amazonian restingas.
The richest family cited in restingas of the Northeast Region of Brazil is Fabaceae, which Rodriguésia 72: e01532019. 2021 is possibly because many representatives of the family exhibit great plasticity to different niches and easily grow under extreme nutritional conditions, mainly due to symbiosis with nitrogen fixing bacteria. In the present study, this family was recorded for all phytophysiognomies, from areas of rhizomatous psammophiles, herbaceous swamps and dune fields to restinga forest, where it is the group with the greatest number of species. Recently, Silva et al. (2019) confirmed 16 new occurrences of this family for restingas in Pará.
Cyperaceae and Poaceae are also dominant in restingas of the Northeast Region of Brazil, notably in the states of Ceará (Santos-Filho et al. 2011) and Sergipe (Oliveira et al. 2014) that have a similar richness compared to coastal Pará; for all three states, they are listed as some of the richest families in herbaceous swamps and dune fields. This is probably because representatives of these families easily reproduce and are wind dispersed in these environments, guaranteeing establishment in open formations with high luminosity (Almeida Jr. et al. 2009;Cantarelli et al. 2012).
Among the species endemic to Brazil that are cited for restingas of Pará, the following are notable: Swartzia brachyrachis var. snethlageae (Ducke) Ducke (Fabaceae), which is restricted to Pará (in formations of restinga, campinarana, igapó forest and terra firme forest) and Maranhão, although Almeida Jr. et al. (2017) does not cite restinga for this state; and Eleocharis bahiensis D.A.Simpson (Cyperaceae), which has a disjunct distribution in Pará and Bahia and is always associated with restinga vegetation, aquatic environments or rocky outgroups (Giulietti et al. 2009;Nunes et al. 2021). Giulietti et al. (2009) mentions that the latter species is rare and, at that moment, only known from the state of Bahia.
In the species listed as new records confirmed for the flora of Pará (Tab. S1, available on supplementary material <https://doi.org/10.6084/ m9.figshare.13681750.v1>), Cuphea flava Spreng. (Lythraceae) is notable for being endemic to Brazil and cited only for areas of restinga in the Northeast and Southeast regions (Cavalcanti et al. 2021). In restingas in Pará, this species has been recorded many times by specialists of the family. Asemeia rhodoptera (Mart. ex A.W.Benn.) J.F.B.Pastore & J.R.Abbott (Polygalaceae) is endemic to Brazil and cited as restricted to phytophysiognomies of the Cerrado, such as campo limpo and campo rupestre (Aguiar et al. 2008;Mota & Pastore 2021). It has only two confirmed records for restingas in Pará, which reinforces the need for floristic studies in poorly collected restingas of the state.
Four species of Ouratea Aubl. (Ochnaceae) were recorded for restingas of Pará. Two species are endemic to Brazil, Ouratea cassinifolia (A.DC.) Engl., which is only known from Pará and Maranhão (Flora do Brasil 2020), and Ouratea racemiformis Ule, which occurs in the states of Amazonas, Amapá, Pará and Maranhão (Amaral et al. 2008;Almeida Jr. et al. 2017;Flora do Brasil 2020). All confirmed records of both species are from costal or riparian areas.
Blutaparon Raf. (Amaranthaceae) is represented by only two species in Brazil (Senna 2021), Blutaparon portulacoides (A.St.-Hil.) Mears and Blutaparon vermiculare (L.) Mears, which are cited as exclusive to areas of restinga. The confirmation of the occurrence of these species for coastal Pará indicates that, although not endemic, the species are present the coastal Rio de Janeiro (Castelo & Braga 2017) to Maranhão (Serra et al. 2016;Almeida Jr. et al. 2017;Lima & Almeida Jr. 2018).
The occurrence of the same species in different areas of restinga along coastal Brazil might indicate that, to a greater or lesser degree, the vegetation of this environment plays a role as an ecological corridor among different phytogeographic domains. Amaral et al. (2015) noted the coexistence of species with different origins in an area of restinga in Pará. Most of the arboreal elements in this area originate from Amazonian vegetation formations and the shrubs, to an extent, are widely distributed species in Brazil. Serra et al. (2016)  Recently, Amaral et al. (2016) documented the first records of Curatella americana L. (Dilleniaceae) for coastal areas of Amazonia. In studies of continental restingas this species had never been mentioned. In the state, it was known only from restingas on Marajó Island, where there are many populations adjacent to areas of cerrado and it is a dominant species, indicting the possible influence of this vegetation on the colonization process of restinga areas in that region. This was observed for Polygalaceae. Of the eleven species in the family recorded for restingas of Pará, seven are abundant in areas of cerrado on Marajó Island (Costa 2012).
According to Flora do Brazil 2020, restingas of Pará are composed mostly of species that occur in both anthropic areas and many Amazonian habitats (terra firme forest and white sand vegetation), as well as other domains, such as the Atlantic Forest, Cerrado and Caatinga in the Northeast and Southeast regions of the country, demonstrating the importance of adjacent floras to the composition of restinga vegetation.
As indicated by Amaral et al. (2008), dune fields, herbaceous swamp and restinga forest are the physiognomic formations with the greatest richness in restingas of Pará. The first two mainly comprise herbaceous vegetation, since open formations predominate in restingas in the state. This allows areas to be colonized by a dynamic herbaceous vegetation cover, which is possibly regulated seasonally by rainfall and changes in the groundwater level. However, the forest formation is dominated by arboreal elements, less dynamic and predominantly regulated by edaphic conditions. Amaral et al. (2008), Almeida Jr. et al. (2009 and Santos-Filho et al. (2013) noted that these environmental characteristics directly influence the proportion of dominance of life forms in the different restinga physiognomies.
From an ecological perspective, the absence of endemism contrasts with the important diversity found in Amazonian restinga. Species that colonize geologically recent environments, such as restinga, make morphological, physiological and ecological adjustments to the severe climatic and nutritional conditions of these areas. This shows the value of genetic richness, which is still not taken into account in biological conservation strategies in Brazil (Scarano 2006). Thus, it is vital that the areas of restinga in Pará remain a priority for the conservation of biodiversity in the state.

Conclusions
We recorded the occurrence of 470 species of angiosperms in areas of restinga in coastal Pará, mainly species of Fabaceae, Cyperaceae, Poaceae, Myrtaceae and Rubiaceae. Dune fields and restinga forest had the greatest richness among the phytophysiognomies. This work is a survey that updated what is known about the restinga flora of Pará, based on a study from 10 years ago, and the 11 new occurrences reported are important results. Further, significant areas of this vegetation are still poorly explored. It was found that in the last decade there was an intensification of collecting in areas already widely visited, except for coastal restinga of Marajó Island that was surveyed more recently, resulting in a better understanding of this environment. In general, we hope this work contributes to advances in research and effective management and conservation strategies related to restingas, which are important environments in Amazonia.