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Articles • Acta Bot. Bras. 33 (3) • Jul-Sep 2019 • https://doi.org/10.1590/0102-33062018abb0421 linkcopy

Open-access Vascular flora of Lençóis Maranhenses National Park, Maranhão State, Brazil: checklist, floristic affinities and phytophysiognomies of restingas in the municipality of Barreirinhas

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    ABSTRACT

    This study presents a floristic survey of the vascular plants of restingas of Lençóis Maranheses National Park, in the municipality of Barreirinhas, Maranhão, Brazil, including descriptions of the principal phytophysiognomies and similarity analyses including other restinga areas in North and Northeastern Brazil. Samples from the study area deposited in the herbaria MG, IAN and MAR were inventoried and fieldwork for the collection of additional botanical samples was undertaken between September 2015 and August 2017. Unweighted pair group method with arithmetic mean (UPGMA) using Jaccard index was used to calculate the similarity among floras of the restingas of the states of Pará, Piauí, Ceará and Maranhão. A total of 289 species in 189 genera and 73 families was recorded, including 56 new occurence records for the state of Maranhão. The richest families were Poaceae, Cyperaceae, Fabaceae, Rubiaceae, Eriocaulaceae and Myrtaceae. Similarity indexes revealed low similarity among the selected areas, suggesting high floristic identity for each area, as well as possible collection bias among the areas.

    Keywords: dunes; floristics; new occurrence records; seed plants; white sand vegetation

    Introduction

    Maranhão state is situated in the Northeastern region of Brazil and occupies an area of more than 330,000 km2. It is situated within an area of transition between three different biomes: Cerrado, Amazon and Caatinga (Aragão & Conceição 2008). Among the different vegetation types found in this state, the restinga is a coastal scrub occurring always along the sandy coast in the Amazon and Atlantic Forest biomes (Maranhão 2002).

    In the northeastern region of Maranhão state there is an extensive area dominated by sandy sedimentary eolic deposits occupying approximately 18,000 km2 concentrated in the coastal region (Bandeira 2013). This area is situated in the transition between the three biomes found in the state, forming a mosaic of environments associated with sandy ecosystems, considered unique in Brazil (Saraiva & Fernandes-Pinto 2007). According to the Brazilian vegetation map (IBGE 2012), this area is dominated by pioneering formations with the occurence of vegetation with a marine influence (restingas, mangroves), associated with savannas and tension zones between savanna and seasonal forest (Castro & Piorski 2002). Situated in this region, the Lençóis Maranhenses National Park (PNLM) is considered a 'tropical desert' constituted by extensive dunes and thousands of freshwater lakes (Damme & Dumont 2010), of notable scenic beauty. According to Moschini-Carlos et al. (2008), the Lençóis Maranhenses correspond to a single series of dunes that extend from the Gulf of Maranhão up to the Parnaíba river, begining at the coast and advancing towards the continent for around 50 km, influenced by river courses and the sea.

    A total of 3064 species of Angiosperm are attributed to Maranhão state, ranking as 19th in floristic richness amonst the states of Brazil (Flora do Brasil 2020 2018). Despite including part of three major Brazilian biomes, the flora documented in Maranhão corresponds to only a little more than 9 % of the Brazilian flora (Flora do Brasil 2020 2018). Important studies on coastal vegetation in the state of Maranhão were carried out, such as those of Araújo et al. (2016) and Lima & Almeida Júnior (2018). However, collection efforts are necessary to enhance the extant collections and in order to produce more precise evaluation of the state's floristic composition.

    Floristic inventories were carried out in some restinga areas in Maranhão (Serra et al. 2016; Almeida Júnior et al. 2017; Lima & Almeida Júnior 2018), however, few studies on the flora have been developed specifically for the PNLM, apart from some scattered specimens deposited in herbaria, and the study by Moschini-Carlos et al. (2008), that describe the morphometric, physical and chemical variables of the ponds in PNLM, with emphasis on the planktonic community. Despite the importance of these studies, knowledge of the park’s flora remains elementary.

    The objective of this paper is to complete a first survey of the vascular flora in the Lençóis Maranhenses National Park, municipality of Barreirinhas, including a description of the principal phytophysiognomies as well as to carry out floristic comparisons with other restingas in the North and Northeastern regions of Brazil.

    Materials and methods

    Study area

    This study was carried out in the Lençóis Maranhenses National Park (PLNM) located on the eastern coast of the state, 2°38’24”S 42°50’48”W (Fig. 1). The PNLM, established 2nd June 1981 by decree number 86,060 (ICMBIO 2016), consists of around 155 thousand hectares dominated by areas of restinga, encompassing the municipalities of Primeira Cruz, Santo Amaro and Barreirinhas. The sampling was restricted to the municipality of Barreirinhas, within the PNLM, covering 302 hectares. The average annual temperature of the region is 28.5 ºC, with most frequent precipitation in February and May, and a dry season from June to January (Miranda et al. 2012; ICMBIO 2016). Considered a transition zone between the semi-arid climate and equatorial humidity, the landscape of the Lençóis Maranhenses is shaped by rivers carrying sediments in the direction of the coast, causing the formation of the restingas in these zones. These landscapes are characteristic to the region and consist of white dunes populated by a particular vegetation (Moschini-Carlos & Pompêo 2016). This vegetation is composed of a mosaic of phytophysiognomies, generally dominated by coastal environments such as restingas and mangroves. Considering its peculiar phytophysiognomies, a brief description of the types found within the study area is proposed in this work, adapted from Bastos (1995) and Bastos et al. (2003) for the restingas of coastal Pará state.

    Figure 1
    Map showing the study area: municipality of Barreirinhas in the Lençóis Maranhenses National Park.

    Botanical collections and herborization

    Seven expeditions for the collection of botanical material, each lasting at least five days, were carried out from September 2015 to December 2017, considering dry and wet periods. Collections were restricted to vascular plants, seeking to sample all of the habitats of the study area. Only fertile samples were collected. The samples were herborized according to appropriate techniques (Fidalgo & Bononi 1989; IBGE 2012; Walter & Fagg 2015) and incorporated into the MG Herbarium (herbarium acronyms according to Thiers 2009).

    Herbarium survey

    Parallel to the fieldwork, collections of the herbaria MG, IAN, and MAR were studied and inventoried, seeking samples from the municipality of Barreirinhas with the aim of adding them to the PNLM database that was used to generate the species list presented in this work.

    Identification of botanical samples

    The collections studied were identified with reference to the relevant taxonomical bibliography; comparison with samples previously deposited in the Herbarium MG and identified by specialists; and, when necessary, duplicates were sent to specialists to confirm the identifications.

    Preparation of species list

    Based on the specimen database from the study area, a list of vascular plants was generated, alphabetically organized according to family, indicating, for each species: voucher (collector + collector number + herbarium); distribution in Brazil by biome based on the Flora of Brazil online 2020 (Flora do Brasil 2020 2018); habitat, based on the description of the vegetation proposed here, and habit, based on the categories followed by Flora do Brasil 2020 (2018).

    The angiosperm list follows the APG IV (2016) classification system, with exception of Cordiaceae and Heliotropiaceae kept apart from Boraginaceae s.l. (BWG 2016) and Passifloraceae s.s. For ferns, Smith et al. (2006) and Rothfels et al. (2012) were followed, while for the lycophytes, Kramer & Green (1990).

    The species list of the PNLM was compared with the threatened species list for the flora of Brazil online (MMA 2014), available at the National Centre of Conservation of Flora, for the confirmation of the occurrence of species threatened with extinction in the study area (CNCFLORA 2018).

    Similarity analysis

    The floristic composition of the area studied was compared with surveys completed in areas of restinga Northern and Northeastern Brazil: data from two areas in the state of Pará, in the municipalities of Algodoal/Maiandeua and Crispim/Marapanim (Amaral et al. 2008) were compiled and merged into a list for Pará state restingas; a first compilation of the vascular flora of the restingas in Maranhão state, based on herbarium survey (Almeida Júnior et al. 2017); restingas in Piauí state, in the municipalities of Ilha Grande, Parnaíba, Luís Correia and Cajueiro da Praia (Santos-Filho et al. 2015); and a checklist of the restingas in the state of Ceará (Santos-Filho et al. 2011). All of these listings had synonymy adjusted manually according to consultation of the Flora of Brazil 2020 database. Imprecisely identified (cf. or aff.) or material not identified to species level was excluded from the analysis. The species lists of the compared areas are available as supplementary material. The similarity analysis was completed utilizing the Jaccard index (Sneath & Sokal 1973), by the non-weighted pair method with Arithmetic Mean (UPGMA).

    Results

    Checklist

    The specimens compiled from the studied herbaria comprised 59 herbarium sheets from MG, 154 from IAN and 347 from MAR. The fieldwork contributed 525 samples, which are deposited in MG, thus totalling 1085 materials from the Barreirinhas municipality.

    The analysis of these samples revealed the occurrence of 289 species, consisting of 286 angiosperms, two ferns and one lycophyte. Within the angiosperms, 63 % of the species are Eudicots (178 species), 36 % are Monocots (105 species) and 1 % of the group belongs to the Magnoliids (three species, Tab. 1).

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    Table 1
    Checklist of the vascular plant species in the Lençóis Maranhenses National Park Barreirinhas, Maranhão state, Brazil. Abbreviations for collector names: Mo = N.F.O. Mota; S = O. Silva; Marc = M.C.F.V. dos Santos; Mt = K.L.Martins; M = R.C. de Mendonça; B = J.M.Brito; Ca = G.C.A Carvalho; La = D.M.A Lacerda; Sa = S.M. Santos; Ex = E.F.B. de Carvalho; Cb = C. Cabral; Me = F.N.Mendes; Rm = M.C.Ramos; Rh = R. Henriques; O = R.P. Orlandi; Bo = C.B. de A. Bohrer; R = M.L. Rodrigues. Biomes: Amz = Amazon rainforest; Atl = Atlantic rainforest; Caa = Caatinga; Cer = Cerrado; Pmp = Pampa; Pnt = Pantanal. Habitats: Hv = Halophytic Vegetation; Rfi = Restinga fields; Sr = Shrubby Restinga; Sc = Scrub; Il = Interdunal lagoons; Rfo = Restinga forest; Cf = Cocais forest; Gf = Gallery forest and Mangroves. Habits: He = Herb; Sh = Shrub; Tr = Tree; Vi = Vine. First records for the state of Maranhão are assigned with +, endangered species with *.

    The 289 recorded species are distributed in 189 genera and 73 families (Tab. 1), and the most representative families were Poaceae with 37 species (12 %), Cyperaceae 35 ssp. (12 %), Fabaceae 31 spp. (10 %), Rubiaceae 17 spp. (5 %), Eriocaulaceae ten spp. (3 %), Myrtaceae nine spp. (3 %), Apocynaceae and Polygalaceae eight spp. (2 %), Xyridaceae seven spp. (2 %) and Euphorbiaceae six spp. (2 %) (Fig. 2).

    Figure 2
    Richest families and genera of PNLM. Number of species for each taxon in parentheses.

    The predominant habit was herbaceous, with 53.28 % of the species, followed by shrubs and trees, with 13.14 % and 12.45 %, respectively. Representing less than 8 % of the species, the lianescent habit was the least abundant in the study area (Fig. 3).

    Figure 3
    Habits of the species occurring in the PNLM.

    In this study, 56 new species records were made for Maranhão state (Tab. 1), including 15 species widely distributed in Brazil: Actinostachys pennula (Schizaeaceae), Calophyllum brasiliense (Calophyllaceae), Rhynchospora filiformis (Cyperaceae), Eriocaulon cinereum (Eriocaulaceae), Centrosema pascuorum (Fabaceae), Utricularia myriocista (Lentibulariaceae), Heteropterys nervosa (Malpighiaceae), Mayaca longipes (Mayacaceae), Myrciaria floribunda (Myrtaceae), Paspalum pumilum, Trichanthecium polycomum, Sacciolepis vilvoides (Poaceae), and Spermacoce prostrata (Rubiaceae) (Flora do Brasil 2020 2018).

    Two undescribed species were recorded, Mesosetum sp. nov. (Poaceae) and Xyris sp. nov. (Xyridaceae), which are undergoing description prior to publication. The only species considered threatened with extinction, in the endangered (EN) category, was Bacopa cochlearia (MMA 2014), with only one record for the PNLM, referring to an interdunal lagoon (Lagoa Azul).

    Description of phytophysiognomies

    The vegetation in the study area is classified here under eight distinct phytophysiognomies, occurring with most frequency in the PNLM and characterized as following:

    1) Halophytic Vegetation: tidal areas with plants that have some resistance to salinity (Fig. 4A-B). In this formation we can observe herbaceous plants such as Blutaparon portulacoides (Amaranthaceae), Cyperus articulatus, C. obtusatus, C. subsquarrosus, Eleocharis geniculata (Cyperaceae), Paspalum vaginatum, Spartina alternifolia, Sporobolus virginicus (Poaceae), and sparse shrubs of Conocarpus erectus (Combretaceae);

    Figure 4
    Main phytophysiognomies of the PNLM. A-B. Halophytic vegetation. C-D. Scrub. E-F. Interdunal Lagoons. Photographs by Pedro Viana (A-C, E-F) and Nara Mota (D).

    2) Scrub: Scrub formations around dunes are generally localized on top of dunes, composed of gnarled trees and shrubs, many times with stems completely buried in sand (Fig. 4C-D). Common shrub species include Anacardium occidentale (Anacardiaceae), Chrysobalanus icaco (Chrysobalanaceae), Chamaecrista flexuosa and Indigofera microcarpa (Fabaceae), Byrsonima laevis and B. sericea (Malpighiaceae), Mouriri guianensis (Melastomataceae). Within the herbaceous species, Cyperus crassipes and Rhynchospora tenuis (Cyperaceae), Chamaecrista flexuosa and Indigofera microcarpa (Fabaceae) and Trachypogon spicatus (Poaceae) stand out;

    3) Interdunal lagoons: lagoons/ ponds that form as a result of the accumulation of precipitation during the rainy period (Fig. 4E-F). These water bodies present vegetation constituted primarily by annual herbs, such as Helantium tenellum (Alismataceae), Eriocaulon cinereum, E. setaceum and Paepalanthus sessiliflorus (Eriocaulaceae), Schultesia guianensis (Gentianaceae), Utricularia cornuta and U. subulata (Lentibulariaceae), Bacopa cochlearia (Plantaginaceae), Xyris jupicai and Xyris sp. nov. (Xyridaceae) that appear in the margins of the lagoons at the beginning of the dry period and dominate the entire bed of the lagoon in the peak of drought, when they are completely empty. Few perennial species are observed in this environment, though Panicum aquaticum (Poaceae) and Nymphoides humboldtiana (Menyanthaceae) are generally found in the lagoons during the rainy season;

    4) Restinga fields: Hydromorphic fields or sandy marshes of oligotrophic soils with mostly continuous stratum (Fig. 5A-B). During the rainy season they can become flooded and are also characterized by a large number of annual species such as Burmania capitata (Burmaniceae), Drosera sessilifolia (Droseraceae), Paepalanthus bifidus, P. polytrichoides and Syngonanthus cuyabenses (Eriocaulaceae), Utricularia benjaminiana and U. myriocista (Lentibulariaceae), Polygala adenophora (Polygalaceae), Habenaria spp. (Orchidaceae), Xyris paraensis (Xyridaceae), amongst others. Herbaceous perennial species are also observed, including Euploca polyphylla (Heliotropiaceae), Gomphrena sp. (Amaranthaceae), Bulbostylis conifera, B. junciformis, Cyperus haspan, Lagenocarpus spp. (Cyperaceae), Abolboda pulchella (Xyridaceae), Tetraulacium veroniciforme (Plantaginaceae). Within these, shrub species Krameria tomentosa (Krameriaceae), Cuphea antisyphilitica (Lythraceae), Comolia villosa (Melastomataceae) and Dizygostemon sp. (Plantaginaceae) stand out;

    Figure 5
    Main phytophysiognomies of the PNLM. A-B. Restinga fields. C. Shruby Restinga. D. Shruby Restinga and in the background restinga forest. E. Gallery Forest. F. River Preguiça mouth, showing the mangrove. Photographs by Nara Mota (A-D) and Pedro Viana (E-F).

    5) Shrubby Restinga: an area formed from both continuous and discontinuous ground cover, with a higher frequency of shrubs and isolated trees, also forming clumps, with physiognomy resembling Cerrado sensu strictu (Fig. 5C). Within the tree and shrub species, Himatanthus articulatus (Apocynaceae), Monteverdia erythroxyla (Celastraceae), Chrysobalanus icaco (Chrysobalanaceae), Clusia grandiflora (Clusiaceae), Humiria balsamifera (Humiriaceae), Vismia guianensis (Hypericaceae), Byrsonima sericea (Malpighiaceae), Eugenia punicifolia (Myrtaceae) and Ouratea caudata (Ochnaceae) stand out. Lagenocarpus guianensis (Cyperaceae), Andropogon leucostachyus, Mesosetum loliiforme, Paspalum carinatum, Streptostachys asperifolia (Poaceae) are some of the herbaceous species found in this phytophysiognomy. Lianescent species are frequently observed, such as Mandevilla hirsuta and M. scabra (Apocynaceae), Ipomoea spp. (Convolvulaceae), Davilla cearensis and Doliocarpus spraguei (Dilleniaceae), and Passiflora foetida (Passifloraceae);

    6) Restinga forest: formed by a dense layer of trees and shrubs, producing a continuous canopy. Generally, presents individuals with thin, gnarled trunks growing on ground with accumulated organic material, and this is loose in comparison to what is seen in open restinga. Another defining characteristic of species is their pronounced deciduousness, with a xeromorphic aspect (Fig. 5D). In this formation the prominent presence of Protium heptaphyllum subsp. ulei (Burseraceae), Caryocar brasiliense (Caryocaraceae), Abarema cochleata, Andira vermifuga, Copaifera martii, Dimorphandra gardneriana and Hymenaea velutina (Fabaceae), Myrcia multiflora and Myrcia splendens (Myrtaceae), Matayba discolor (Sapindaceae), Manilkara triflora (Sapotaceae) are observed;

    7) Cocais forest: phytophysiognomy characterized by the abundant presence of palms Copernicia prunifera, occasionally occurring sympatrically with Mauritia flexuosa.

    8) Gallery forest and Mangroves: vegetation occurring in the banks of the Preguiça River and its tributaries (Fig. 5E). Proximity to the ocean determines the composition of species of this physiognomy. Close to the estuary, the vegetation is typically of mangroves with low species richness and the predominance of few tree species (Fig. 5F), such as Rhizophora harrisonii and R. racemosa (Rhizophoraceae). As distance from the ocean increases and salinity falls, the species richness increases, and species of Arecaceae, such as Mauritia flexuosa, some Annonaceae and Araceae can be observed.

    Floristic similarity

    The similarity indexes calculated between the areas (Tab. 2) ranged from 0.082 (Pará and Piauí states restingas) to 0.197 (this study and Pará state restingas). According to Kent & Coker (1992), values larger than or equal to 0.5 indicate high similarity. Therefore, it can be inferred that the similarity between the areas is to be considered low.

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    Table 2
    Matrix of similarity coefficients (Jaccard) between the compared areas. Barreirinhas: this study; Pará state: Algodoal/Maiandeua and Crispim/Marapanim (Amaral et al. 2008); Piauí state (Santos-Filho et al. 2015); Maranhão state (Almeida Junior et al. 2017); Ceará state (Santos-Filho et al. 2011).

    The clustering analysis (Fig. 6) revealed a group formed between the study area and restingas of Pará state, which, in turn, is related with the restingas of Maranhão, but with low similarity (similarity index 0.178).

    Figure 6
    Dendogram of Floristic Similarity between the study areas analysed: Barreirinhas: this study; Pará state: Algodoal/Maiandeua and Crispim/Marapanim (Amaral et al. 2008); Piauí state (Santos-Filho et al. 2015); Maranhão state (Almeida Junior et al. 2017); Ceará state (Santos-Filho et al. 2011).

    Discussion

    The families with higher species richness in this research coincide with the richest families for other studies of Brazilian restingas (Araújo 2000; Pereira & Araújo 2000; Santos et al. 2003; Almeida Júnior et al. 2007; 2017; Amaral et al. 2008; Santos-Filho et al. 2011; 2015; Gomes & Guedes 2014; Serra et al. 2016). According to Melo Júnior & Boeger (2015), families like Fabaceae and Myrtaceae present high numbers of species in the restinga. Amaral et al. (2008) detected Fabaceae, Poaceae and Cyperaceae as the richest families on the restinga in Pará and Amapá states.

    The low number of fern species and lycophytes may be explained by the biological particularities of these groups, which are largely dependent on factors such as the climate, availability of water and substrate type (Gonzatti et al. 2014). The PNLM presents a longer period of drought, associated with sandy soil with low water retention, which can discourage the establishment of fern and lycophyte species.

    Although southeastern Maranhão is considered one of the largest knowledge gaps for the understanding of the Brazilian flora (BFG 2015), the presence of 56 new records for the state within the PNLM, along with the two new species (Tab. 1), demonstrates that, in reality, the whole of Maranhão state, including the restingas (Zickel et al. 2004; Ribeiro 2011) represents a huge knowledge gap and needs careful botanical exploration. There is a need for botanical research into the different vegetal formations of Maranhão to better understand the floristic richness of the state.

    The breakdown of the new records found within this work is interesting. Some were previously cited predominantly for the Amazon biome: Paepalanthus polytrichoides (Eriocaulaceae), Doliocarpus spraguei (Dilleniaceae), Leptolobium nitens, Vatairea sericea (Fabaceae), Eschweilera decolorans (Lecythidaceae), Utricularia benjaminiana (Lentibulariaceae), Borreria paraensis, Duroia paraensis (Rubiaceae), Ternstroemia delicatula (Pentaphyllaceae), Eragrostis guianensis, Reimarochloa aberrans, Rhytachne guianensis (Poaceae). Four were cited, in Brazil, for the Cerrado: Lepidaploa rufogrisea (Asteraceae), Bulbostylis lagoensis (Cyperaceae), Syngonanthus philodicoides (Eriocaulaceae), Asemeia rhodoptera (Polygalaceae). Finally, three were previously cited for the Caatinga biome: Stilpnopappus cearensis (Asteraceae), Rhynchospora curvula (Cyperaceae) and Bacopa cochlearia (Plantaginaceae). These results demonstrate how these three biomes contribute to the composition of the PNLM flora, revealing its ecotonal character (Santos-Filho et al. 2013a). In this way, different features and plant synusia typical of the mid-Northern region of Brazil can be found, accompanied by corresponding soil and climate variations (Santos-Filho et al. 2013b).

    In relation to the species habit, the data was found to be similar to other flora studies of restingas in Northern and Northeastern Brazil (e.g. Amaral et al. 2008; Santos-Filho et al. 2015; Oliveira et al. 2015), with the predominance of herbaceous species, followed by shrub and tree species, reinforcing the vegetation classification of the region (sensuIBGE 2012) as pioneer formations, with a higher number of species adapted to survive in adverse situation (Oliveira et al. 2015). According to Martins & Batalha (2011) herbs, in general, present the best resistence to drought, withstanding high luminosity and strong winds, making it possible for them to survive in different restinga physiognomies in the PNLM. The high similarity between the restinga flora in PNLM Barreirinhas and the restingas in Pará state suggests the colonization of coastal areas of Maranhão from the Amazon biome. These facts are also corroborated by the new records the PNLM flora, where the Amazonian Rainforest contributes with the largest number of exclusive species (12 spp.), when compared with the Cerrado and Caatinga (four species each).

    The similarity of PNLM flora with the areas compared in this study is considered low. This panorama can be explained by the location of PNLM, which is an area of transition between three biomes. In the study area they were recorded as species from the Amazon, Caatinga and Cerrado, revealing a unique character towards its flora. Compared with areas of restinga found exclusively in the Caatinga or Amazon biomes, the similarity of PNLM flora is clearly demonstrated to be low. Nevertheless, these results could be influenced by eventual discrepancies in the sampling efforts utilized in the different studies.

    Based on these results it may be concluded that the restingas of the PNLM in the municipality of Barreirinhas present a high number of species, including many that have not been previously recorded from Maranhão. This high number of new records highlights the necessity to increase collections in Maranhão state, including all its plant formations. The peculiarity of the flora in the study area was revealed through the occurrence of new species. The low similarity with other areas of restinga studied justifies the importance of continuing floristic studies in the PNLM, especially in areas not covered by the present study.

    Acknowledgements

    Thanks to the Museu Paraense Emílio Goeldi and the Universidade Federal Rural da Amazônia; ICMBio in Barreirinhas; the curators of the IAN (EMBRAPA), MAR (Universidade Federal do Maranhão) and MG (Museu Paraense Emílio Goeldi) herbaria; the specialists identifiers and Temístocles Rodrigues. We thank Vanessa Zappi-Taylor and Daniela C. Zappi for the English version. This study received financial support from the CAPES no. PRO-Amazônia 3268/2013.

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    Publication Dates

    • Publication in this collection
      12 Sept 2019
    • Date of issue
      Jul-Sep 2019

    History

    • Received
      07 Dec 2018
    • Accepted
      21 May 2019
    Creative Common - by 4.0
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