Edaphic Endemism in the Amazon: Vascular Plants of the canga of Carajas, Brazil.
Biodiversity loss, mainly attributed to habitat change and over-exploitation, pollution and invasive species (Marchese, 2015), demands urgent strategies to protect native species. Severe threats to natural habitats lead to current estimates suggesting that one in five of the world's plant species is threatened with extinction globally (Brummitt et al., 2015; Darbyshire et al., 2017). The presence of endangered, endemic and rare taxa in conjunction with species diversity is used to define Key Biodiversity Areas (KBAs) or Important Plant Areas (IPAs) around the globe, many of them focusing on tropical mountains (Harold & Mooi, 1994; Eken et al., 2004; Kasecker et al., 2009; Darbyshire et al., 2017). The KBA are interconnected sites that are large enough to support species for which they are important (Eken et al., 2004; Bakarr et al., 2007). Efforts to combine IPAs with zoological groups (Important Bird Areas) to evidence KBAs have been carried out for some countries in Europe (Melovski et al, 2012). The flora of these areas is often unique and represents a highly relevant reserve of biodiversity for the global prioritization of conservation efforts (Kier et al., 2005; Merckx et al., 2015). Recent studies show that between 26 and 49% of the plants found in the Atlas Mountains are endemic and strongly correlated to the altitudinal range (Rankou et al., 2013). In Brazil, the recognition of 752 KBAs by Kasecker et al. (2009) highlights 149 areas within the Amazon Rainforest biome, where the Serra dos Carajas is evidenced as a KBA with basis on 10 locally found rare species.
Analogous to the south-western Australian Banded Iron Formations (BIFs), the canga or ironstone formations in Brazil are considered ancient ecosystems, characterized by a rich savanna-like flora associated with the decomposition of the iron-rich substrate (Gibson et al., 2017; Nunes et al., 2015; Viana et al., 2016). In both countries, such areas provide unique island-like environments with high levels of species turnover between different sites, high levels of endemism and rare geographically restricted species (Gibson et al., 2010; Jacobi et al., 2007; Mota et al., 2018; Viana et al., 2016; Zappi et al., 2017b). Brazil is second only to Australia in mining and exportation of iron ore, creating many challenges for conservation of the vegetation growing in these areas (Gibson et al., 2017, 2010; Zappi et al., 2017b), and Carajas is the largest iron-ore reserve in the world (Duddu, 2014). In Brazil, campo rupestre, an open vegetation growing on a range of different rock types, generally found at the top of the mountains, has long been recognized as a distinct vegetation type (Silveira et al., 2016), while the iron-rich conglomerate is known as canga. Campo rupestre on canga (CRC hereafter) is found in the region of the Serra dos Carajas, in the state of Para, one of the largest mineral provinces in the world, imbedded within the Amazon Rainforest (Viana et al., 2016), among other sites. In the case of the Serra dos Carajas, these open habitats are immersed in a forest matrix and isolated by altitude and substrate (Mota et al., 2015; Viana et al., 2016). The different surrounding vegetation isolates the open vegetation, precluding or decreasing gene flow between mountain tops, where distinct drivers create special conditions of speciation in the campo rupestre (Lanes et al., 2018; Moraes et al., 2012; Pereira et al., 2007).
The first botanical investigations of the CRC of the Serra dos Carajas date back to 1969, when botanists of the Museu Paraense Emilio Goeldi (MPEG) studied the area that corresponds today to the Carajas National Forest (FLONA of Carajas), created in February 1998 (Viana et al., 2016). The first list for this region included 232 species from 58 plant families (Silva et al., 1996). In January 2015, a multi-institutional project lead by Instituto Tecnologico Vale and Museu Paraense Emilio Goeldi to develop a complete Flora of the canga of the Serra dos Carajas was launched, and 116 families with 856 species of seed plants authenticated by almost 130 botanists worldwide were written up (Mota et al., 2018), in addition to 186 fern and lycophytes (Salino & Almeida, 2018) and 89 bryophytes (Oliveira-da-Silva & Ilkiu-Borges, 2018). The comprehensive floristic account represents an appropriate baseline to fill the local knowledge gap and to contribute towards the challenge of getting to know the plant diversity of the Amazon (Brazil Flora Group [BFG], 2015; Cardoso et al., 2017). Moreover, it addresses most of the difficulties to define or identify endemic species listed by Ferreira & Boldrini (2011), namely missing taxonomic and distribution data, scant sampling efforts, distributions associated with political and not ecological delimitation, and geographical extent being often underestimated.
Research developed both in the BIFs and CRC have highlighted considerable flora and fauna endemism (Borsali, 2012; Conceicao et al., 2016; Gibson et al., 2017; Jacobi et al., 2007; Mota et al., 2018; Viana et al., 2016). Sustainable use of these areas implies investing time and effort to record and study the local biodiversity in order to determine authoritatively which species are to be considered important in terms of conservation (endemic, rare or threatened). In Brazil, the Codigo Florestal regulates the use of forests (MMA, 2012) aiming to protect the native vegetation, highlighting the protection of endemic, rare and endangered species within the planning and development of projects that affect natural habitats. The Codigo Florestal also determines that any project proposal involving land use and exploitation has to support the conservation of the biota and environmental services associated with the target area in order to minimize environmental impact (Feistauer et al., 2014).
In this study, we aim to i) establish a baseline of the edaphic endemism and investigate the rarity of these plant species occurring in the CRC at Carajas; ii) assess these plant species in the Serra dos Carajas using Species Distribution Modelling (SDM); iii) considering endemism and high biodiversity are not always positively correlated (Lamoreux et al., 2006), we investigate this aspect in the CRC of Carajas; and iv) develop a basis to guide multi-disciplinary research towards protecting endemic and rare species in the CRC of Carajas and worldwide.
The Serra dos Carajas spreads over 250 km East-West in southeastern Para and comprises several distinct plateaus at altitudes between 600 and 760 m a.s.l. (Fig. 1). A series of conservation units with different protection categories encompass the majority of the remaining forests of the region, covering approx. 12,000 [km.sup.2] (STCP, 2003; Viana et al., 2016). The Floresta Nacional de Carajas, or FLONA of Carajas, and the recently created Parque Nacional dos Campos Ferruginosos, or PNCF (June 2017) represent two major conservation areas including parts of the municipalities of Parauapebas and Canaa dos Carajas. Within these areas, vast sways of tall forest surround mountain-tops that are rich in iron-ore, where the campos rupestres on canga occur. The total area of CRC in the region of Carajas is 115.8 [km.sup.2], of which 77 [km.sup.2] are distributed between two main areas: Serra Norte and Serra Sul outcrops, included in the FLONA of Carajas (Souza-Filho et al., 2019) and are estimated to cover around 5% of this total area (STCP, 2016). The remaining canga areas occur within the PNCF, namely the Serra do Tarzan and Serra da Bocaina, while some are found outside protected areas, such as the Serra Arqueada, Serra do Cristalino, Serra Leste and Serra de Campos--Sao Felix do Xingu (Souza-Filho et al., 2019).
Assessment of endemism and rarity
There is no universal methodology to determine whether a species is endemic to a given place apart from the study of its distribution. Herewith we considered as locally endemic of the CRC of Carajas all vascular plants growing within the limits of the canga vegetation, but not the plants that also grow on other substrates on open vegetation (e.g. granitic outcrops) or in the forest below or surrounding the iron-ore outcrops, in an attempt to follow the concept of edaphic endemism (Shaw, 1989; Kruckenberg, 2002), where a plant species remains faithful to a specific substrate throughout its distribution. To our best knowledge, only plants growing on canga, be it in grooves or in the transition areas, were included. Twenty-seven one-week field expeditions to locate putative endemic species were carried out between May 2016 and March 2018 (Table 1, Fig. 2). The following steps were taken in order to list all the taxa referred to as endemic from the CRC of Carajas:
Herbarium and Protologue Searches
Searches in the following herbaria BHCB, HCJS, IAN, INPA, MBM, MG, NY and RB (acronyms according to Thiers (2011) were carried out to locate type-specimens collected in Carajas (search terms used were "type" or "types" and "Maraba" or "Parauapebas" or "Canaa dos Carajas" or "Serra dos Carajas" or "Carajas"). Supplementary searches were performed in the Global Plants Database (JStor, 2018) and SCOPUS Database (SCOPUS, 2018) to include plant-specimens housed in less obvious collections. Twenty recently described taxa were also brought to our attention by the authors themselves (Table SI). Protologues for all taxa found were obtained to verify that the type-specimens were from the region and to assess the total species distribution. An initial list was produced (Table S2, 73 taxa) then refined to prepare a list of "putative endemics" where the distribution given at the point of description of the taxa was only Carajas (Table S3, 59 taxa).
The resulting list (Table S3) was compared with the Brazilian Red List of Plants (Martinelli & Moraes, 2013) and Rare Plants from Brazil (Giulietti et al., 2009) in order to check whether the taxa were already classified as threatened or considered rare. Further distribution comparisons were made with already published data from the Flora of the canga of the Serra dos Carajas series, chiefly from the following families: Apocynaceae, 2 pp. (Fernandes et al., 2018), Araceae, 1 sp. (Coelho, 2018), Asteraceae, 4 spp. (Cruz et al, 2016), Bignoniaceae, 2 spp. (Lohmann et al., 2018), Blechnaceae (Salino et al., 2017), Convolvulaceae, 3 spp. (Simao-Bianchini et al., 2016), Cyperaceae, 3 spp. (Nunes et al., 2016), Eriocaulaceae, 2 spp. (Watanabe et al., 2017), Erythroxylaceae, 2 spp. (Costa-Lima & Loiola, 2018), Gentianaceae, 1 sp. (Guimaraes et al., 2018), Gesneriaceae, 1 sp. (Chautems et al., 2018), Isoetaceae, 2 spp. (Pereira et al., 2017), Leguminosae, 4 spp. (Mattos et al., 2018), Lentibulariaceae, 1 sp. (Mota & Zappi, 2018), Lythraceae, 1 sp. (Cavalcanti et al., 2016), Melastomataceae, 3 spp. (Rocha et al., 2017), Orchidaceae, 2 spp. (Koch et al.,
2018), Orobanchaceae, 1 spp. (Scatigna & Mota, 2017), Picramniaceae, 1 sp. (Pirani & Devecchi, 2016), Piperaceae, 2 spp. (Monteiro, 2018), Poaceae, 4 spp. (Viana et al., 2018), Rubiaceae, 7 spp. (Zappi et al., 2017a), Rutaceae, 1 sp. (Pirani & Devecchi, 2018), Sapotaceae (Terra-Araujo & Zappi, 2018), Selaginellaceae (Goes-Neto et al., 2016), Styracaceae (Viana & Mota, 2016), Thymelaeaceae, 1 spp. (Mota & Giulietti, 2016), Vitaceae (Lombardi, 2016) and Xyridaceae, 1 spp. (Mota & Wanderley, 2016).
The rarity of the taxa confirmed as edaphic endemics was ascertained, using the criteria recommended by Rapini et al. (2009), that considers as rare the plant species with records of up to 150 km distance between each other and distributed over an area up to 10,000 [km.sup.2]. This area is equivalent to the Extent of Occurrence (EOO) used by IUCN (2014) to prepare conservation assessments. Likewise, the Area of Occupancy (AOO) used by IUCN (2014) was ascertained. The endemic species were classified as Highly Restricted Endemic (HRE)--with <100 [km.sup.2] of EOO or Range Restricted Endemic (RRE)--with <5000 [km.sup.2] but >100 [km.sup.2] of EOO (Darbyshire et al., 2017). Distances between outcrops are shown in Fig. 3.
Species distribution model forecasts potential distributional areas based on environmental conditions where species were found (Elith & Leathwick, 2009), representing the most suitable areas for species occurrence (Phillips, 2008). We relied on a previous potential distribution model prepared for Amazonian Eriocaulaceae (Giulietti et al., 2016), a herbaceous plant family that occurs in campo rupestre and other open vegetation types, as a predictor for new occurrences of putative endemics. This model aimed to highlight areas that might harbor the same species that were found on CRC of Carajas. Approximately one thousand specimens collected were deposited at the MG herbarium and sent to plant specialists (Figs. 4, 5, 6, 7, 8 and 9).
New potential distribution models were prepared using the final list of 38 endemic species produced here. Occurrence records of the confirmed endemic taxa were organized into a database. From the environmental variables obtained from Worldclim website (Hijmans et al., 2005), we selected six variables through a Pearson correlation analysis (0.75 threshold), with a resolution of 30 arc-seconds (approximately 1 [km.sup.2]): Annual mean temperature, Isothermality, Temperature Seasonality, Max Temperature of Warmest Month, Precipitation of Wettest Month and Precipitation of Driest Month. Despite the importance of altitude to our selected plants, this variable was excluded due to high correlation with temperature. We are also aware of the importance of soil type to the selected plants, but there is no such information with an equivalent resolution to all study areas available, which hindered the use of this variable during our modeling procedure.
The distribution models were generated using the Maxent algorithm, implemented in the dismo package (Hijmans, 2015) for R (R Core Team)(Fielding & Bell, 1997). Maxent needs at least 10 records to build the models, and because of this, taxa with less than 10 records could not be analyzed. Thus, from the 38 species listed here, it was possible to model only 28. We used only spatially independent records (occurrence records reported for different cells of 30 arc-seconds) to construct the models. Maxent also requires information about locations where species are absent; but since this type of data for such geographical extension is difficult to obtain, the algorithm automatically generates pseudo-absence data randomly throughout the modeling area. The occurrence dataset was divided into three subsets and three modeling procedures were performed using two-thirds of the data for training and one-third for test. To evaluate the performance of each model, we calculated the area under the receiver operating curve (AUC) (Fielding & Bell, 1997), which ranges from 0 to 1, and True Skill Statistic (TSS) (Allouche, Tsoar, & Kadmon, 2006), which varies between -1 and 1. We maintained the models with AUC > 0.7 and TSS > 0.6 which values indicate a good performance (Fielding & Bell, 1997; Allouche et al., 2006). All analyses were carried out in R environment (R Core Team, 2018).
We use a threshold of 70% of occurrence probability to transform the final obtained models for each species on binary models (0 or 1). After this, all models were summed using ArcGIS (ESRI, 2018); thus, the ensemble model highlights the areas with the highest suitability for the 28 analyzed species, which are represented as the areas with the highest probability of occurrence.
Results and Discussion
Precise diagnosis of endemism of CRC
The initial list of 73 taxa (Supplementary material Table S2) that had type-specimens from Carajas was reduced, through the discarding of records that were known to have wider distribution at the point of description, resulting in a list of 58 putative endemic taxa including 53 angiosperms and five ferns and lycophytes (Supplementary material Table S3). The study of newly prepared floristic treatments for the Flora of the canga of the Serra dos Carajas (Mota et al., 2018) and recent field surveys (Table 1) contributed to the exclusion of 20 taxa from the putative species list for the following reasons:
1. Wide distribution. Taxa that have been found to have wider geographic distribution than initially suggested were excluded. Two of these taxa were synonymized into species with wider distribution, namely Ipomoea carajasensis, recently included in the synonymy of I. maurandioides, a species with distribution in Brazil, Bolivia, Paraguay and Argentina (Wood et al., 2015); and Bulbostylis carajana, which was sunk into Bulbostylis conifera (Nunes et al., 2016). Apart from these, Ipomoea marabaensis (discovered elsewhere in Para and extending to Tocantins), Centrosema carajasense (found in Mato Grosso), Mimosa acutistipula var ferrea (collected in Maranhao), Mormodes paraensis (new collection in Roraima), Borreria semiamplexicaulis (collected in Maranhao), Pradosia granulosa (also collected in Maranhao), and Pilocarpus carajaensis was found elsewhere in the state of Para. Two fern species, Blechnum areolatum and B. longipilosum were also collected in Maranhao after their description.
2. Borreria semiamplexicaulis and Ipomoea marabaensis were included as Rare for Brazil (Giulietti et al., 2009). However, these occur in other areas of the state of Para and elsewhere (Zappi et al., 2017a), with I. marabaensis also occurring in Tocantins (Simao-Bianchini et al., 2016) and their status as rare plants needs to be reevaluated.
3. Exclusive to the forest. This group of 4 taxa occurred only in the lowland forest environment: Jacaranda carajasensis is a tree restricted to the FLONA of Carajas and listed as threatened (Critically Endangered) because of its narrow distribution (Gentry, 1992; MMA, 2014). Heliconia carajaensis is a poorly understood giant herb from forest understorey, not recorded in the Brazilian species list (FBO 2020, under construction). Voyria alvesiana (Guimaraes et al., 2018) is found on ombrophylous forest and has no records from the canga so far. Selaginella stomatoloma, the only heterosporous lycophyte listed, is a diminutive shadeloving rupicolous plant which grows in dense lowland to premontane forests and is known only from three collections, all from Carajas (Valdespino, 2015), none of these from the canga study area.
4. Local canga and forest. Therefore, despite being found only locally, Mouriri cearensis subsp. carajasica, is found both associated with canga and in the dense rainforest surrounding the outcrops. Hypolytrum paraense occurs more often in the transitional area between canga and tall forest (Nunes et al., 2016).
5. Not exclusive to ferruginous substrate. Taxa that do not grow exclusively in CRC, thus not being considered edaphic endemic (sensu Kruckenberg, 2002). Marsdenia bergii is a robust climber that occurs in CGC however its distribution is not restricted to this substrate and, despite being classified as Rare for Brazil (Giulietti et al., 2009), has been found growing on granite within the area of the FLONA of Carajas (Fernandes et al., 2018), alongside Mitracaipus carajasensis (Zappi et al., 2017a) and Brasilianthus carajensis. It is possible that both species are new arrivals in the granite outcrop, following the opening of roads that link the outcrops, mining plants and other mines, as was established by (RL.Viana, pers. comm.).
In terms of threatened species, the findings of this work reflect the need for revision of the categorization of some species currently considered as Vulnerable. In the case of Ipomoea carajasensis, this taxon was found to be part of a wider species concept, nowadays known as I. maurandioides (Wood et al., 2015). Pradosia granulosa, classified as Vulnerable based on its restricted distribution (Martinelli & Moraes, 2013) has been recorded throughout the state of Para and its IUCN category may need to be re-examined.
Categories of Endemism According to Species Distribution Data
The final list of edaphic endemics of CRC Carajas comprises 38 species of vascular plants distributed in 31 genera and 22 families (Table 2; Supplementary Information S4), including three monotypic genera: Carajasia (Rubiaceae11Fig. 9), Monogereion and Parapiqueria (Asteraceae11Fig. 6). From these endemic species, 24 can be classified as Rare Species for Brazil (Table 2), based on their restricted geographic distribution, with an extent of occurrence (EOO) of less than 10,000 [km.sup.2] and locations less than 150 km (according to Rapini et al., 2009). For the 14 remaining species, even though nine present 5,000 [km.sup.2] < EOO > 10,000 [km.sup.2], we did not find a fit within the criterion of distance between outcrops explained above (Table 2).
A total of 30 species that present EOO smaller than 5,000 [km.sup.2] have been classified as either Highly Restricted Endemic (HRE) or Range Restricted Endemic (RRE) (Darbyshire et al., 2017). The Highly Restricted Endemic were the lycophyte Isoetes cangae (Fig. 9) as well as six angiosperms from the FLONA of Carajas: Carajasia cangae, Daphnopsis filipedunculata, Ipomoea cavalcantei, Parapiqueria cavalcantei, Paspalum carajasense, alongside Mimosa dasilvae, from outsde the FLONA of Carajas and the PNCF. The remaining 23 species were classified as Range Restricted Endemic (RRE) (Table 2).
The 38 endemic species can be categorized in four groups according to their specific conservation requirements (Table 2):
(1) A single taxon, Mimosa dasilvae, is restricted to the Serra de Campos in Sao Felix do Xingu. It also was classified as both HRE and Rare for Brazil.
(2) Twenty are relatively widely distributed in the CRC throughout the region, including FLONA of Carajas. PNCF, Serra Arqueada, Serra do Cristalino, Serra Leste and Serra de Campos. Of these, 11 were classified as RRE with EOO between 113 and 4903 [km.sup.2].
(3) Nine angiosperm taxa are restricted to the FLONA of Carajas and PNCF. These are: Bulbostylis cangae, Cavalcantia glomerata, Erythroxylum carajasense, E. nelson-rosae, Lepidaploa paraensis, Paspalum cangarum, Philodendron carajasense, Picramnia ferrea (Fig. 8) and Sinningia minima (Fig. 7). All of them were classified as RRE. Erythroxylum nelson-rosae and Picramnia ferrea were already considered rare for Brazil (Giulietti et al., 2009).
(4) Eight taxa are exclusively from the FLONA of Carajas. From those, only two are found both in the Serra Norte and Serra Sul: the herbaceous Axonopus carajasensis and Peperomia pseudoserratirhachis, both classified as RRE. Three species are found only in the Serra Norte: a liana. Ipomoea cavalcantei. herbaceous Paspalum carajasensis and the treelet Daphnopsis filipedunculata, all classified as HRE. Three species are exclusive to the Serra Sul: the monotypic herbaceous genera Carajasia cangae and Parapiqueria cavalcantei and the aquatic lycophyte Isoetes cangae, and all of these also fit within HRE. Axonopus carajasensis and Ipomoea cavalcantei have already been recorded as Rare for Brazil (Giulietti et al., 2009), and also endangered (Martinelli & Moraes, 2013; MMA, 2014). In spite of the type specimen of P. cavalcantei being originally from the Serra Norte (specimen Cavalcante 216211RB), current collections are all from the Serra Sul.
The ensemble of species distribution modelling highlighted 20 areas with the highest suitability for 28 endemic species to occur (Fig. 4). The majority of these areas are found westwards from the FLONA of Carajas, with only three eastwards and two towards the northeast, in the border between the states of Para and Maranhao. Most of these areas (13) are found at relatively high altitudes (above 600 m a.s.l.).
Comparing our Findings with Global Evidence
According to (Gibson et al., 2010), the vegetation and flora patterns in the BIFs from South West Australia appear to be related to local topographical factors and the long period of time these landscapes have remained unglaciated and above the sea level. The plant communities found there differ in composition from the surrounding Mediterranean type matrix and exhibit high levels of endemism. Zappi et al. (2017b) studied the flora of campo rupestre over quartzitic and canga substrates in the Espinhaijo Range, in Eastern Brazil, an area that occupies 66,450 [km.sup.2] and is home for over 5,000 species (Silveira et al., 2016), with approximately 40% of them apparently endemic (Brazil Flora Group [BFG], 2015). In the CRC of Carajas, restrictions to plant establishment include shallow, stony soil, high levels of insolation, elevated temperatures, temporarily waterlogged substrate and the presence of potentially toxic metal concentration (Schaefer et al, 2016). However, an area of canga that adds up to mere 115 [km.sup.2] (Souza-Filho et al, 2019) hosts a total of 856 species of seed plants (Mota et al. 2018). The present study shows that 38 (over 4%) of the angiosperm species are endemic to the CRC of Carajas. Studies developed in the campo rupestre of the Serra do Cipo, in Minas Gerais (Giulietti et al., 1987), have found 1590 species distributed in an area of approximately 200 [km.sup.2], where the endemism is strongly correlated to different plant families, with forest dwelling taxa with almost no endemic taxa, while species that grow in open vegetation surpass 40% of endemism for the Velloziaceae. Pirani et al. (2015) evaluated the endemism in 2943 species in the same region, and found that 196 (6.6%) were endemic to the area. It is important to highlight that these data did not take into account the edaphic endemism, being limited to the geography of the species. However, while 114 plant families yielded no endemism, endemism was concentrated in seven families, namely the Melastomataceae (5 out of 149 spp., 3.3% endemic), Asteraceae (12 out of 301 spp., 4.3% endemic), Poaceae (10 out of 198 spp., 5% endemic), Rubiaceae (5 out of 91 spp., 5.1% endemic), Xyridaceae (11 out of 60, spp. 18% endemic), Eriocaulaceae (49 out of 133 spp., 36.8% endemic) and Velloziaceae (24 out of 61 spp., 40% endemic).
When considering the CRC of Carajas, with the exception of the Velloziaceae, all above listed families have endemic species: Asteraceae, 34 spp., with two genera and 4 species (i.e. 12%) endemic (Cruz et al., 2016); Melastomataceae, 63 spp., one edaphic endemic species (Rocha et al., 2017); Poaceae, 87 spp., 4 species (i.e. 4.6%) endemic; Rubiaceae, 48 spp., with one genus and 5 species (i.e. 10%) endemic (Zappi et al., 2017a); Eriocaulaceae, 10 spp., 2 (i.e. 20%) endemic (Watanabe et al., 2017); and Xyridaceae, 4 spp. of which one is endemic (Mota & Wanderley, 2016; Mota et al., 2018). Therefore the proportion of endemic species in Carajas is comparable to what is found for the Serra do Cipo in the Cadeia do Espinhaco (Eastern Brazil), and also for the canga in the Quadrilatero Ferrifero, where a survey of nearly a thousand species reports between 27 (Borsali 2012) and 36 endemic species in an area that covers 102 [km.sup.2] (Carmo & Jacobi, 2013). Furthermore, the inclusion of substrate specificity leads to a narrower endemism concept in our analyses. Other iron-ore sites worldwide, such as the 25 BIF ranges surveyed in Western Australia, have recorded over an area of approx. 650 [km.sup.2] (Gibson et al., 2017) over 1700 taxa of which 24 were found to occur on individual sites while a further six taxa were restricted to a group of ranges, resulting in 1.8% species endemism. Detailed studies such as the ones developed for Carajas (Mota et al., 2018) have revealed that a large number of species initially considered as single site endemics from the CRC are distributed more widely than previously thought, but their total range is still restricted to iron-ore outcrops in the region. Meanwhile, after all the sampling effort invested, there are some species that remain recorded for a single site, such as Mimosa dasilvae and the six species exclusive from the FLONA of Carajas (see Table 2).
Out of the 38 endemic species from the CRC, 24 were classified as rare for Brazil (Table 2), of which six (Axonopus carajasensis, Eriocaulon carajense, Eiythroxylum nelson-rosae, Ipomoea cavalcantei, Picramnia ferrea and Utricularia physoceras) were already rare as referred by Giulietti et al. (2009), amongst others that were found not to be CRC endemic after the present research (such as Ipomoea marabaensis, Marsdenia bergii). The CRC of Carajas are now the second Key Biodiversity Area in northern Brazil, after the Reserva Florestal Adolpho Ducke, with 25 rare species, and the Serra do Araca, with 10 species (Kasecker et al., 2009).
The vascular plants from the canga of the Serra dos Carajas include 1034 species of vascular plants (856 seed plants: Mota et al., 2018 + 156 ferns and lycophytes: Salino & Almeida, 2018) in an area covering at most 150 [km.sup.2], with seven HRE and 23 RRE species. These numbers highlight a unique flora that compares favourably to the 1109 plant species of vascular plants reported for the Quadrilatero Ferrifero of Minas Gerais (ca. 7200 [km.sup.2]) (Carmo & Jacobi, 2013) and the 1700 species found over 600 [km.sup.2] in the Australian BIFs (Gibson et al., 2017). In the latter sites, the surfaces measured included areas surrounding the iron-rich outcrops.
Concluding Remarks--Conservation of the CRC Endemic Species
The protection of the endemic species from the CRC depends on the increase of the scientific knowledge regarding their accurate range, as well as their morphology, adaptations, population dynamics, demography and genetics. The information presented herein is of value for decision-making and invigilation of the current laws by environmental agencies, providing a sound base for their interaction with the companies that use and transform the land, ensuring sustainable development of this site. International efforts have been made towards improving the sustainability of mining, suggesting strategies to avoid the loss of species (ICMM & IUCN, 2014), for mitigation and compensation (Duke & ten Kate, 2014) and the restoration of post-mining areas (Maron et al., 2012; Giannini et al., 2017). However, for the effective compliance with legal requirements and conservation strategies, it is necessary that biodiversity data is made available and analysed from the scientific point of view, resulting in effective compliance with legal claims, and guiding further strategies to effectively protect or restore biodiversity.
Acknowledgements We would like to thank the Museu Paraense Emilio Gocldi (MPEG) and Institute) Tecnologico Vale (ITV) for the infrastructure and support that were fundamental to develop this project. The financial support was provided by the project that represented the base for the Term of Agreement between MPEG/ITVDS/FADESP (01205.000250/2014-10) and by CNPq (processo 455505/2014-4; 443365/2015-6). To Dr. Marlucia Bonifacio Martins (MPEG), Dr. Ana Vilacy Galucio (MPEG). Dr. Anna Luiza Ilkiu-Borges and Dr. Vera Lucia Imperatriz Fonseca (ITV), their dedication to consolidate and oversee the Term of Agreement between MPEG and ITV. To the herbarium curators of all institutions involved, especially to BHCB, IAN, INPA. RB. This work would not have been possible without the support and dedication of our coordinator. Prof. Vera L. Imperatriz-Fonseca, who tirelessly championed the completion of this study at ITV. We would like to thank our colleagues for their insights and ongoing discussion around the theme of endemic species, especially to Rodolfo Jaffe, Pedro W. M. Souza Filho. Clovis Maurity, Matheus Nogueira. And Marcos E.L. Lima for their enthusiasm and help during fieldwork. Plant specialists Daniele Monteiro, Andre S. Gil, James Costa-Lima, Alain P. Chautems and Andre O. Simoes also provided important insight on their plant groups. Images were kindly provided by Climbie Hall, Fernando Marino, Andre Andre, Bruno Raineri and Joao Marcos Rosa. Specimens collected within protected areas were subject of permits issued by ICMBio/IBAMA (federal) and Ideflor (Para state) conservation units.
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Ana M. Giulietti (1,5) * Tereza C. Giannini (1) * Nara F.O. Mota (1,2) * Mauricio T. C. Watanabe (1) * Pedro L. Viana (2) * Mayara Pastore1 (2) * Uiara C. S. Silva (1) * Marinez F. Siqueira (3) * Jose R. Pirani (4) * Haroldo C. Lima (3)* Jovani B. S. Pereira (1) * Rafael M. Brito (1) * Raymond M. Harley (5) * Jose 0. Siqueira (1) * Daniela C. Zappi (1,2,6)
(1) Instituto Tccnologico Vale, Rua Boaventura 955, Belem, PA 66055-090. Brazil
(2) Coord. Botanica. Muscu Paraense Emilio Gocldi. Av. Perimetral 1901, Belem, PA 66077-830, Brazil
(3) Instituto de Pesquisas Jardim Botanico do Rio de Janeiro, Rua Pacheco Leao 915, Rio de Janeiro. RJ 22460030, Brazil
(4) Departamento de Botanica da Universidade de Sao Paulo, Rua do Matao 277, Sao Paulo, SP 05508900, Brazil
(5) Royal Botanic Gardens. Kew, Richmond, Surrey TW9 3AB, UK
(6) Author for Correspondence; e-mail: email@example.com
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s1222901909214-x) contains supplementary material, which is available to authorized users.
Caption: Fig. 1 Outcrops that form the Serra dos Carajas, Para. Brazil: Carajas National Forest (FLONA of Carajas): Serra Norte (A) and Serra Sul (B); National Park of Campos Ferruginosos (PNCF): Serra do Tarzan (C) and Serra da Bocaina (D); Serra Arqucada (E); Serra do Cristalino (F); Serra Leste (G): Serra de Campos (Sao Felix do Xingu) (H)
Caption: Fig. 2 Distances in Kilometers between the main outcrops of canga in the Serra dos Carajas, Para, Brazil, used to ascertain plant species rarity
Caption: Fig. 3 Areas surveyed in this study to determine the endemic species of the Serra dos Carajas, Para, Brazil (see also Table 1)
Caption: Fig. 4 Areas with the highest probability of occurrence of the endemic species found in the Serra dos Carajas. Para. Brazil (green border) in a model comprising 28 species. (A) FLONA of Carajas (Mun. Canaa dos Carajas and Parauapcbas); (B) National Park of Campos Ferruginosos (Serra do Tarzan and Serra da Bocaina Mun. Canaa dos Carajas); (C) Serra do Cristalino and Serra do Rabo (Mun. Canaa dos Carajas and Curionopolis); (D) Serra Leste or Serra do Screno (Mun. Curionopolis); (E) Serra do Cinzento (Mun. Maraba); (F) Border between Municipalities of Maraba and Sao Felix do Xingu; (G) Border between Municipalities of Maraba and Parauapebas; (H) Border between Municipalities of Sao Felix do Xingu, Maraba and Parauapcbas; (I) Serra da Seringa (Mun. Agua Azul do Norte and Ourilandia do Norte); (J) Serra do Bacaja (Mun. Sao Felix do Xingu); (K. L. M) Areas in the Municipality of Sao Felix do Xingu; (N) Serra da Fortalcza (Mun. Sao Felix do Xingu); (O) Serra do Trairao (Bannach); (P) Serra do Cubeneranquem (Mun. Ourilandia do Norte); (Q) Serra dos Gradaus (Mun. Cumaru do Norte); (R) Serra dos Gradaus (Mun. Cumaru do Norte and Redenpao); (S) Serra dos Gradaus (Mun. Cumaru do Norte and Santa Maria das Barrciras); (T) Border of Municipality of Dom Eliseu; (U) Border of Municipality of Rondon
Caption: Fig. 5 Portraits of endemic species from the Serra dos Carajas. Para, Brazil (Apocynaceae to Asteraceae I): Matelea microphylla (Apocynaceae), habit and flower11photos F. Marino; Philodendron carajasensis (Araeeae), habit, foliage and inflorescence: photos A Arruda, N. Mota and B. Ranieri; Cavalcantia glomerata (Asteraccae), plant visited by butterfly and inflorescence in detail: photos PL. Viana; Lepidaploa paraensis (Asteraceac), habit, inflorescences and detail showing florets: photos PL. Viana
Caption: Fig. 6 Portraits of endemic species from the Serra dos Carajas. Para. Brazil (Asteraceae II to Convolvulaceae): Monogereion carajensis (Asteraceae), habit and detail of the inflorescence: photos P.L. Viana; Purapiqueria cavalcantei (Asteraceae), habit, whole plant and detail of the inflorescence: photos N. Mota and P.L. Viana; Anemopaegma carajasensis (Bignoniaceae): flowers, habit and fruit: photos: P.L. Viana and N. Mota; Ipomoea cavalcantei (Convolvulaceae), flowers and two views of the habit: photos P.L. Viana
Caption: Fig. 7 Portraits of endemic species from the Serra dos Carajas, Para, Brazil (Cyperaceae to Gesncriaceae): Bulbostylis cangae (Cyperaceae), habit: photo P.L. Viana; Eleocharispedrovianae (Cyperaceae), aquatic habit and inflorescences: photos P.L. Viana; Eriocaulon carajasensis (Eriocaulaceae), detail of inflorescence: photo N. Mota; Syngonanthus discretifolius (Eriocaulaceae), population, habit and inflorescence: photos M. Watanabc and J.M. Rosa; Mimosa skineri (Fabaceae), habit and detail of inflorescences: photos P.L. Viana; Sinningia minima (Gesneriaceae), whole plant: photo N.F. Mota; Utricularia physoceras (Lentibulariaceae), population shots and detail of flowers: photos: P.L. Viana
Caption: Fig. 8 Portraits of endemic species from the Serra dos Carajas, Para, Brazil (Lythraccae to Poaccae): Cuphea carajasensis (Lythraccae), habit and flower colour variation within the population: photos: N. Mota and P.L. Viana; Pleroma carajasensis (Melastomataceac), inflorescence and habit: photos P.L. Viana; Buchnera carajasensis (Orobanchaccae), flower photo N. Mota; Picramnia ferrea (Picramniaceae), habit with yellow fruits and detail of male inflorescence: photos N. Mota; Peperomia albopilosa (Piperaceae), whole plant and detail of infructescence: photos N. Mota: Paspalum cangarum (Poaccac), inflorescence and detail showing open flowers: photos P.L. Viana; Axonopus carajasensis (Poaccac): detail showing open flowers: photo P.L. Viana; Sporobolus multiramosus (Poaceae), habit and detail of inflorescence: photos P.L. Viana
Caption: Fig. 9 Portraits of endemic species from the Serra dos Carajas. Para, Brazil (Rubiaceae to Xyridaceae): Borreria carajasensis (Rubiaceae). habit and plant: photos P.L. Viana; Borreria elaiosulcata (Rubiaceae), habit and detail of inflorescence: photos P.L. Viana; Borreria heteranthera (Rubiaceae), inflorescence: photo A. Arruda; Carajasia cangae (Rubiaccae), habit, whole plant and flowers in detail: photos P.L. Viana; Perama carajasensis (Rubiaceae), habit: photo P.L. Viana; Daphnopsis filipedunculata (Thymelacaceac), habit and detail of inflorescence: photos N. Mota and F. Marino; Xyris brachysepala (Xyridaccae), inflorescence: photo C. Hall; Isoetes cangae (Isoctaceae), aquatic habit: photo A. Arruda: Isoetes serracarajensis (Isoetaceae), aquatic habit: photo N. Mota
Table 1 Areas surveyed during this study to ascertain the endemism of the species from the canga of Carajas (see also Fig. 2) Month Year Province Municipality May 2016 AM Barcelos May 2016 AM Barcelos May 2016 PA Sao Felix do Xingu May 2016 PA Sao Felix do Xingu May 2016 PA Curionopolis July 2016 PA Sao Geraldo do Araguaia July 2016 TO Araguatins July 2016 TO Tocantinopolis July 2016 TO Ananas Oct 2016 PA Santarem Oct 2016 PA Monte Alegre Nov 2016 PA Maraba Mar 2017 PA Curionopolis April 2017 PA Redeni;ao April 2017 PA Cumaru do Norte April 2017 PA Rio Maria April 2017 PA Bannach April 2017 PA Sao Felix do Xingu April 2017 PA Curionopolis April 2017 PA Ourilandia do Norte June 2017 PA Canaa dos Carajas June 2017 PA Viseu July 2017 PA Santarem July 2017 PA Belterra Month Year Locality Latitude May 2016 Serra do Araca 00[degrees]51'44"N May 2016 White sand fields 00[degrees]28'19"N May 2016 Serra de Campos 06[degrees]23'34"S May 2016 Serra Arqueada 06[degrees]30'27"S May 2016 Serra do Cristalino 06[degrees]27'12"S July 2016 Serra das Andorinhas 06[degrees]12'53"S July 2016 Transamazonica highway 05[degrees]46'37"S July 2016 Transamazonica highway 06[degrees]13'43"S July 2016 TO-210 highway 06[degrees]22'7"S Oct 2016 Alter do Chao 02[degrees]28'36"S Oct 2016 Parque Estadual de Monte 02[degrees]01'13"S Alegre Nov 2016 Serra do Cururu 05[degrees]51'58"S Mar 2017 Serra Leste 05[degrees]59'33"S April 2017 Redengao Rocky Fields 08[degrees]04'23"S April 2017 Santa Teresa Highway 07[degrees]54'52"S April 2017 Radio Tower Hill 07[degrees]18'34"S April 2017 Local Road 07[degrees]38'35"S April 2017 Serra de Campos 06[degrees]23'43"S April 2017 Serra do Cristalino 06[degrees]27'28"S April 2017 Serra Arqueada 6[degrees]30'33"S June 2017 Niquel do Vermelho 6[degrees]28'11"S June 2017 Apeu-Salvador 00[degrees]55'22"S July 2017 Reserva Extrativista 02[degrees]24'15"S Tapajos Arapiuns July 2017 Floresta Nacional do 03[degrees]02'58"S Tapajos Month Year Longitude Altitude (m) Endemic found May 2016 63[degrees]20'41"W 1034 No May 2016 63[degrees]23'39"W 55 No May 2016 51[degrees]52'40"W 660 Yes (13) May 2016 51[degrees]09'44"W 699 Yes (9) May 2016 49[degrees]40'32"W 760 Yes (9) July 2016 48[degrees]31'15"W 410 No July 2016 48[degrees]03'06"W 250 No July 2016 47[degrees]28'56"W 275 No July 2016 48[degrees]02'05"W 390 No Oct 2016 54[degrees]55'37"W 18 No Oct 2016 54[degrees]10'54"W 255 No Nov 2016 50[degrees]13'15"W 610 No Mar 2017 49[degrees]37'07"W 660 Yes(4) April 2017 50[degrees]10'05"W 500 No April 2017 50[degrees]26'06"W 250 No April 2017 49[degrees]58'45"W 250 No April 2017 50[degrees]22'22"W 580 No April 2017 51[degrees]54'15"W 640 Yes(13) April 2017 49[degrees]40'40"W 765 Yes(14) April 2017 51[degrees]9'23"W 620 Yes (8) June 2017 49[degrees]54'15W 270 No June 2017 46[degrees]11'18"W 10 No July 2017 55[degrees]'03'02"W 20 No July 2017 54[degrees]57'54"W 20 No Table 2 List of endemic species from Carajas (Para, Brazil), including FLONA of Carajas (FC), Parquc Nacional dos Campos Fenuginosos (PNCF), Serra Arquea (SA), Serra do Cristalino (SC), Serra Leste (SL) and Serra de Campos--Sao Felix do Xingu (SF). Area of Occupancy (AOO) and Extent of Occurrence (EOO). Highly Restricted Endemic (HRE). Range Restricted Endemic (RRE); [x = occurs, = old record, population not found again]. For images see Plates 5-9 Family Species Angiosperms 1 Apocynaceae Matelea microphylla Morillo--Fig. 5 2 Araceae Philodendron carajasense E.G.Gon?. & A.J.Arruda--Fig. 5 3 Astcraceae Cavalcantia glomerata (G.M.Barroso & R.M.King) R.M. King & H. Rob.--Fig. 5 4 Astcraceae Lepidaploa paraensis (H.Rob.) H.Rob.--Fig. 5 5 Astcraceae Monogereion carajensis G.M.Barroso & R.M.King *--Fig. 6 6 Astcraceae Parapiqueria cavalcantei R.M.King & H.Rob. Fig. 6 7 Bignoniaceae Anemopaegnia carajasense A.H.Gentry cx Firctti-Lcggieri & L.G.Lohmann --Fig. 6 8 Convolvulaceae lpomoea cavalcantei D.F.Austin**-Fig. 6 9 Cyperaceae Bulbostvlis cangae C.S.Nunes & A.Gil--Fig. 7 10 Cyperaceae Eleocharis pedrovianae C.S.Nunes, R.Trevis. & A.Gil--Fig. 7 11 Eriocaulaceae Eriocaulon carajense Moldcnke Fig. 7 12 Eriocaulaceae Syngonanthus discretifolius (Moldcnke) M.T.C.Watan.--Fig. 7 13 Erythroxylaceae Erythroxylum carajasense (Plowman) J.L.Costa 14 Erythroxylaceae Erythroxylum nelson-rosae Plowman ** 15 Gcsneriaceae Sinningia minima A.O.Araujo & Chautems--Fig. 7 16 Leguminosae Mimosa dasilvae A.S.L.Silva & Secco 17 Leguminosae Mimosa skinneri Benth. var. carajarum Barneby *--Fig. 7 18 Lentibulariaceae Utricularia physoceras P.Taylor --Fig. 7 19 Lythraceae Cuphea carajasensis Lourteig--Fig. 8 20 Melastomataceae Pleroma carajasense K.Rocha, R.Goldenb. & F.S.Mey--Fig. 8 21 Orchidaceae Uleiorchis longipedicellata A.Cardoso & Ilk.-Borg. 22 Orobanehaceae Buchnera carajasensis Scatigna & N.Mota--Fig. 8 23 Picramniaceae Picramnia ferrea Pirani & W.W.Thomas--Fig. 8 24 Piperaceae Peperomia albopilosa D.Monteiro --Fig. 8 25 Piperaceae Peperomia pseudoserratirhachis D.Monteiro 26 Poaceae Axonopus carajasensis M.Bastos ** --Fig. 8 27 Poaceae Paspalum cangarum C.O.Moura, P.L.Viana & R.C.Oliveira--Fig. 8 28 Poaceae Paspalum carajasense S.Dcnham 29 Poaceae Sporobolus multiramosus Longhi-Wagner & Bocchat--Fig. 8 30 Rubiaceae Borreria carajasensis E.L.Cabral & L.M.Miguel--Fig. 9 31 Rubiaceae Borreria elaiosulcata E.L.Cabral & L.M.Miguel--Fig. 9 32 Rubiaceae Borreria heteranthera E.L.Cabral & Sobrado--Fig. 9 33 Rubiaceae Carajasia cangae E.L.Cabral & Dessein--Fig. 9 34 Rubiaceae Perama carajensis J.H.Kirkbr. --Fig. 9 35 Thymclacaceae Daphnopsis filipedunculata Nevling & Barringer Fig. 9 36 Xyridaceae Xyris brachysepala Kxal Fig. 9 Lycophytes 37 Isoctaceae Isoetes cangae J.B.S.Pereira, Salino & Stutzel--Fig. 9 38 Isoctaceae Isoetes serracarajensis J.B.S.Percira, Salino & Stutzel--Fig. 9 Family Publication FC PNCF year Serra Serra Tarzan Bocaina Angiosperms Note Sul 1 Apocynaceae 1988 X X 2 Araceae 2013 X X X 3 Astcraceae 1980 X X X 4 Asteraceae 1994 X X X X 5 Asteraceae 1971 X X X X 6 Asteraceae 1980 X 7 Bignoniaceae 2018 X X X 8 Convolvulaceae 1981 X 9 Cyperaceae 2017 X X X 10 Cyperaceae 2016 X X X X 11 Eriocaulaceae 1973 X X X 12 Eriocaulaceae 2015 X X X 13 Erythroxylaceae 2017 X X X 14 Erythroxylaceae 1986 X X X X 15 Gesneriaceae 2015 X X X 16 Leguminosae 2000 17 Leguminosae 1991 X X X X 18 Lentibulariaceae 1986 X X X X 19 Lythraceae 1987 X X X X 20 Melastomataceae 2017 X X 21 Orchidaceae 2015 X 22 Orobanehaceae 2017 X X X X 23 Picramniaceae 1988 X X X X 24 Piperaceae 2018 X X 25 Piperaceae 2018 X X 26 Poaccae 1991 X X 27 Poaceae 2018 X X 28 Poaceae 2005 X 29 Poaceae 1993 X X X X 30 Rubiaceae 2012 X X X 31 Rubiaceae 2012 X X X X 32 Rubiaceae 2015 X X X X 33 Rubiaceae 2015 X 34 Rubiaceae 1980 X X X X 35 Thymclacaceae 1993 X 36 Xyridaceae 1988 X X X X Lycophytes 37 Isoctaceae 2016 X 38 Isoctaceae 2016 X X X X Family SA SC SL SF EOO (Km2) AOO (Km2) Angiosperms 1 Apocynaceae X X 4436 20 2 Araceae 1363 44 3 Astcraceae 1394 44 4 Asteraceae 1376 68 5 Asteraceae X X X 7654 100 6 Asteraceae 5 12 7 Bignoniaceae X 4195 40 8 Convolvulaceae 82 48 9 Cyperaceae 709 24 10 Cyperaceae X 4903 72 11 Eriocaulaceae X 4756 40 12 Eriocaulaceae X 4464 108 13 Erythroxylaceae 1287 48 14 Erythroxylaceae 1285 60 15 Gesneriaceae 1461 88 16 Leguminosae X -- 4 17 Leguminosae X X X X 7633 132 18 Lentibulariaceae X 2030 96 19 Lythraceae X X X 7778 156 20 Melastomataceae X X 6496 72 21 Orchidaceae X 156 12 22 Orobanehaceae X X 5419 72 23 Picramniaceae 1774 56 24 Piperaceae X 3878 44 25 Piperaceae 152 16 26 Poaceae 564 16 27 Poaceae 252 20 28 Poaceae 53 16 29 Poaceae X 1937 56 30 Rubiaceae X X 5869 88 31 Rubiaceae X 2203 160 32 Rubiaceae X 1936 64 33 Rubiaceae 37 36 34 Rubiaceae X X X X 8922 1283 35 Thymelacaceae 37 20 36 Xyridaceae X X X 6412 140 Lycophytes 37 Isoctaceae -- 4 38 Isoctaccac X 1472 36 Family Ende-mism Rare Habit Angiosperms 1 Apocynaceae RRE Liana 2 Araceae RRE X herb 3 Asteraceae RRE X subshrub 4 Asteraceae RRE X subshrub 5 Asteraceae -- shrub 6 Asteraceae HRE X subshrub 7 Bignoniaceae RRE shrub 8 Convolvulaceae HRE X liana 9 Cyperaceae RRE X herb 10 Cyperaceae RRE herb 11 Eriocaulaceae RRE herb 12 Eriocaulaceae RRE herb 13 Erythroxylaceae RRE X shrub 14 Erythroxylaceae RRE X shrub 15 Gesneriaceae RRE X herb 16 Leguminosae HRE X shrub 17 Leguminosae -- subshrub 18 Lentibulariaceae RRE X herb 19 Lythraceae -- subshrub 20 Melastomataceae shrub 21 Orchidaceae -- X herb 22 Orobanehaceae herb 23 Picramniaceae RRE X shrub 24 Piperaceae RRE herb 25 Piperaceae RRE X herb 26 Poaceae RRE X herb 27 Poaceae RRE X herb 28 Poaceae HRE X Herb 29 Poaceae RRE X herb 30 Rubiaceae -- herb 31 Rubiaceae RRE X herb 32 Rubiaceae RRE X herb 33 Rubiaceae HRE X herb 34 Rubiaceae -- herb 35 Thymelacaceae HRE X shrub 36 Xyridaceae -- Herb Lycophytes 37 Isoetaceae HRE X herb 38 Isoetaceae RRE X herb
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|Author:||Giulietti, Ana M.; Giannini, Tereza C.; Mota, Nara F.O.; Watanabe, Mauricio T.C.; Viana, Pedro L.; P|
|Publication:||The Botanical Review|
|Date:||Dec 1, 2019|
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