A National Forest Inventory (NFI) encompassing the entire territory of Brazil is in progress. It is coordinated and promoted by the Brazilian Forest Service of the Ministry of Environment. In each state, the NFI collaborates with local herbaria by receiving collected plant material and performing species identification. Consultants are hired by the NFI and work at the local herbaria under the supervision of a curator. In exchange for curatorial assistance, the NFI provides equipment and consumables for the herbarium. Other public projects collaborating with NFI are Reflora and the Brazilian Biodiversity Information System (SiBBr). Both projects have online platforms that seek to connect herbaria and make all their data freely available, including high quality digital images of specimens. Through inter-institutional collaboration, the joint interests of NFI, Reflora, SiBBr and local herbaria have improved collections, expanded the online Reflora database, and provided the NFI with verified species lists. These strategic uses of public funding are positively affecting Botany, particularly during a period of economic crisis and cuts in research. Here, we illustrate the increase in floristic knowledge through the improvement of a herbarium collection in Rio Grande do Norte (RN) – the Brazilian state with the lowest levels of plant richness. We report 71 new occurrences of vascular plants for RN, belonging mainly to the Poaceae, Fabaceae and Malvaceae. Most of the species with new occurrences have a Neotropical distribution (21 spp.) and only seven are restricted to the Brazilian Northeast. Our findings highlight previous gaps in RN’s floristic knowledge. The partnership NFI, Reflora, SiBBr and the UFRN herbarium improved herbarium curation, digital collection, and quality of data. Finally, a fellowship provided by Reflora and SiBBr allowed improving curation by distributing duplicates and incorporating the Herbarium of Câmara Cascudo Museum.

Brazil Flora Group, Flora, floristics, Herbarium collection, Inventory, Reflora, SiBBr, IFN

A National Forest Inventory (NFI) covering all of Brazil is currently in progress. The NFI is a major undertaking by the Brazilian government, specifically, the Brazilian Forest Service, a public section of the Ministry of Environment, to periodically gather information about the forests and land cover of Brazil, through a systematic sampling of the territory using a 20 km × 20 km grid. In each state, the NFI invites local herbaria to receive and identify the collected specimens. Consultants are hired by the NFI and stay at the local herbarium under the supervision of a curator to identify plants to species. In exchange for this curatorial assistance, the NFI helps the herbarium by providing equipment and consumables. In Rio Grande do Norte (RN), the NFI started in 2014. Two additional public projects that are working with the NFI are Reflora and the Brazilian Biodiversity Information System (SiBBr). Reflora and the SiBBr are online platforms that connect herbaria, making data and high quality images of specimens in their collections freely available. The main goal of Reflora is to complete the Flora do Brasil 2020 online project, which relies on specimen data and images from herbaria in Brazil, the USA, and Europe. Inter-institutional collaboration serves the interests of NFI, Reflora, SiBBr and local herbaria, improving collections, expanding the Reflora database, and providing the NFI with accurate lists of plants. In this paper, we discuss the details and results of a four-part collaboration that makes strategic use of public funding to positively impact the study of Botany during tough economic times.

Rio Grande do Norte (RN) is a Brazilian state that consists of two phytogeographical domains: Dry Woodlands (Caatinga) and Atlantic Forest (Floresta Atlântica). The savanna (Cerrado) vegetation is scattered in small patches throughout the state. Different vegetation types occur within these phytogeographical domains: deciduous, semi-deciduous, subperennial and seasonal mixed palm forest (dominated by Copernicia prunifera (Mill.) H.E. Moore), dunes and coastal sand plain vegetation (restinga), xeric rocky outcrops, natural and anthropic fields, mangroves, saline desert and aquatic vegetation (SUDENE 1971). Both of the main phytogeographical domains in RN have been profoundly altered by human activities. The Atlantic Forest, where most of the sugar cane cultivation has been done for centuries, is fragmented and degraded and urgently needs ecological restoration. Its remaining coverage varies from 8–17%, depending on whether mangroves and restinga coastal plains are included or excluded in the estimate (Maciel et al. 2011). The Caatinga has lost 45% of its original coverage in RN (C. Fonseca, Dept. Ecology, UFRN, pers. com.); what remains is within a few protected areas.

The Lista de Espécies da Flora do Brasil (Forzza et al. 2010, 2012) and the Checklist das plantas do Nordeste Brasileiro (Barbosa et al. 2006) gathered preliminary knowledge of the flora of RN. Recent taxonomic work has complemented this knowledge by focusing on specific taxonomic groups or on floristic studies. Groups that have been studied recently include Chamaecrista (Queiroz and Loiola 2009), Turneraceae (Rocha et al. 2012), Paspalum (Oliveira et al. 2013a), Leguminosae-Papilionoideae (São-Mateus et al. 2013), Erythroxylaceae (Costa-Lima et al. 2014), Capparaceae (Soares-Neto and Jardim 2015), Cyperus (Ribeiro et al. 2015a), Fabaceae (Amorim et al. 2016), and Bignoniaceae (Colombo et al. 2016). Recent floristic studies focused on specific areas or vegetation types, such as the deciduous and semi-deciduous forests (Cestaro and Soares 2004; 2008), savanna (Oliveira et al. 2012), riparian vegetation (Oliveira et al. 2013b, Ribeiro et al. 2014) and the herbaceous vegetation in Seridó (Santana and Souto 2006, Amorim et al. 2006, Ferreira et al. 2009, Queiroz et al. 2015). Furthermore, field work in RN has produced new records (e.g. Versieux et al. 2013a, 2013b). It is likely that the historically limited number of herbaria (only two in Index Herbariorum), graduate programs focused on biodiversity, and taxonomists may have led to insufficient sampling and underestimation of the true taxonomic diversity of the state.

The most recent account listed 1,222 species of angiosperms in RN, only five of which are endemic to the state (BFG 2015, Flora do Brasil 2020): Aspilia procumbens Baker (Asteraceae), Arachis seridoensis Valls et al. (Fabaceae), Sida macaibae Mont. (Malvaceae), Eugenia pipensis A.R.Lourenço & B.S.Amorim (Myrtaceae), and Gouinia virgata (J. Presl) Scribn. (Poaceae). The growing knowledge of flora in RN is striking and is illustrated by estimates of species richness. In 2010 the RN list included 707 species of angiosperms (Forzza et al. 2010), while in 2015 this number nearly doubled to 1,222 species – a 73% increase in five years (BFG 2015). Research investments that supported these results include the participation of researchers in inter-institutional projects, the creation of two new graduate programs in biodiversity in the largest university of the state (UFRN), and an increase in the number of botanical monographs. We also expect an increase in the publication of floristic studies in the next few years, since many recently-collected data are still in preparation.

Although the UFRN herbarium is a small collection (~25,000 specimens), it is the most representative of RN’s flora. The objective of this paper is to describe the progress in the RN floristic knowledge after joint efforts dedicated to the NFI in RN. Together, IFN, SiBBr and Reflora projects have been addressing poor species coverage and lack of investments in botanical collections. Having completed this field inventory, we can show the new species records for the RN flora, and whether these species are restricted to the northeast of Brazil or else are widely-distributed species that have been previously overlooked in RN. Finally, we report how participation in this joint initiative has influenced and affected the infrastructural legacy of the UFRN herbarium.

The NFI fieldwork in RN was carried out from March to October 2014 by private environmental consultants, and specimens began to be deposited in the UFRN herbarium in December 2014. The sampling units of the NFI are distributed according to the National Sampling Points Grid (Grade Nacional de Pontos Amostrais – GNPA), established by the Brazilian Forest Service. The grid density is 20×20 km, covering all of Brazil (IFN 2012). A total of 133 sampling units, called conglomerates, were placed systematically throughout RN. A conglomerate is composed of four subunits (20×50 m), which are established in the field following magnetic cardinal directions, and radiating 50 m from a central point. Inside each subunit, representative specimens of each species of herbaceous and woody plants were collected following specific protocols for Caatinga and Atlantic Forest (IFN 2012). Biophysical data including necromass, litter and soil characteristics, as well as socio-environmental data were also collected in each conglomerate (Freitas et al. 2016). Our summaries presented here are based only on the species richness data from conglomerates, as well as on the new occurrences indicated by specialists that visited our collections or received duplicates of material previously collected and deposited in UFRN herbarium.

A total of 556 voucher specimens were collected and analyzed to estimate the number of new occurrences for RN. All specimens collected were identified at the UFRN Herbarium using appropriate taxonomic literature and floras, comparisons with specimens identified by specialists, or direct determination by taxonomic specialists. We also incorporated the collection of the Câmara Cascudo Museum (MCC), which used to be an independent collection within UFRN. The MCC collection was partially revised by a technician provided by Reflora and SiBBr projects. All vouchers from the NFI were deposited at UFRN (including non-fertile material) and duplicates were sent to other herbaria (RB, HUEFS, UFP, SP, MG; acronyms follow Thiers continuously updated). Furthermore, during the project, the entire UFRN herbarium collection was digitalized into high quality images that are now available in Jabot platform http://ufrn.jbrj.gov.br.

We used Lista de Espécies da Flora do Brasil (http://floradobrasil.jbrj.gov.br), now updated to Flora do Brasil 2020, to determine whether species identified were new records for the state. Though Flora do Brasil 2020 should be continuously updated, we highlight new records in our list, in case that new occurrences reported in scientific literature have been missed.

To get a better picture of the flora of RN, we checked whether the new occurrences are taxa with broad or restricted ranges, as this information may indicate the degree to which they are absent from collections. We defined five categories of distribution according to geographical and political boundaries to infer whether new species records had a distribution restricted to the northeast of Brazil or else they are more widely distributed: 1. Pantropical (“Cosmopolite”): occurring in many places even outside of the tropics, 2. American: occurring all over the Americas, 3. Neotropical: occurring in the Neotropical region, 4. Brazilian: occurring in many states of Brazil – not exclusive to the Northeast region, 5. Northeast: occurring in the Northeast region of Brazil. In addition, we provide comments about each new recorded taxon, including the phytogeographical domains and municipalities where it occurs in RN. Maps were created in QGIS 2.14 (QGIS Development Team 2016) using TEOW (Terrestrial Ecoregions of the World) as a cartographic base (Olsen et al. 2001).

The Brazilian states are abbreviated as follows: AC: Acre, AL: Alagoas, AP: Amapá, AM: Amazonas, BA: Bahia, CE: Ceará, DF: Distrito Federal, ES: Espírito Santo, GO: Goiás, MA: Maranhão, MT: Mato Grosso, MS: Mato Grosso do Sul, MG: Minas Gerais, PA: Pará, PB: Paraíba, PR: Paraná, PE: Pernambuco, PI: Piauí, RJ: Rio de Janeiro, RN: Rio Grande do Norte, RS: Rio Grande do Sul, RO: Rondônia, RR: Roraima, SC: Santa Catarina, SP: São Paulo, SE: Sergipe, TO: Tocantins.

The NFI sampled 133 conglomerates in RN, including 127 in Caatinga and six in Atlantic Rainforest (Figure 1). The sampling covered 86 out of a total of 167 municipalities in the state. We recorded a total of 556 specimens, 285 species and 57 families. The Cerrado was not sampled.

Figure 1. 

Map of Rio Grande do Norte state and municipalities, phytogeographical domains (Atlantic Rainforest and Caatinga), conglomerates points and new botanical records.

We found 71 newly-occurring species (Table 1) in RN, 43 of which were a result of the NFI inventory (see Fig. 1, overlapping new records and conglomerates points) and 28 of them resulted from additional research developed at the UFRN herbarium and the MCC collection. These new occurrences include species from 21 families, most of them belonging to Poaceae (14 spp.), Fabaceae (13), Malvaceae (13) and Cyperaceae (7). New occurrences have been reported in 55 different municipalities in RN and the municipalities with the highest number of new occurrences were Canguaretama (7 spp.), Ceará-Mirim (6), and Macaíba (4). Most newly-occurring species have a Neotropical distribution (21) and only seven species are restricted to the Northeast of Brazil (Table 2).

Considering the curatorial improvement of the UFRN collection we highlight the merging of the Museu Câmara Cascudo into UFRN herbarium. The specimens from the Museu Câmara Cascudo included 405 angiosperms (54 families), and 1,224 macroalgae (31 families). Algae were not studied in this work, but we indicate the new occurrences among angiosperms (Table 2).

Systematic sampling in the entire state of RN during the NFI covered many municipalities that have seen little or no floristic attention in the past. Before the recent surveys, three municipalities – Natal, Mossoró and Serra Negra do Norte – had the highest botanical collecting effort for RN and 129 municipalities had less than 189 records (including 21 without any collection effort whatsoever) (Silva 2015). The low amount of previous effort is reflected in the high number of new occurrences to RN reported in the present study. The municipalities that were previously sampled were mostly concentrated along the Central Potiguar and Agreste Potiguar mesoregions of RN. This study reports new occurrences from the under-sampled Agreste mesoregion (e.g., Pureza), although it also reports new occurrences from some intensively-sampled regions, such as Mossoró, Serra Negra do Norte and Natal. This finding suggests that the botanical sampling in RN remains insufficient even in areas with the highest floristic efforts, such as the capital of the state and the second largest city, which also hosts an herbarium (Mossoró).

Most new occurrences belong to Poaceae, Fabaceae and Malvaceae. Fabaceae and Poaceae are the most species-rich families reported for the Caatinga (BFG 2015) and most new records are from this domain. Although the Atlantic Forest is the most species-rich ecoregion in Brazil (BFG 2015) the NFI conducted more sampling in the Caatinga than in the Atlantic Forest in RN. Sampling effort was allocated in this manner because Caatinga is geographically predominant in this state (Figure 1), while the Atlantic Forest covers only a narrow strip along the east coast, and its area has been severely reduced. Colombo et al. (2016) observed that increased efforts to sample the flora of RN have resulted in improved knowledge of the flora of the Caatinga. Despite our focus on the Caatinga, we found that two of the three municipalities with the highest number of new occurrences, Ceará-Mirim and Canguaretama, were within the Atlantic Forest. This likely reflects the intrinsic diversity of the Atlantic Forest. We believe the Caatinga is the most under-studied area where future sampling efforts should be focused.

Our sampling efforts improved occurrence data of widely-distributed species in Brazil. Some species were originally absent only in RN state, such as Clidemia hirta (Melastomataceae), while others were unknown in several other northeastern Brazilian states, such as Inga vera (Fabaceae) (also unknown in Alagoas and Sergipe) and Amburana cearensis (Fabaceae), which is categorized as endangered (Americas Regional Workshop 1998). Amburana cearensis was recently recorded for RN (Amorim et al. 2016) and currently is only absent in Sergipe. We also improved occurrence data of species with restricted distributions, such as Stilpnopappus laiseae (Asteraceae) and Ayenia erecta (Malvaceae), which were previously reported only from Piauí, and Sorghum bicolor var. arundinaceum (Poaceae), which was previously known only from Acre. We added occurrence data for a few other species already registered for the RN flora but with few known localities. This is the case of the CactaceaeTacinga subcylindrica and Brasiliopuntia brasiliensis, previously known from only one collection in the Açu municipality in 2013. New collections from 2015 onwards considerably expanded the documented occurrence of T. subcylindrica in RN (to the municipalities of Equador, João Câmara, Areia Branca and Macau). Only one collection of B. brasiliensis was reported in 2001 in the municipality of Macaíba, however, new collections were made from 2011 onwards in the municipality of Ceará-Mirim.

Only seven out of 71 newly-occurring species (~10%) have a distribution that is restricted to northeastern Brazil. These low numbers of endemic species are a general pattern for northeast Brazil flora compared to other regions. According to BFG (2015), only 22.7% of 10,661 species of the northeast Brazil are endemic. Also, most of the area in the northeast is Caatinga, which shows a lower percentage of endemic taxa (19.7% of 4,657, BFG 2015), despite being a unique biome in Brazil.

The results of this NFI indicate that the number of species for RN is still underestimated. However, the knowledge of RN’s flora is growing rapidly. New species have recently been discovered (Sobral 2010, Araújo and Alves 2013, Lourenço et al. 2013, Terra-Araújo et al. 2013, Ribeiro et al. 2015b, Souza et al. 2016) and new occurrences for genera or species have been reported for RN (Versieux et al. 2013a, 2013b, São-Matheus et al. 2013, Magalhães et al. 2014, Amorim et al. 2016, Colombo et al. 2016, Gomes-Costa and Alves 2016). In five years, the number of species records for RN increased by 78% (BFG 2015). To continue this trend, we recommend intensive effort focusing on areas that have not been explored by modern taxonomists (Silva 2015), continuous collection across seasons, investment in training of local taxonomists, and improvements to the infrastructure of herbaria.

We emphasize the importance of collaboration among institutions to improve herbarium collections. Most Brazilian herbaria can be considered small, having less than 20,000 records (Vieira 2015). Currently Reflora hosts 54 collections, out of which 40 can be considered small. In our view, small collections are more prone to difficulties due to limited number of staff and funding, lack of visits from specialists (influencing the quality of the data), fewer type specimens, and curators with an overload of tasks (most of them professors). Lack of recognition within institutions, when an herbarium is regarded as belonging to a lab or to a particular professor, leave many collections vulnerable to loss or damage. By facilitating visits by specialists to study specimens, and funding technical fellowships, we improved the quality of our data and incorporated a valuable collection that otherwise would have been abandoned. The impact of visits from specialists on our floristic list is demonstrated by the number of new records reported for Poaceae and Cyperaceae and also by the merging of Museu Câmara Cascudo collection to UFRN herbarium, revealing new occurrences from specimens collected decades ago. The Museu Câmara Cascudo collection for algae is still awaiting examination by specialists, which will likely lead to more new botanical occurrences to RN.

The partnership between NFI, Reflora, SiBBr and UFRN Herbarium has advanced knowledge of biodiversity by exploring areas with few botanical records and adding new species records for the Flora of Rio Grande do Norte. The geographical distribution of newly-added species is mostly Neotropical (21 spp.), while fewer (seven spp.) are endemic to northeastern Brazil. From these results, we conclude that species that have not been recorded to date may occur in different habitats, and that the entire state requires additional floristic inventories. Furthermore, we revealed areas that were poorly covered by existing botanical collections. We also recorded new species from areas with relatively high previous effort of collection, indicating that the species richness in RN remains underestimated. Even our collections may contain specimens that should be further analyzed and studied by specialists, who rarely have opportunities to visit small herbaria. Future botanical projects should fill these remaining gaps in collections, particularly focusing on seasonality. Finally, the NFI/Reflora/SiBBr projects in RN improved the UFRN herbarium collection by digitizing all specimens and improved the curation of the collection through exchange of material among institutions, increased visibility of our specimens online, and attention from specialists.

We thank Serviço Florestal Brasileiro (especially Dr. J. V. Freitas and G. Stancioli Pinho) and consultants involved in fieldwork, sampling and processing material during the NFI in Rio Grande do Norte. Reflora, SiBBr, and NFI enabled the entire UFRN herbarium digitization through donation of a digital camera and computers. J. Lombardi, L. Biral, R. Goldenberg, F. Mayer, B. Amorim, A. Roque, L. Rocha, E. Córdula provided taxonomic support. I. Alves, M. Alves, A. Fontes, E. Nascimento mounted, digitalized, and organized vouchers. Jason R. Straka assisted with editing of this manuscript. UFRN intern M. Alves has an undergraduate fellowship from Procad Capes (#88881.068513/2014-01). LMV and RCF have productivity fellowships from CNPq. Lastly, we thank the directors of Museu Câmara Cascudo, UFRN, for allowing the UFRN herbarium to house their collection and reviewers and editor Ricarda Riina for their comments.