Accessibility / Report Error

Look at the trees: synopsis of Terminalia s.s. in the Brazilian Amazon with conservation and distribution implications

Abstract

Terminalia L. has a pantropical distribution, almost exclusively constituting tropical Combretaceae. In this work, a comprehensive synopsis of all the native species of Terminalia s.s. in the Brazilian Amazon is presented, including diagnostic characters, identification key, illustrations, geographic distribution maps, diversity and richness patterns with a new occurrence in Brazil, and a table with conservation status and number of records/ protected areas and their protected areas for all species. This information seeks to support the identification of these tree species, in addition to actions to conserve trees in the Brazilian Amazon.

Key words
Amazon; diversity; Myrtales; new occurrences; spatial analysis

INTRODUCTION

The Amazon is the most diverse rainforest in the world, standing out for its large number of species (Cardoso et al. 2017CARDOSO D ET AL. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA 114: 10695-10700., Antonelli et al. 2018ANTONELLI A, ZIZKA A, CARVALHO FA, SCHARN R, BACON CD, SILVESTRO D & CONDAMINE FL. 2018. Amazonia is the primary source of Neotropical biodiversity. Proc Natl Acad Sci USA 115: 6034-6039.). Such biological diversity results from a complex interaction between abiotic (e.g., hydrological and topographic alterations) and biotic factors, such as species adaptations and intra and interspecific interactions (Fine et al. 2004FINE PVA, MESONES I & COLEY PD. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305: 663-665., Eva & Huber 2005EVA HD & HUBER O. 2005. A proposal for defining the geographical boundaries of Amazônia. In: EXPERT CONSULTATION WORKSHOP, Ispra, European Commission in collaboration with the Amazon Cooperation Treaty Organization., Hoorn et al. 2010HOORN C ET AL. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931., Antonelli et al. 2018ANTONELLI A, ZIZKA A, CARVALHO FA, SCHARN R, BACON CD, SILVESTRO D & CONDAMINE FL. 2018. Amazonia is the primary source of Neotropical biodiversity. Proc Natl Acad Sci USA 115: 6034-6039.).

Tree species in the Amazon are one of the groups that are most affected by deforestation, with an estimated 58% reduction in species richness by 2050 (Gomes et al. 2019GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.). In this scenario, small- or large-scale studies that collect data about distribution patterns, richness, and ecological aspects of tree species and mitigation of deforestation are essential to establish actions that reduce the loss of plant diversity. Furthermore, such studies help to define areas of interest for taxa conservation, such as those developed by Cardoso et al. (2017)CARDOSO D ET AL. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA 114: 10695-10700. and Gomes et al. (2019)GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553. who presented the general list of species, as well as the richness and area of tree occurrence for the entire Amazon region, respectively.

Among the tree groups in the Amazon region, Terminalia L. is highlighted with 12 species recorded in different phytophysiognomies (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). The genus, included in the Terminaliinae (DC.) Exell & Stace subtribe, is formed by about 290 species with pantropical distribution, almost exclusively constituting the tropical Combretaceae (Stace 1965STACE CA. 1965. The significance of the leaf epidermis in the taxonomy of the Combretaceae. A general review of tribal, generic and specific characters. Bot J Linn Soc 59: 229-252., 2010, POWO 2021POWO – PLANTS OF THE WORLD ONLINE. 2021 Plants of the World Online. Royal Botanic Gardens. Available at http://www.plantsoftheworldonline.org.. Acess on 24 January 2021.
http://www.plantsoftheworldonline.org....
). It is represented by trees with simple and alternate leaves, usually clustered at the apex of the branches, bisexual or unisexual flowers, apetals and fruits betulids, actinomorphic or zygomorphic. The group presents high vegetative and reproductive morphological diversity, making it difficult to recognize the taxa (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., Ribeiro et al. 2018RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257.).

In Brazil, the genus comprises 22 species, of which seven are endemic, belonging to nine sections (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p.). Terminalia representatives occur in different phytogeographic domains of the country, however, the largest diversity of Terminalia, including native and exotic species, was recorded in the Amazon, corresponding to 55% of the species (12 spp.), followed by the Atlantic Forest (11 spp.) and Neotropical savanna (Cerrado) (8 spp.) (Ribeiro et al. 2020RIBEIRO RTM, REBOUÇAS NC, LOIOLA MIB & SALES MF. 2020. Terminalia s.s. (Combretaceae) in Maranhão state, Brazil. Rodriguésia 71: e00942019.).

Regarding taxonomic treatments of the group, the study by Stace (2010)STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., which includes Terminalia representatives from the Neotropical region, is still the most recent and comprehensive. However, despite the descriptions, not all species were illustrated, and further updates are needed regarding new occurrences and aspects of distribution, richness and conservation of taxa in Brazil, which have not yet been contemplated for this group.

For Brazil, important taxonomic studies were developed involving representatives of Terminalia s.s. from Central-West, Northeast, Southeast and South Brazilian geopolitical regions include those by Marquete & Valente (1996)MARQUETE NFS & VALENTE MC. 1996. Combretaceae. In: COLEÇÃO RIZZO, Flora dos Estados de Goiás e Tocantins, Brasília, p. 1-59., Marquete et al. (2003)MARQUETE NFS, TEIXEIRA J & VALENTE MC. 2003. Terminalia L. (Combretaceae) na região Sudeste do Brasil. Bradea 16: 99-123., Linsigen et al. (2009)LINSIGEN LV, CERVI AC & GUIMARÃES O. 2009. Sinopse taxonômica da família Combretaceae R. Brown na Região Sul do Brasil. Acta Bot Bras 23: 738-750., Soares-Neto et al. (2014)SOARES NETO RL, CORDEIRO LS & LOIOLA MIB. 2014. Flora do Ceará, Brasil: Combretaceae. Rodriguésia 65: 685-700., Ribeiro et al. (2017RIBEIRO RTM, LOIOLA MIB & SALES MF. 2017. Flora do Espírito Santo: Subtribo Terminaliinae (Combretaceae). Rodriguésia 68: 1547-1557., 2018, 2020RIBEIRO RTM, MARQUETE N & LOIOLA MIB. 2020. Combretaceae in Flora do Brasil 2020 em construção. 2020. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB6913>. Access on 18 February 2021.
http://floradobrasil.jbrj.gov.br/reflora...
), and Sousa et al. (2018)SOUSA VF, RIBEIRO RTM, LOIOLA MIB & VERSIEUX LM. 2018. Combretaceae no estado do Rio Grande do Norte, Brasil. Rodriguésia 69(4): 1771-1787..

To this date, only two Combretaceae species inventories were carried out in the Brazilian Amazon. The first one, undertaken in the Adolfo Ducke Forest Reserve in the State of Amazonas, listed only eight representatives of Buchenavia Eichler and Combretum Loefl. (Marquete & Valente 2005MARQUETE NFS & VALENTE MC. 2005. Flora da Reserva Ducke, Amazonas, Brasil: Combretaceae. Rodriguésia 56(86): 131-140.). Recently, one species of Combretum (Combretum laxum Jacq.) was recorded in the Serra dos Carajás, State of Pará (Praia 2017PRAIA T DE S. 2017. Flora das cangas da Serra dos Carajás, Pará, Brasil: Combretaceae. Rodriguésia 68: 945-946.).

The representatives of Terminalia s.s. are recognized for their great timber potential, which may be related to the reduction of their natural populations in extraction areas in the Brazilian Amazon (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., Mayoral et al. 2017MAYORAL C, VAN BREUGEL M, CEREZO A & HALL JS. 2017. Survival and growth of five neotropical timber species in monocultures and mixtures. Forest Ecol Manag 403: 1-11.).

Studies about the conservation status of Terminalia taxa are still punctual and include few species, especially those developed by Borges et al. (2012)BORGES R, MORAES MA, MONTEIRO NP, BEVACQUA AM & MARTINELLI G & MARQUETE NFS. 2012. Available data and risk assessment of the Brazilian threatened species of Combretaceae. Rodriguésia 63: 31-38. who evaluated four species (Terminalia acuminata (Allemão) Eichler, T. argentea Mart. & Zucc., T. mameluco Pickel and T. triflora (Griseb.) Lillo), Loiola et al. (2013)LOIOLA MIB ET AL. 2013. Combretaceae. In: MARTINELLI G & MORAES MA. Livro vermelho da flora do Brasil, Rio de Janeiro: Andrea Jakobsson - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, 1100 p., including only T. acuminata, and the National Center for Plant Conservation (CNC Flora 2021CNCFlora. 2021. Centro Nacional de Conservação da Flora. Available at <http://www.cncflora.jbrj.gov.br/portal>. Access on 28 January 2021.
http://www.cncflora.jbrj.gov.br/portal...
) and IUCN Red List of Threatened Species (IUCN 2021IUCN - INTERNATIONAL UNION FOR CONSERVATION OF NATURE. 2021. The IUCN red list of threatened species. Available at <https://www.iucnredlist.org/>. Access on 19 January 2021.
https://www.iucnredlist.org/...
) list five and eight species, respectively.

From a phylogenetic perspective, Maurin et al. (2017)MAURIN O, GERE J, VAN DER BANK M & BOATWRIGHT JG. 2017. The inclusion of Anogeissus, Buchenavia and Pteleopsis in Terminalia (Combretaceae: Terminaliinae). Bot J Linn Soc 184: 312-325. proposed including Buchenavia in Terminalia. Therefore, we have chosen to analyze only Terminalia s.s. The delimitation of Terminalia s.l. is still inconclusive and have being studied by molecular approach to establish a stable taxonomic concept for the taxon, based on consistent and comprehensive morphological and phylogenetic data.

Due to the lack of recent work for this group in the Amazon region and in attempts to fill some gaps about the taxonomy and distribution of species in Brazil, which were previously pointed out by Marquete et al. (2003)MARQUETE NFS, TEIXEIRA J & VALENTE MC. 2003. Terminalia L. (Combretaceae) na região Sudeste do Brasil. Bradea 16: 99-123. and Ribeiro et al. (2018)RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257., the synopsis presented here is intended to provide information about Terminalia s.s. taxa of the Brazilian Amazon with: 1) diagnostic characters, identification key and illustrations of all taxa; 2) characterization of patterns of geographic distribution, diversity and richness of Terminalia species, including new occurrence records; 3) conservation status assessment according to “B1” criteria of IUCN red list (IUCN 2017IUCN - INTERNATIONAL UNION FOR CONSERVATION OF NATURE. 2017. Guidelines for using the IUCN Red List Categories and criteria, Version 13. Available at <http://www.iucnredlist.org/documents/RedListGuidelines.pdf>. Access on 19 January 2021.
http://www.iucnredlist.org/documents/Red...
) and definition of species registered in Protected Areas (PA) and their respective PA.

MATERIALS AND METHODS

Brazilian Amazon

The Amazon Domain has about six million km2 comprising various ecosystems, including rainforest, savanna (Amazonian savannas) and flooded fields (Carvalho & Mustin 2017CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahs. Nat Ecol Evol 1(4): 100., Gomes et al. 2019GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.). This extensive region encompasses the following countries: Brazil, Bolivia, Colombia, Ecuador, French Guiana, Guyana, Peru, Suriname, and Venezuela (Gomes et al. 2019GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.).

Within the geographic boundaries of Brazil, the Amazon is a phytogeographic domain present in the North Brazilian geopolitical region and in some states in the Central-West and Northeast regions (Figure 1a), including a region known as the “Arc of Deforestation”, which is an area that has the highest deforestation rates within the legal Brazilian Amazon (Steege et al. 2003STEEGE H, PITMAN N, SABATIER D, CASTELLANOS H, VAN DER HOUT P, DALY DC & SILVEIRA M ET AL. 2003. A spatial model of tree α-diversity and tree density for the Amazon. Biodivers Conserv 12: 2255-2277., Herrera et al. 2019HERRERA D, PFAFF A & ROBALINO J. 2019. Impacts of protected areas vary with the level of government: Comparing avoided deforestation across agencies in the Brazilian Amazon. Proc Natl Acad Sci USA 116(30): 14916-14925., IBGE 2021IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATISTICA. 2021. Regional maps. Available at <https://www.ibge.gov.br/en/geosciences/maps/regional-maps/17927-legal-amazon.html?edicao=17929&t=sobre>. Access on 28 January 2021.
https://www.ibge.gov.br/en/geosciences/m...
).

Figure 1
a,b,c. Terminalia s.s. taxa in the Brazilian Amazon. —a. Distribution pattern. —b. Species richness. —c. Diversity using the Shannon índex. Grids in 1° × 1° grids. Arrows indicate new occurrences.

According to Cardoso et al. (2017)CARDOSO D ET AL. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA 114: 10695-10700., the Amazon region has about 7.000 spp. of trees (48% of the total plant biodiversity of the Amazon region). Brazil stands out for having almost 5.000 spp., equivalent to 68% of the tree species occurring in the Amazon domain. Therefore, the considerations presented here regarding the distribution, conservation, diversity and richness aspects of Terminalia taxa and vegetation types follow the limits of the Amazonian phytogeographic domain in Brazil (including states in the Central-West, North and Northeast regions) using shapefiles (.shp) obtained from the Ministry of the Environment (MMA 2021MMA – MINISTÉRIO DO MEIO AMBIENTE, 2021. Download de dados geográficos. Available at <http://mapas.mma.gov.br/i3geo/datadownload.htm>. Access on 28 January 2021.
http://mapas.mma.gov.br/i3geo/datadownlo...
) and National Institute for Space Research (INPE 2021INPE - INSTITUTO NACIONAL DE PESQUISAS ESPACIAIS. 2021. AmBData Varíaveis para modelagem de distribuição de espécies. Available at http://www.dpi.inpe.br/Ambdata/English/vegetation.php. Access on 28 January 2021.
http://www.dpi.inpe.br/Ambdata/English/v...
) websites.

Morphological analysis

The taxonomic synopsis presented in this study was based on the morphological analysis of herborized specimens and field collections. Exsiccates from the following herbaria were examined: BM, BR, CEN, CTBS, ESA, GH, GOET, F, FI, FLAS, HUEFS, IAN, INPA, K, LE, LTR, M, MA, MAR, MG, MO, MYF, NY, OXF, P, PEUFR, R, RB, RON, S, SPF, TCD, U, UB, UC, UNIP, US, VEN and W (acronyms according to Thiers 2021THIERS B. 2021 [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at http://sweetgum.nybg.org/science/ih. Access 28 January 2021.
http://sweetgum.nybg.org/science/ih...
). The standardization of vegetative and reproductive structural terminology was based on Stace (1965)STACE CA. 1965. The significance of the leaf epidermis in the taxonomy of the Combretaceae. A general review of tribal, generic and specific characters. Bot J Linn Soc 59: 229-252., Hickey (1973)HICKEY LJ. 1973. Classification of the architecture of dicotyledonous leaves. Am J Bot 60: 17-33. and Radford et al. (1974)RADFORD AE, DICKSON WC, MASSEY JR & BELL CR. 1974. Vascular plant systematics. New York: Harper and Row, 891 p.. Species determination was based mainly on Stace (2010)STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p. and data from the Brazilian Flora 2020 project (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). Furthermore, notes of geographic distributions and habitat data were based on field collections and information from the literature and exsiccate labels.

All original citations and types were analyzed by the authors and are indicated by the barcode or herbarium accession number and exclamation point. The protologues and types were examined through the Global Plants on JSTOR (2021)JSTOR. 2021. Global Plants on JSTOR. Available at <https://plants.jstor.org/>. Access on 28 January 2021.
https://plants.jstor.org/...
and the Biodiversity Heritage Library (2021)BIODIVERSITY HERITAGE LIBRARY. 2021. The Biodiversity Heritage Library. Available at <https://www.biodiversitylibrary.org/>. Access on 1 January 2021.
https://www.biodiversitylibrary.org/...
websites.

For each species, this synopsis includes the characteristics of taxa essential for recognition, illustrations (some published here for the first time), a brief characterization of distribution, ecology, conservation comments and some selected specimens.

Morphological diagnostic characteristics not yet highlighted in previous works were evidenced here as inflorescence patterns in Terminalia ramatuella Alwan & Stace and T. yapacana Maguire and details about the flowers of T. dichotoma G. Mey. and T. lucida Hoffmanns. ex Mart. & Zucc. that aid in the recognition and distinction of these taxa. Additional comments that help to distinguish the taxa which have not yet been extensively studied, such as T. crispialata (Ducke) Alwan & Stace, T. ramatuella Alwan & Stace, T. virens (Spruce ex Eichler) Alwan & Stace and T. yapacana Maguire, are explored in this study.

Species occurrence data and spatial analyses

Initially, we compiled the occurrence data for all Terminalia species recorded in the Brazilian Amazon based on the synopsis proposed here and other literature and database sites, such as Flora Neotropica Monograph (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p.), speciesLink system of the Reference Center on Environmental Information – CRIA (CRIA 2021CRIA. 2021. speciesLink. Available at <http://www.splink.org.br/>. Access on 17 January 2021.
http://www.splink.org.br/...
), the Reflora Virtual Herbarium (REFLORA 2021REFLORA - REFLORA VIRTUAL HERBARIUM. 2021. Reflora Virtual Herbarium. Available at http://reflora.jbrj.gov.br/reflora/herbarioVirtual. Access on 17 January 2021.
http://reflora.jbrj.gov.br/reflora/herba...
) and the Global Biodiversity Information Facility - GBIF (GBIF 2021). The initial data set contained 1300 records, which was reduced to 872 records for the 11 species studied after being checked and validating taxonomic identification.

Whenever possible, records without coordinates were georeferenced using the “GeoLoc” tool available on CRIA (http://splink.cria.org.br/geoloc?criaLANG=pt) or Google Earth (https://www.google.com/earth/). Duplicate occurrences for a municipality and taxon or records prior to 1945 were disregarded for spatial analyses, the latter due to possible inaccuracies and lack of information, resulting in about 100 records.

All records verified and confirmed for Terminalia species in the Brazilian Amazon were plotted on a map divided into 782 grid squares of 1×1° representing our Operating Geographic Units (OGU). For each grid square, the species richness (as the total number of species) and diversity (using the Shannon index, which considers the contribution of each species per grid square) were calculated using DIVA-GIS 7.5 program (Hijmans et al. 2001HIJMANS RJM, CRUZ E, ROJAS E & GUARINO L. 2001. DIVA-GIS. A geographic information system for the management and analysis of genetic resources data, Peru: International Potato Center and International Plant Genetic Resources Institute, 40 p.). All the maps presented here were generated through the Quantum GIS 3.8 software (QGIS 2021QGIS. 2021. QGIS Geographic Information System. Open Source Geospatial Foundation. Available at http://qgis.osgeo.org. Access on 28 January 2021.
http://qgis.osgeo.org...
).

Conservation aspects

The preliminary conservation status of the Terminalia taxa registered for the Brazilian Amazon were defined according to criteria “B1” proposed by the IUCN red list, Version 13 (IUCN 2017), considering the EOO (Extent of occurrence) and AOO (Area of occupancy), which were both implemented in GeoCAT (Bachman et al. 2011BACHMAN S, MOAT J, HILL AW, TORRE J & SCOTT B. 2011. Supporting red list threat assessments with GeoCAT: Geospatial conservation assessment tool. ZooKeys 150: 117-126.). In addition, a table with the number of Protected Areas (PA) is provided, and the names of Protected Areas (PA) (Municipal, State or Federal levels) for each species are mentioned (Table I).

Table I
Distribution and conservation data of Terminalia s.s. occurring in the Brazilian Amazon. Abbreviations of Brazilian states: AC – Acre, AL – Alagoas, AM – Amazonas, AP – Amapá, BA – Bahia, CE – Ceará, GO – Goiás, MA – Maranhão, MG – Minas Gerais, MT - Mato Grosso, MS - Mato Grosso do Sul, PA – Pará, PI – Piauí, PR – Paraná, RJ – Rio de Janeiro, RO – Rondônia, RR – Roraima, SP – São Paulo, TO – Tocantins. Red List Category: CR - Critically endangered, EN – Endangered, VU – Vulnerable, LC - Least concern. *indicates new occurrences. Abbreviations for Conservation units: APA - Environmental Protection Area, FLONA - National Forest, REBIO - Biological Reserve, RESEX - Extractive Reserve.

RESULTS

Taxonomic and morphological aspects of Terminalia s.s.

In the Brazilian Amazon, 11 native species of Terminalia s.s. were registered: Terminalia amazonia (J.F.Gmel.) Exell, T. argentea, T. crispialata, T. dichotoma, T. glabrescens Mart., T. lucida, T. oblonga (Ruiz & Pav.) Steud., T. quintalata Maguire, T. ramatuella, T. virens and T. yapacana. The exotic species, T. catappa L. was not included in this study.

According to Stace (2010)STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., the genus representatives in the Neotropical region are positioned in 12 sections. Of these, nine include taxa registered for Brazil and the Amazon species were recorded in six sections (Chuncoa (Pav. ex Juss.) C.B. Clarke, Diptera (Eichler) Engl. & Diels, Pachyphylla Maguire & Exell, Ramatuellea (Kunth) Alwan & Stace, Rhombocarpae Engl. & Diels and Oblongae Engl. & Diels) (Table I).

The sections Pachyphylla and Ramatuellea stand out for having representatives that only occur in the Amazon domain (Brazil and extra-Brazil). In addition, the taxa of these sections have less occurrence records than the other Terminalia taxa registered in Brazil.

Geographic distribution, richness and diversity patterns

Terminalia s.s. is widely distributed in the Brazilian Amazon (Figure 1a) and has the following distribution limits: to the north, T. amazonia in the municipality of Oiapoque, AP; to the south, T. oblonga in the municipality of Cabixi, RO; to the east, T. lucida in the municipality of Alcântara, MA; and to the west, T. dichotoma in the municipality of Rodrigues Alves, AC.

Regarding collections efforts’, T. dichotoma, T. lucida and T. amazonia stood out for presenting the largest number of records for the Amazon, with 23, 20 and 17 occurrences in different municipalities, respectively, while T. yapacana (one) and T. ramatuella (two) have the lowest number of occurrences.

Terminalia yapacana presents its first register in the Brazilian territory in Amazonas state, and until now, the taxon only had been known in the Venezuelan Amazon. In Amazonas state, the species is associated with the rainforest near river courses (Figure 1a). In addition to T. yapacana, three other new occurrences of Terminalia were identified for the Brazilian Amazon (Table I), one for T. amazonia in the state of Rondônia and two for T. glabrescens in the states of Pará and Rondônia (Figure 1a).

Three richness centers were identified in the region, the first and second in the state of Amazonas with four species each and a third in the state of Pará with three taxa (Figure 1b). Terminalia s.s. diversity in the Amazon (Figure 1c) seems to be associated with three main areas in state of Amazonas with a diversity index of 1.38 and 1.32, respectively, and the third in the state of Pará with an index of 1.09. The grid squares with highest diversity are located in the north of the Amazon region. However, we highlight a second center of diversity in the south, in the state of Rondônia, with lower values, index of 0.62.

Conservation

Of the eleven species of Terminalia confirmed and analyzed here, six (55%) (T. amazonia, T. argentea, T. dichotoma, T. glabrescens, T. lucida and T. oblonga) were recorded in protected areas (PA) in the Amazon. Of the taxa occurring in PA, T. oblonga presented the largest number of records (4) in different units (Table I).

The species with the highest EOO was T. amazonia (2,511,901,232 km2) and the smallest were T. ramatuella and T. yapacana (0,000 km2), whose species were represented by few collections. T. dichotoma stands out with the largest AOO area (92,000 km2), while T. yapacana presented the smallest (4,000 km2). More detailed information can be found in species comments and in Table I.

Taxonomic treatment

1. Terminalia L., Syst. Nat. 12. (2): 674. 1767. TYPE: Terminalia catappa L.

Shrubs to trees, branches glabrous. Leaves alternate, spirally arranged, usually clustered at the end of the branches. Glands 2 or absent in the petiole. Inflorescences in subcapitate, capitate or elongated spikes, axillary or terminal. Flowers unisexual or bisexual. Calyx (4−)5−lobed, developed lobes, reflexed or not. Corolla absent. Stamens (8−)10, inserted in two whorls; anthers versatile. Nectariferous disk, usually developed, ringlike, margin free. Fruit betulid, dried, actinomorphic or zygomorphic, 2−5-alate.

Key to the Brazilian Amazon species of Terminalia s.s.

1a. Leaves with sparse to dense-sericeous, dense cinereous-sericeous, or dense-puberulous indument in the abaxial surface.

2a. Leaves without domatia; subcapitate or capitates spikes ...............……… T. glabrescens Mart.

2b. Leaves with domatia; elongated spikes.

3a. Leaves chartaceous to subcoriaceous, acuminate apex; eucamptodromous-brochidodromous venation; zygomorphic fruit …........................................……. T. argentea Mart. & Zucc.

3b. Leaves always coriaceous, rounded to retuse apex; brochidodromous venation; actinomorphic fruit.

4a. Leaves with 5−7 pairs of secondaries veins; fruits with an indumentum dense cinereous-sericeous, wings with entire margins ................................................................................. T. ramatuella Alwan & Stace

4b. Leaves 8−14 pairs of secondaries veins; fruits glabrous, wings with crispate margins …………..……...… T. crispialata (Ducke) Alwan & Stace

1b. Leaves with abaxial surface glabrous.

5a. Subcapitate spikes; fruit wings with sinuate margins …................................................................... T. virens (Spruce ex Eichler) Alwan & Stace

5b. Elongated spikes; fruit wings with flat margins.

6a. Chartaceous to subcoriaceous leaves.

7a. Leaves with 3−5 pairs of secondaries veins; style glabrous; fruits 4−7 × 10−17 mm, 4-winged, unequal wings …….…….. T. amazonia (J.F.Gmel.) Exell

7b. Leaves with 5−8(−10) pairs of secondaries veins; style villous to dense-villous; fruits 24−36 × 27−50 mm, 2-winged, equal wings.

8a. Leaves with cuneate base; style villous in the proximal half; fruit with spongy wings ………….…….....................................……….. T. dichotoma G. Mey.

8b. Leaves with attenuate base; style dense-villous from the proximal half to the apex; fruit with coriaceous wings …..... T. oblonga (Ruiz & Pav.) Steud.

6b. Strongly coriaceous leaves.

9a. Leaves with acute to short-acuminate apex; style dense-villous, except glabrous only at apex; fruits 12−23 × 16−32 mm, 2-winged, zygomorphic ………..………... T. lucida Hoffmanns. ex Mart. & Zucc.

9b. Leaves with rounded to retuse apex; style glabrous or sparse-pubescent at the base; fruits 3−11 × 2−10 mm, (4-)5-winged, actinomorphic.

10a. Leaves narrow-obovate to oblanceolate, 3−5.7 × 1.4−3.1 cm; fruit with rounded wings …….......................................................…........ T. yapacana Maguire

10b. Leaves obovate to oblong-obovate, 8−14.1 × 5.8−7.6 cm; fruit with narrow-elliptic wings …………................................ T. quintalata Maguire

1. Terminalia amazonia (J.F.Gmel.) Exell, Fl. Suriname 3(1): 173. 1935. TYPE: Peru. Sylvis fluvio Amazonio contermis, Chunco du Maragnon, 1786 (fl.), Pavon & Dombey s.n. (holotype, P-00681414!) (Figure 2a-c).

Figure 2
a,b,c. Terminalia amazonia —a. Leaf. —b. Fruit. c. Apical view of the fruit. d,e. T. argentea —d. Leaf with detail of petiolar glands. —e. Fruit (front view). f,g,h. T. crispialata —f. Leaf. g,h. Fruit. i,j,k. T. dichotoma —i. Leaf. j. Flower. k. Fruit. l,m,n. T. glabrescens —l. Leaf. m. Fruit (front view). n. Fruit (apical view). o,p,q. T. lucida —o. Leaf. p. Flower. q. Fruit (front view). a,c. LR Marinho & BGS Ribeiro 726 (IAN); d,e. JM Pires & GA Black 6437 (IAN); f,h. Huber et al. 10806 (INPA, K, MIRR, NY, US); i,j. DF Austin et al. 7414 (INPA, RB); k. NT da Silva 4814 (MG, NY, UEC); l, n. PV Oliveira et al. 11-286 (RB); o. PC da S. Rosário et al. 158 (MG, NY); q. IC Antônio PSCF 912 (IAN, MG, UFPA).

Terminalia amazonia is very closely related to T. glabrescens in morphological aspects of its leaves, and pattern of its inflorescence and fruits. However, Terminalia amazonia can be differentiated by its leaves glabrous on the abaxial face (vs. leaves dense-sericeous with ferrugineous trichomes), 3−5 pairs of secondary veins (vs. 6−8 pairs of secondary vein pairs), and fruits 4-winged (vs. fruits 5-winged).

Selected examined material. BRAZIL. Acre: Sena Madureira, trail to rio Iaco from km 7 road Sena Madureira to Rio Branco, 68º 39’ 24” W, 9º 3’ 57” S, 1 Oct.1968 (fr), G.T. Prance 7717 (F, INPA, K, MG, U, US). Maranhão: Itapecuru Mirim, Fazenda São Benedito, 29 Nov.1975 (fl), D.P. Lima 13401 (PEUFR). Pará: Almeirim, Jari, estrada entre Planalto A e Tinguelim, km 16, 3 Feb. 1970 (fr), N.T. Silva 3412 (IAN); Belém, Bosque Municipal Rodrigues Alves, mata de terra firme, 28 Dec. 1946 (fl), A. Ducke 2042 (IAN, MO, NY, R, RB).

Habitat, distribution and conservation status: Terminalia amazonia is distributed from Mexico to Bolivia (Stace, 2010). In Brazil, the species occurs in the North (Acre, Amapá, Amazonas, Pará and Rondônia) and Northeast (Maranhão, Pernambuco and Piauí) regions (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). T. amazonia is found in areas of Ombrophyllous and Terra-Firme forests in the Brazilian Amazon. A new occurrence is reported here for the state of Rondônia (Figure 1a). Regarding conservation aspects, the species is designated as least concern (LC) due to its EOO of 2,511,901,232 km2 and endangered (EN) due to its AOO of 68,000 km2 (Table I). T. amazonia has been recorded in protected areas in the Amazon and indigenous lands, including the National Forest of Tapajós and Alto Turiaçu Indigenous Land of the Ka’apor Indigenous People (Table I).

Vernacular names: Chapada (Maranhão), cuiarana (Pará), miringiba de mata (Pará), mirindiba roxa (Rondônia), periquiteira (Pará), tanimbuca (Amapá), tanimbuca folha média (Pará), tukury’y (Maranhão), tukur-y-wa-´y (Maranhão).

Notes: Terminalia amazonia, both in the original work and in the revision by Stace (2010)STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., did not present any material in herbaria related to the type collection. Based on information from the protologue, the collection of Pavon & Dombey in 1786 deposited at the P herbarium is referred to as the type-collection herein. Unlike Terminalia glabrescens, T. amazonia has more records in the Amazon region, while T. glabrescens is more frequent in the Northeast and Southeast regions of Brazil, in Savanna (Cerrado), Stepic Savanna (Caatinga) and Ombrophyllous Forest (Atlantic Rainforest).

2. Terminalia argentea Mart. & Zucc. Flora 7(1; Beil. 4): 130. 1824; Nov. Gen. Sp. Pl. 1: 43. 1824. TYPE: Brazil. Bahia: In montosis ad villa do Rio Contos, 1817-1820, Martius 1714 (holotype, M0146731!; isotypes, M0146732!, M0146733!) (Figure 2d-e).

Terminalia argentea is distinguished by its narrow-elliptic, elliptic to ovate leaves with acuminate apex, dense-sericeous indument on adaxial surface when young, eucamptodromous-brochidodromous venation; short capitate spikes and zygomorphic 2-winged fruit with rounded wings.

Selected examined material: BRAZIL. Mato Grosso: Garapu, Serra do Roncador, vicinity of Garapu, 2 Oct.1964 (fr), G.T. Prance et al. 59230 (K, LTR, M, NY, S, UB, US). Pará: Belém, Bosque Municipal Rodrigues Alves, 28 May 1947 (fl, fr), J.M. Pires & G.A. Black 1622 (IAN); Novo Progresso, Serra do Cachimbo, 17 Dec. 1956 (fr), J.M. Pires & G.A. Black 6437 (BM, IAN, LTR, NY, UB). Tocantins: Presidente Kennedy, 2 Feb. 1980 (fr), T.C. Plowman et al. 8301 (INPA, LTR, MG, MO, NY, US).

Habitat, distribution and conservation status: Terminalia argentea is exclusive to South America, occurring in Brazil, Bolivia, Paraguay and Peru (Stace, 2010). In Brazil, it is one of the most widely distributed taxa in the country, occurring in all regions of the Brazilian territory (Central-West, North, Northeast, Southeast and South) (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). In the Amazon region (Figure 1a), the species was registered in the states of Mato Grosso (Central-West), Pará and Tocantins (North). It is often found in Brazilian territory in areas of Savanna, Gallery Forest and Ombrophyllous Forest within the Amazon phytogeographic domain. As for conservation, T. argentea is hereby designated as least concern (LC) due to its EOO of 614,719,310 km2 and endangered (EN) due to its AOO of 24,000 km2 (Table I). The taxon was registered in Protected Areas in the Amazon, especially in the Nascentes da Serra do Cachimbo Biological Reserve, which guarantees the preservation of the vegetation in the Arc deforestation region (Table I).

Vernacular names: Capitão do campo (Mato Grosso), pau de bicho (Mato Grosso), tanimbuca amarela (Pará).

3. Terminalia crispialata (Ducke) Alwan & Stace, Ann. Missouri Bot. Gard. 76: 1126. 1989. TYPE: BRAZIL. Amazonas: Caatinga ad Igarape Jurupary, baixo Rio Uaupés, 2 Nov. 1932, A. Ducke 25024 (holotype, RB [barcode] 537404!; isotypes, K-000640640!, US-00117645!) (Figure 2f-h).

Terminalia crispialata is characterized by its leaves with dense-puberulous indument only on the abaxial surface of leaves, 4(-5)-winged fruits, wings with crispate margins.

Selected examined material: BRAZIL. Amazonas: Santa Isabel do Rio Negro, na beira do Lago Dodona, 20 Sep. 2000 (fr), J.A.C. Silva 913 (INPA, MG). Roraima: Caracaraí, 16 Apr. 1974 (fr), J.M. Pires et al. 13992 (IAN, LTR).

Habitat, distribution and conservation status: Terminalia crispialata occurs in Brazil, Colombia and Venezuela (Stace, 2010). In Brazil, the taxon was registered only in the states of Amazonas and Roraima, both in the Northern region (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). T. crispialata occurs in environments of Amazonian Campinarana, inundated forest known as igapó and Amazonian Savanna. This species is designated as least concern (LC) due to its EOO of 196,098,824 km2 and endangered (EN) due to its AOO of 28,000 km2 (Table I). The species has not yet been registered in protected areas in the Amazon (Table I).

Vernacular names: None registered.

4. Terminalia dichotoma G. Mey. Prim. Fl. Esseq. 177-178. 1818 ≡ Terminalia latifolia var. dichotoma (G. Mey.) DC., Prodr. (1828: 12). TYPE: Guyana. Essequibo: In silvis insulae Arowabish Essequibo, G. Meyer 113 (holotype, GOET-000941!) (Figure 2i-k).

Terminalia dichotoma has a close affinity to T. lucida due to leaf shape and fruit consistency. However, T. dichotoma is distinguished from T. lucida by longer leaves 9−22 × 4−10 cm (vs. 5−7.5 × 1.6−3.4 cm) and chartaceous to subcoriaceous (vs. leaves coriaceous); style villous in the proximal half (vs. dense-villous, except glabrous only at apex) and fruit 28−36 × 27−29 mm (vs. 12−23 × 16−32 mm), with spongy wings (vs. coriaceous wings).

Selected examined material: BRAZIL. Acre: Rio Juruá, 1 km upstream from Colônia Rodriguez Alvez, Oct. 1986, (fr), Campbell et al. 10983 (INPA, LTR, MG, NY). Amapá: Rio Oiapoque, river banks between Oiapoque and Santo Antonio, 26 July 1960, (fl), H.S. Irwin et al. 47154 (IAN, K, LTR, MG, NY, R). Amazonas: Alvarães, Estação Ecológica de Mamirauá, 23 Nov. 1999, (fr), M.A.D de Souza et al. 763 (IAN, INPA, RB). Pará: Jacundá, Jatobal, area to be flooded by Tucuruí dam, margin of rio Tocantins, 20 Oct. 1977 (fl), A.S.L. Silva et al. 77 (K, MG, US). São Domingos do Capim, comunidade Independência, 6 Sep.1999, (fr), A.G. Nave & A. Novello 6 (ESA, UNIP).

Habitat, distribution and conservation status: Terminalia dichotoma occurs in different South American countries (Brazil, Ecuador, Guyana, French Guyana, Peru, Suriname, Trinidad and Venezuela). In Brazil, the taxon presents records in the North and Northeast regions (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). In the Brazilian Amazon, T. dichotoma was found in inundated forest known as várzea and Ombrophyllous Forest vegetations. As for conservation status, the species was designated as least concern (LC) due to its EOO of 2,445,804,330 km2 and endangered (EN) due to its AOO of 92,000 km2 (Table I). It has been registered in protected areas such as the Mamirauá Sustainable Development Reserve (Table I).

Vernacular names: Cinzeiro (Pará), cuiarana (Pará), tanibouca (Pará), tanimbouca (Amapá, Amazonas), tanimbuca (Pará).

5. Terminalia glabrescens Mart. Flora 20, Beibl. 2: 124. 1837 ≡ Myrobalanus glabrescens (Mart.) Kuntze, Revis. Gen. Pl. 1: 237. 1891. TYPE: Brazil. Rio de Janeiro: Serra da Broca, prov. Sebastianopolis, July-Aug. 1833, Luschnath s.n. (holotype, BR697541!; isotypes, LE not seen, M not seen, P not seen) (Figure 2l-n).

Terminalia glabrescens is distinguished by its leaves sericeous with ferrugineous trichomes, 6−8 pairs of secondary vein pairs, and fruits 5-alate. For full comparison see T. amazonia.

Selected examined material: BRAZIL. Mato Grosso: Itaúba, resgate de flora da UHE Colíder, 3 Sep. 2015 (fr), P.V. Oliveira et al. equipe 11-286 (RB). Pará: Itaituba, estrada Santarém-Cuiabá, BR 163, km 794, Serra do Cachimbo, 26 Apr.1983 (fr), I.L. Amaral 958 (K, INPA, UB, US).

Habitat, distribution and conservation status: Terminalia glabrescens occurs in southwestern South America in Brazil, Bolivia and Paraguay (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p.). In Brazil, the species is registered in all regions (Central-West, North, Northeast, Southeast and South). In the Amazon, T. glabrescens was recorded in Ombrophyllous Forest and Amazonian Savanna environments, as well as in ecotone (transition) areas between these vegetations, specifically in Mato Grosso state. The states of Pará and Rondônia are reported here with two new occurrences for the taxon. Occurrences of T. glabrescens in the Amazon, including the new records, appear to represent the septentrional boundary of taxon distribution. The species has been defined here as least concern (LC) due to its EOO of 67,959,874 km2 and endangered (EN) due to its AOO of 12,000 km2 (Table I). T. glabrescens was only recorded in the Guariba-Roosevelt Extractive Reserve (Table I).

Vernacular names: Cuiarana (PA).

6. Terminalia lucida Hoffmanns. ex Mart. & Zucc. Flora 7(1, Beil.): 130. 1824; Nov. Gen. Sp. Pl. 1: 43. 1824 ≡ Myrobalanus lucida (Hoffmanns ex Mart. & Zucc.) Kuntze, Revis. Gen. Pl. 1: 237. 1891. TYPE: Brazil. Pará: Siber, 1812, J.C. von Hoffmannsegg s.n. (lectotype, designated by Stace [2010: 181] BR-0000006975067!; isolectotype, BM-000838189!) (Figure 2o-q).

Terminalia lucida can be recognized and distinguished from T. dichotoma by its coriaceous leaves, style villous, except glabrous only at apex and fruit with 12−23 × 16−32 mm, coriaceous wings.

Selected examined material: BRAZIL. Maranhão: Palmeirândia, 16 Aug. 2011 (fl), M. Ribeiro PM21 (IAN, MAR). Pará: Altamira, Acampamento de Aero-Sul a 1 km de Porto Alegre, 24 Oct. 1986 (fr), S.A. da M. Souza et al. 464 (MG, MO, SPF).

Habitat, distribution and conservation status: According to Stace (2010)STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p., Terminalia lucida occurs in Africa (Guinea, Guinea Bissau and Sierra Leone) and South America (Brazil, Colombia, French Guiana, Guyana and Suriname), is characterized by a disjunct distribution. In Brazil, the taxon is registered for the Central-West (Goiás, Mato Grosso), Northeast (Bahia, Maranhão, Piauí) and North (Pará, Tocantins) regions (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). In the Amazon, T. lucida has been found in areas of Várzea and in sandy environments, such as Coastal Forest. The species has been defined here as least concern (LC) due to its EOO of 1,071,85,167 km2 and endangered (EN) due to its AOO of 80,000 km2 (Table I). In protected areas in the Amazon, it occurs only in the Marajó Archipelago Environmental Protection Area (APA).

Vernacular names: Cararambeira (Pará), cinzeiro (Pará), cororombeira (Pará), cuia-rana or cuiarana (Pará), tanibouca (MA).

7. Terminalia oblonga (Ruiz & Pav.) Steud., Nomencl. Bot., ed. 2, 2: 668. 1841 ≡ Gimbernatia oblonga Ruiz & Pav., Syst. Veg. Fl. Peruv. Chil. 275. 1798 ≡ Chuncoa oblonga (Ruiz & Pav.) Pers., Syn. Pl. 1: 486. 1805 ≡ Myrobalanus oblonga (Ruiz & Pav.) Kuntze, Revis. Gen. Pl. 1: 237. 1891. TYPE: Peru. Huanuco: Pozuzo nemoribus, 1780-1788, R. Pavón & Dombey s.n. (holotype MA-AJB04-D-1568!; isotypes: F not seen, FI not seen, MA-00813647!, MA-00813648!, OXF-00059256!) (Figure 3a-b).

Figure 3
a,b. Terminalia oblonga —a. Leaf. —b. Fruit (front view). c,d. T. quintalata —c. Leaf. —d. Fruit (front view). e,f. Terminalia ramatuella —e. Branch with infructescence. —f. Fruit (front view). g,h. T. virens —g. Leaf. —h. Fruit (front view). i. T. yapacana —i. Branch with leaves and infrutescence. a,b. CS Figueiredo 829 (MO, NY); c,d. GT Prance 28874 (INPA, NY, RB); e,f. HC de Lima et al. 3194 (NY, RB); g,h. JA Silva 374 (INPA, K, NY, SP, US); i. B Maguire 30480 (K, RB).

Terminalia oblonga is distinguished from the other species by elliptic-oblong, oblong to obovate-oblong leaves, acute to short-acuminate apex, attenuate base, elongated inflorescence, style dense-villous from the proximal half to the apex and fruits 2-winged with wings rounded or subtriangular, coriaceous.

Selected examined material: BRAZIL. Acre: Sena Madureira, Reserva Extrativista Cazumbá-Iracema, 3 May 2017 (fr), H. Medeiros et al. 2149 (RB). Amazonas: Benjamin Constant, Esperança, ad ostium fluminis Javary, 26 Jan.1942 (fl), A. Ducke 880 (IAN, MO, US). Rondônia: Porto Velho, margem esquerda do rio Madeira, 22. June 2010 (fr), G. Pereira-Silva 15428 (CEN, HUEFS, INPA, NY, RB, RON).

Habitat, distribution and conservation status: Terminalia oblonga is distributed in Central and South America (Stace, 2010). In Brazil, the taxon was registered in the North (Acre, Amazonas, Pará and Rondônia) and Northeast (Bahia and Pernambuco) regions of the country. In the Amazon, T. oblonga occurs in Igapó, Terra Firme Forest, Ombrophyllous Forest and Amazonian vegetation. The species has been designated as least concern (LC) due to its EOO of 1,533,416,561 km2 and endangered (EN) due to its AOO of 64,000 km2 (Table I). The taxon occurs in protected areas and indigenous lands in the Amazon, among which includes the Raimundo Irineu Serra APA.

Vernacular names: Andiroba-rana (Pará), imbiridiba amarelo (Acre).

8. Terminalia quintalata Maguire Bull. Torrey Bot. Club 75: 649. 1948. TYPE: Guyana. Essequibo: Potaro River Gorge, below Amatuk Portage, 19 May 1944, Maguire & Fanshawe 23551 (holotype, NY-00245980!; isotypes: BM not seen, BR-0000006975142!, F-0054651!, FDG not seen, G not seen, K-000640650!, GH-00068632!, MO-313448!, P-01901247!, RB-00537371!, RB-00537415!, U-0001200!, UC-00793860!, US-00117618!, VEN-0029118!) (Figure 3c-d).

Terminalia quintalata seems to be similar to T. yapacana, however, differs due to the larger leaves 8−14.1 × 5.8−7.6 cm, obovate or oblong-obovate (vs. leaves 3−5.7 × 1.4−3.1 cm, narrow-obovate to oblanceolate), elongated inflorescence 7−16 cm (vs. 5−7.5 cm), (4-) 5-winged fruits, with narrow-elliptic wings.

Selected examined material: BRAZIL. Amazonas: Barcelos, 3 km ao sul da parte central da Serra Aracá e 8 km a leste do rio Jauari, 29 Feb. 1984 (fr), W.A. Rodrigues et al. 10489 (K, INPA, NY, US). Rondônia: São Miguel do Guaporé, July 1975 (fl), B.G.S. Ribeiro 1099 (IAN, MG).

Habitat, distribution and conservation status: Terminalia quintalata is distributed in Brazil, Guyana and Venezuela, generally found along the course of the Amazon rivers (Stace, 2010). In Brazil, it only occurs in the Amazon, with records in the states of Amazonas and Rondônia (Ribeiro et al. 2020RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.). The species was recorded in Ombrophyllous Forest and Amazonian Savanna. T. quintalata was designated here as least concern (LC) due to its EOO of 306,888,235 km2 and as endangered (EN) due to its AOO of 12,000 km2 (Table I). Based on the records, it was not possible to verify this taxon in protected areas in the Amazon.

Vernacular names: None registered.

9. Terminalia ramatuella Alwan & Stace Ann. Missouri Bot. Gard. 76: 1126. 1989. TYPE: Venezuela. Amazonas: Rio Atapabo, 1799-1804, A.J.A. Bonpland s.n. (holotype, P-00679492!; isotypes, P-00789746!, F-0044100F!) (Figure 3e-f).

Terminalia ramatuella is a well-defined species, distinct from similarly distributed species of the genus, such as T. crispialata, T. quintalata and T. virens. It is characterized by its narrow-obovate or elliptic, 5−7 pairs of secondaries veins and dense cinereous-sericeous indument on the abaxial surface of leaves and fruits. In addition, capitate spikes and fruits 4-5 winged, wings narrow-rhombic, entire.

Selected examined material: BRAZIL. Amazonas: São Gabriel da Cachoeira, Comunidade de Camarão do Rio Içana, 21 July 2012 (fl), F. Bonadeu 667 (CTBS, HUEFS, INPA); Beira do Rio Cubate, 19 Nov. 1945 (fr), R.L. Fróes 21421 (F, IAN, K, NY, US).

Habitat, distribution and conservation status: Terminalia ramatuella has limited occurrence in Brazil, Colombia and Venezuela (Stace, 2010). It is a taxon with few records in Brazilian collections. For the Brazilian Amazon, the species only occurs in the state of Amazonas in Ombrophyllous and Várzea Forests vegetation, usually associated with rivers. T. ramatuella was designated as critically endangered (CR) due to its EOO of 0,000 km2 and critically endangered (CR) due to its AOO of 8,000 km2 (Table I). Based on the records, it was not possible to verify this taxon in protected areas in the Amazon.

Vernacular names: None registered.

Notes: A common misspelling (Terminalia ramatuellea instead of T. ramatuella) of the taxon name has been observed in some studies. In the original work, the taxon is called T. ramatuella, as in this study.

10. Terminalia virens (Spruce ex Eichler) Alwan & Stace, Ann. Missouri Bot. Gard. 76(4): 1126. 1989. TYPE: Venezuela. Amazonas: Rio Guaima, above its confluence with Rio Casiquiare, Nov. 1854, R. Spruce 3758 (lectotype, designated by Stace [2010: 246] W-0000257!; isolectotypes, A, GH, B destroyed neg. in US not seen, BM not seen, BR [barcode] 5639618 not seen, C not seen, CGE not seen, F not seen, G not seen, GOET not seen, K-000640638!, K-000640639!, LE not seen, OXF-00059257!, P-01901334!, P-01901335!, RB [barcode] 17671!, TCD-0000706!, W-0333711!) (Figure 3g-h).

Terminalia virens is distinguished from T. ramatuella by its elliptic-oblong to obovate-oblong leaves (vs. narrow-obovate or elliptic) and subcapitate inflorescences (vs. elongated inflorescences). In addition, T. virens may be similar to T. crispialata, differing by elliptic, rare rounded, fruits, wings with entire or sinuate margins, while T. crispialata has ovate fruits, wings with crispate margins.

Selected examined material: BRAZIL. Amazonas: Barcelos, Rio Aracá, 28 July 1985 (fr), J.A. Silva 374 (INPA, K, LTR, MG, NY); São Gabriel da Cachoeira, Rio Cubaté, afluente do Içana, 02 Nov. 1987 (fl), C. Farney et al. 1874 (FLAS, INPA, MG, NY, RB). Roraima: Caracaraí, rio Xeriuni, Apr.1974 (fl), J.M. Pires et al. 14025 (IAN, INPA, LTR, MG, RB).

Habitat, distribution and conservation status. Terminalia virens is restricted to northwestern South America, specifically to Brazil, Colombia and Venezuela (Stace, 2010). In Brazil, it occurs only in the North region (Amazonas and Roraima). It is present in Ombrophyllous and Várzea Forests vegetation, associated with the river courses of the region, such as Rio Negro and its tributaries, similar to T. ramatuellea. From a conservation perspective, T. virens was designated as vulnerable (VU) due to its EOO of 12,708,813 km2 and endangered (EN) due to its AOO of 12,000 km2 (Table I). Based on the records, it was not possible to verify this taxon in protected areas in the Amazon.

Vernacular names: None registered.

11. Terminalia yapacana Maguire Mem. New York Bot. Gard. 8: 132. 1953. TYPE: Venezuela. Amazonas: Yapacana Savanna III, Cerro Yapacana, Alto Rio Orinoco, 125 m, 1 Jan. 1951, (fr), Maguire et al. 30590 (holotype, NY-00245985!; isotypes: BM not seen, IAN [barcode] 72731!, RB-00537416!, US-00117627!, VEN [barcode] 31340!) (Figure 3i).

Terminalia yapacana is related to T. quintalata, and is characterized and distinguished by its 3−5.7 × 1.4−3.1 cm, narrow-obovate to oblanceolate leaves (vs. 8−14.1 × 5.8−7.6 cm, obovate to oblong-obovate leaves) and fruits with rounded wings (vs. fruits with narrow-elliptic wings).

Selected examined material: BRAZIL. Amazonas: Barcelos, Rio Aracá, igapó, 18 Aug. 2014 (fl), C.E. Zartman 9587 (INPA).

Additional examined material: VENEZUELA. Amazonas: Atabapo, E of Caño Perro de Agua confluence, 30 Nov. 1978 (fr), O. Huber & S. Tillett 2788 (INPA, LTR, MYF).

Habitat, distribution and conservation status: Terminalia yapacana, until now, was restricted to Venezuela (Stace, 2010). However, through the present study, the species’ distribution expanded to Brazil, including a new registry in Amazonas state. The confirmation of T. yapacana was possible after observing a set of diagnostic characters, such as smaller and narrow-obovate to oblong-oblanceolate leaves and relatively shorter inflorescences, when compared to T. quintalata (related species). T. yapacana is present in Igapó, Amazonian forest vegetation, and is associated with the river course of the region. Regarding conservation, the taxon was designated as critically endangered (CR) due to its EOO of 0,000 km2 and critically endangered (CR) due to its AOO of 4,000 km2 (Table I). The species was not registered in protected areas in the Brazilian Amazon.

Vernacular names: None registered.

DISCUSSION

Terminalia s.s. is considered a complex group from a morphological point of view, as well as presents wide plasticity of its morphological features (Marquete et al. 2003MARQUETE NFS, TEIXEIRA J & VALENTE MC. 2003. Terminalia L. (Combretaceae) na região Sudeste do Brasil. Bradea 16: 99-123., Ribeiro et al. 2018RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257.).

According to Ribeiro et al. (2018)RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257., the concept of Terminalia taxa is commonly based on morphological aspects of inflorescences and fruits. Further detailing of vegetative and reproductive structures allows us to differentiate taxa related through unused characters, such as leaf and style indument, thus facilitating the process of recognizing group taxa, either in the field or based on sterile or fertile specimens.

The taxa of Terminalia s.s. registered in the Brazilian Amazon have different global distribution patterns, whether or not they are restricted to South America. Some taxa are widely distributed in South America, such as T. amazonia, T. argentea, T. dichotoma, T. glabrescens and T. lucida, while others are more restricted to the Amazon region, i.e., T. quintalata, T. ramatuella, T. yapacana and T. virens (Stace 2010STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p.).

Furthermore, the diversity of vegetation formations in which Terminalia species were recorded indicate that they have high ecological versatility, as they are present both in humid environments such as the Ombrophyllous Forest, as well as drier areas such as the Amazonian Savanna. In the Amazon, we highlight the savanna regions with significant area reduction, mainly due to deforestation (Carvalho & Mustin 2017CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahs. Nat Ecol Evol 1(4): 100., Gomes et al. 2019GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.).

The distribution patterns of taxa (Figure 1a) reflected the concentration of records in some regions of the Amazon and the absence of occurrences in others, which are mainly associated with easier or more difficult access. According to Borges et al. (2012)BORGES R, MORAES MA, MONTEIRO NP, BEVACQUA AM & MARTINELLI G & MARQUETE NFS. 2012. Available data and risk assessment of the Brazilian threatened species of Combretaceae. Rodriguésia 63: 31-38., the existence of underexploited areas hinders studies about distribution and conservation assessment for these taxa in the Amazon.

The richness and diversity areas were concentrated in three centers in the northern portion of the Amazon region, in Dense Ombrophyllous Forest and Amazonian Campinarana Forest vegetation. Therefore, these centers are associated with vegetations that exclusively (Pachyphylla and Ramatuellea sections) or largely (Chuncoa, Oblongae and Rhombocarpae sections) represent the occurrence records of the taxa of these sections of Terminalia s.s.

In addition, these richness centers of Terminalia s.s. in the Amazon are concentrated in the northern portion of the region, coinciding with the areas of refuge provided by the “refuge theory” proposed by Haffer (1969)HAFFER J. 1969. Speciation in Amazonian forest birds. Science 165: 131-137.. As proposed by this theory, some species occurring in the Amazon remained more restricted to refuge areas, e.g., T. crispialata, T. quintalata, T. ramatuella, T. virens and T. yapacana; while others, such as T. amazonia, T. glabrescens and T. oblonga also occurred in refuges in the Atlantic Forest domain (Andrade-Lima 1966ANDRADE-LIMA D. 1966. Contribuição ao estudo do paralelismo da flora amazônico nordestina. Bragantia 19: 1-30., Haffer & Prance 2002HAFFER J & PRANCE GT. 2002. Impulsos climáticos da evolução na Amazônia durante o Cenozoico: sobre a teoria dos Refúgios da diferenciação biótica. Estud Av 16: 175-206., Ribeiro et al. 2018RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257.).

The patterns of richness and diversity of Terminalia s.s. in the Amazon reinforce the need for field expeditions in different areas, especially in the central region, which would provide more records and new species citations for this area, in addition to the four new occurrences reported here. According to Versieux et al. (2017)VERSIEUX LM ET AL. 2017. Integrative research identifies 71 new plant species records in the state of Rio Grande do Norte (Brazil) and enhances a small herbarium collection during a funding shortage. PhytoKeys 86: 43-74., the increased number of collections in underexploited areas may reveal new occurrences for widely distributed taxa, especially for the more restricted ones. In addition to taxonomic listings, such as those by Steege et al. (2016)STEEGE H ET AL. 2016. The discovery of the Amazonian tree flora with an updated checklist of all known tree taxa. Sci Rep 6(1): epub29549. and Cardoso et al. (2017)CARDOSO D ET AL. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA 114: 10695-10700., studies such as the one presented here may provide information for recognizing and understanding distribution patterns and areas of greater richness and diversity for Amazonian tree taxa in particular.

Protected areas (PA) (municipal, state or federal levels) in which taxa have been registered, in addition to indigenous lands, represent important regions for the preservation of natural populations of Terminalia in the Brazilian Amazon.

Among the studied taxa, T. oblonga presented the largest number of records, being found in four different PA. The presence in PA indicates a lower threat of species disappearance, especially for those considered endangered (Hoffmann et al. 2018HOFFMANN S, BEIERKUHNLEIN C, FIELD R, PROVENZALE A & CHIARUCCI A. 2018. Uniqueness of protected areas for conservation strategies in the European Union. Sci Rep 8: 6445., Herrera et al. 2019HERRERA D, PFAFF A & ROBALINO J. 2019. Impacts of protected areas vary with the level of government: Comparing avoided deforestation across agencies in the Brazilian Amazon. Proc Natl Acad Sci USA 116(30): 14916-14925.).

Terminalia crispialata, T. quintalata, T. ramatuellea, T. virens and T. yapacana were not recorded in PA in the Amazon. In addition, they had lower EOO and AOO. Steege et al. (2015)STEEGE H ET AL. 2015. Estimating the global conservation status of more than 15,000 Amazonian tree species. Sci Adv 1: e1500936. produced estimates for population sizes, deforestation projections and conservation status for more than 15,000 Amazonian trees, indicating reductions in populations by 2050 projections for T. yapacana, as well as T. amazonia, T. argentea, T. crispialata, T. dichotoma, T. glabrescens, T. lucida and T. oblonga. These authors also categorized T. argentea and T. glabrescens as vulnerable (VU), according to IUCN criteria.

Furthermore, Barber et al. (2014)BARBER CP, COCHRANE MA, SOUZA CM & LAURANCE WF. 2014. Roads, deforestation, and the mitigating effect of protected areas in the Amazon. Biol Conserv 177 203-209. and Steege et al. (2015)STEEGE H ET AL. 2015. Estimating the global conservation status of more than 15,000 Amazonian tree species. Sci Adv 1: e1500936. highlight those protected areas and existing indigenous territories in the Amazon help protect viable populations, especially more endangered species, highlighting the importance of avoiding deforestation in these areas, as well as of improving their governance.

Unfortunately, recent data about deforestation in protected areas and indigenous land does not allow us to conclude that populations of Amazonian tree species, including Terminalia s.s., will not suffer significant reductions or even disappear in the region (Freitas et al. 2018FREITAS FLM, SPAROVEK G, BERNDES G, PERSSON UM, ENGLUND O, BARRETTO A & MÖRTBERG U. 2018. Potential increase of legal deforestation in Brazilian Amazon after Forest Act revision. Nat Sustain 1: 665-670., Gomes et al. 2019GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.).

Listings of tree species from the Amazon emphasize the need to identify the taxa from the region. However, these studies should conduct taxonomic treatments, such as the one presented here, including information about habitat, diagnostic characters and patterns of distribution and richness to aid the conservation actions of Amazonian inventoried tree taxa.

ACKNOWLEDGMENTS

The authors would like to thank the Programa de Pós-Graduação em Biodiversidade (Universidade Federal Rural de Pernambuco - UFRPE) for technical and academic support. Rayane de Tasso Moreira Ribeiro thanks the Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco - FACEPE for the postdoctoral scholarship granted (Process BFP-0160-2.03/20). Maria Iracema Bezerra Loiola (Process 308685/2020-2) and Margareth Ferreira de Sales thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for the research productivity scholarship. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Finance Code 001.

REFERENCES

  • ANDRADE-LIMA D. 1966. Contribuição ao estudo do paralelismo da flora amazônico nordestina. Bragantia 19: 1-30.
  • ANTONELLI A, ZIZKA A, CARVALHO FA, SCHARN R, BACON CD, SILVESTRO D & CONDAMINE FL. 2018. Amazonia is the primary source of Neotropical biodiversity. Proc Natl Acad Sci USA 115: 6034-6039.
  • BACHMAN S, MOAT J, HILL AW, TORRE J & SCOTT B. 2011. Supporting red list threat assessments with GeoCAT: Geospatial conservation assessment tool. ZooKeys 150: 117-126.
  • BARBER CP, COCHRANE MA, SOUZA CM & LAURANCE WF. 2014. Roads, deforestation, and the mitigating effect of protected areas in the Amazon. Biol Conserv 177 203-209.
  • BIODIVERSITY HERITAGE LIBRARY. 2021. The Biodiversity Heritage Library. Available at <https://www.biodiversitylibrary.org/>. Access on 1 January 2021.
    » https://www.biodiversitylibrary.org/
  • BORGES R, MORAES MA, MONTEIRO NP, BEVACQUA AM & MARTINELLI G & MARQUETE NFS. 2012. Available data and risk assessment of the Brazilian threatened species of Combretaceae. Rodriguésia 63: 31-38.
  • CARDOSO D ET AL. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA 114: 10695-10700.
  • CARVALHO WD & MUSTIN K. 2017. The highly threatened and little-known Amazonian savannahs. Nat Ecol Evol 1(4): 100.
  • CNCFlora. 2021. Centro Nacional de Conservação da Flora. Available at <http://www.cncflora.jbrj.gov.br/portal>. Access on 28 January 2021.
    » http://www.cncflora.jbrj.gov.br/portal
  • CRIA. 2021. speciesLink. Available at <http://www.splink.org.br/>. Access on 17 January 2021.
    » http://www.splink.org.br/
  • EVA HD & HUBER O. 2005. A proposal for defining the geographical boundaries of Amazônia. In: EXPERT CONSULTATION WORKSHOP, Ispra, European Commission in collaboration with the Amazon Cooperation Treaty Organization.
  • FINE PVA, MESONES I & COLEY PD. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305: 663-665.
  • FREITAS FLM, SPAROVEK G, BERNDES G, PERSSON UM, ENGLUND O, BARRETTO A & MÖRTBERG U. 2018. Potential increase of legal deforestation in Brazilian Amazon after Forest Act revision. Nat Sustain 1: 665-670.
  • GOMES VHF, VIEIRA ICG, SALOMÃO RP & STEEGE H. 2019. Amazonian tree species threatened by deforestation and climate change. Nat Clim Change 9: 547-553.
  • HAFFER J & PRANCE GT. 2002. Impulsos climáticos da evolução na Amazônia durante o Cenozoico: sobre a teoria dos Refúgios da diferenciação biótica. Estud Av 16: 175-206.
  • HAFFER J. 1969. Speciation in Amazonian forest birds. Science 165: 131-137.
  • HERRERA D, PFAFF A & ROBALINO J. 2019. Impacts of protected areas vary with the level of government: Comparing avoided deforestation across agencies in the Brazilian Amazon. Proc Natl Acad Sci USA 116(30): 14916-14925.
  • HICKEY LJ. 1973. Classification of the architecture of dicotyledonous leaves. Am J Bot 60: 17-33.
  • HIJMANS RJM, CRUZ E, ROJAS E & GUARINO L. 2001. DIVA-GIS. A geographic information system for the management and analysis of genetic resources data, Peru: International Potato Center and International Plant Genetic Resources Institute, 40 p.
  • HOFFMANN S, BEIERKUHNLEIN C, FIELD R, PROVENZALE A & CHIARUCCI A. 2018. Uniqueness of protected areas for conservation strategies in the European Union. Sci Rep 8: 6445.
  • HOORN C ET AL. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931.
  • IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATISTICA. 2021. Regional maps. Available at <https://www.ibge.gov.br/en/geosciences/maps/regional-maps/17927-legal-amazon.html?edicao=17929&t=sobre>. Access on 28 January 2021.
    » https://www.ibge.gov.br/en/geosciences/maps/regional-maps/17927-legal-amazon.html?edicao=17929&t=sobre
  • INPE - INSTITUTO NACIONAL DE PESQUISAS ESPACIAIS. 2021. AmBData Varíaveis para modelagem de distribuição de espécies. Available at http://www.dpi.inpe.br/Ambdata/English/vegetation.php Access on 28 January 2021.
    » http://www.dpi.inpe.br/Ambdata/English/vegetation.php
  • IUCN - INTERNATIONAL UNION FOR CONSERVATION OF NATURE. 2017. Guidelines for using the IUCN Red List Categories and criteria, Version 13. Available at <http://www.iucnredlist.org/documents/RedListGuidelines.pdf>. Access on 19 January 2021.
    » http://www.iucnredlist.org/documents/RedListGuidelines.pdf
  • IUCN - INTERNATIONAL UNION FOR CONSERVATION OF NATURE. 2021. The IUCN red list of threatened species. Available at <https://www.iucnredlist.org/>. Access on 19 January 2021.
    » https://www.iucnredlist.org/
  • JSTOR. 2021. Global Plants on JSTOR. Available at <https://plants.jstor.org/>. Access on 28 January 2021.
    » https://plants.jstor.org/
  • LINSIGEN LV, CERVI AC & GUIMARÃES O. 2009. Sinopse taxonômica da família Combretaceae R. Brown na Região Sul do Brasil. Acta Bot Bras 23: 738-750.
  • LOIOLA MIB ET AL. 2013. Combretaceae. In: MARTINELLI G & MORAES MA. Livro vermelho da flora do Brasil, Rio de Janeiro: Andrea Jakobsson - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, 1100 p.
  • MARQUETE NFS & VALENTE MC. 1996. Combretaceae. In: COLEÇÃO RIZZO, Flora dos Estados de Goiás e Tocantins, Brasília, p. 1-59.
  • MARQUETE NFS & VALENTE MC. 2005. Flora da Reserva Ducke, Amazonas, Brasil: Combretaceae. Rodriguésia 56(86): 131-140.
  • MARQUETE NFS, TEIXEIRA J & VALENTE MC. 2003. Terminalia L. (Combretaceae) na região Sudeste do Brasil. Bradea 16: 99-123.
  • MAURIN O, GERE J, VAN DER BANK M & BOATWRIGHT JG. 2017. The inclusion of Anogeissus, Buchenavia and Pteleopsis in Terminalia (Combretaceae: Terminaliinae). Bot J Linn Soc 184: 312-325.
  • MAYORAL C, VAN BREUGEL M, CEREZO A & HALL JS. 2017. Survival and growth of five neotropical timber species in monocultures and mixtures. Forest Ecol Manag 403: 1-11.
  • MMA – MINISTÉRIO DO MEIO AMBIENTE, 2021. Download de dados geográficos. Available at <http://mapas.mma.gov.br/i3geo/datadownload.htm>. Access on 28 January 2021.
    » http://mapas.mma.gov.br/i3geo/datadownload.htm
  • POWO – PLANTS OF THE WORLD ONLINE. 2021 Plants of the World Online. Royal Botanic Gardens. Available at http://www.plantsoftheworldonline.org. Acess on 24 January 2021.
    » http://www.plantsoftheworldonline.org.
  • PRAIA T DE S. 2017. Flora das cangas da Serra dos Carajás, Pará, Brasil: Combretaceae. Rodriguésia 68: 945-946.
  • QGIS. 2021. QGIS Geographic Information System. Open Source Geospatial Foundation. Available at http://qgis.osgeo.org Access on 28 January 2021.
    » http://qgis.osgeo.org
  • RADFORD AE, DICKSON WC, MASSEY JR & BELL CR. 1974. Vascular plant systematics. New York: Harper and Row, 891 p.
  • REFLORA - REFLORA VIRTUAL HERBARIUM. 2021. Reflora Virtual Herbarium. Available at http://reflora.jbrj.gov.br/reflora/herbarioVirtual Access on 17 January 2021.
    » http://reflora.jbrj.gov.br/reflora/herbarioVirtual
  • RIBEIRO RTM, GOMES FM, CORDEIRO LSC, LOIOLA MIB & SALES MF. 2020. Terminalia nildae (Combretaceae): A New Tree Species from the Brazilian Atlantic Forest. Syst Bot 45(2): 268-273.
  • RIBEIRO RTM, LINSINGEN LV, CERVI AC, MARQUETE NFS, LOIOLA MIB & SALES MF. 2018. New Synonyms and Recircumscription of Terminalia sect. Diptera (Combretaceae) from South America. Syst Bot 43(1): 250-257.
  • RIBEIRO RTM, LOIOLA MIB & SALES MF. 2017. Flora do Espírito Santo: Subtribo Terminaliinae (Combretaceae). Rodriguésia 68: 1547-1557.
  • RIBEIRO RTM, MARQUETE N & LOIOLA MIB. 2020. Combretaceae in Flora do Brasil 2020 em construção. 2020. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB6913>. Access on 18 February 2021.
    » http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB6913
  • RIBEIRO RTM, REBOUÇAS NC, LOIOLA MIB & SALES MF. 2020. Terminalia s.s. (Combretaceae) in Maranhão state, Brazil. Rodriguésia 71: e00942019.
  • SOARES NETO RL, CORDEIRO LS & LOIOLA MIB. 2014. Flora do Ceará, Brasil: Combretaceae. Rodriguésia 65: 685-700.
  • SOUSA VF, RIBEIRO RTM, LOIOLA MIB & VERSIEUX LM. 2018. Combretaceae no estado do Rio Grande do Norte, Brasil. Rodriguésia 69(4): 1771-1787.
  • STACE CA. 1965. The significance of the leaf epidermis in the taxonomy of the Combretaceae. A general review of tribal, generic and specific characters. Bot J Linn Soc 59: 229-252.
  • STACE CA. 2010. Combretaceae. Flora Neotropica 107. New York: The New York Botanical Garden Press, 369 p.
  • STEEGE H, PITMAN N, SABATIER D, CASTELLANOS H, VAN DER HOUT P, DALY DC & SILVEIRA M ET AL. 2003. A spatial model of tree α-diversity and tree density for the Amazon. Biodivers Conserv 12: 2255-2277.
  • STEEGE H ET AL. 2015. Estimating the global conservation status of more than 15,000 Amazonian tree species. Sci Adv 1: e1500936.
  • STEEGE H ET AL. 2016. The discovery of the Amazonian tree flora with an updated checklist of all known tree taxa. Sci Rep 6(1): epub29549.
  • THIERS B. 2021 [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at http://sweetgum.nybg.org/science/ih Access 28 January 2021.
    » http://sweetgum.nybg.org/science/ih
  • VERSIEUX LM ET AL. 2017. Integrative research identifies 71 new plant species records in the state of Rio Grande do Norte (Brazil) and enhances a small herbarium collection during a funding shortage. PhytoKeys 86: 43-74.

Publication Dates

  • Publication in this collection
    09 Sept 2022
  • Date of issue
    2022

History

  • Received
    19 Feb 2021
  • Accepted
    17 June 2021
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100 - Rio de Janeiro - RJ - Brazil
E-mail: aabc@abc.org.br