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

: 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, identifi cation 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 identifi cation of these tree species, in addition to actions to conserve trees in the Brazilian Amazon.


INTRODUCTION
The Amazon is the most diverse rainforest in the world, standing out for its large number of species (Cardoso et al. 2017, Antonelli et al. 2018).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 interspecifi c interactions (Fine et al. 2004, Eva & Huber 2005, Hoorn et al. 2010, Antonelli et al. 2018).
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. 2019).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 defi ne areas of interest for taxa conservation, such as those developed by Cardoso et al. (2017) and Gomes et al. (2019) 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. 2020).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 1965, 2010, POWO 2021).It is represented by trees with simple and alternate leaves, usually clustered at the apex of the branches, bisexual or unisexual fl owers, apetals and fruits betulids, actinomorphic or zygomorphic.The group presents high vegetative and reproductive morphological diversity, making it diffi cult to recognize the taxa (Stace 2010, Ribeiro et al. 2018).
In Brazil, the genus comprises 22 species, of which seven are endemic, belonging to nine sections (Stace 2010).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. 2020).
Regarding taxonomic treatments of the group, the study by Stace (2010), 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.
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 2005).Recently, one species of Combretum (Combretum laxum Jacq.) was recorded in the Serra dos Carajás, State of Pará (Praia 2017).
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 2010, Mayoral et al. 2017).
Studies about the conservation status of Terminalia taxa are still punctual and include few species, especially those developed by Borges et al. (2012) who evaluated four species (Terminalia acuminata (Allemão) Eichler, T. argentea Mart.& Zucc., T. mameluco Pickel and T. triflora (Griseb.)Lillo), Loiola et al. (2013), including only T. acuminata, and the National Center for Plant Conservation (CNC Flora 2021) and IUCN Red List of Threatened Species (IUCN 2021) list five and eight species, respectively.
From a phylogenetic perspective, Maurin et al. (2017) 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) and Ribeiro et al. (2018), 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 2017) and definition of species registered in Protected Areas (PA) and their respective PA.
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. 2003, Herrera et al. 2019, IBGE 2021).
According to Cardoso et al. (2017), 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 2021) and National Institute for Space Research (INPE 2021) 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 2021).The standardization of vegetative and reproductive structural terminology was based on Stace (1965), Hickey (1973) andRadford et al. (1974).Species determination was based mainly on Stace (2010) and data from the Brazilian Flora 2020 project (Ribeiro et al. 2020).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) and the Biodiversity Heritage Library (2021) 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

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 2010), speciesLink system of the Reference Center on Environmental Information -CRIA (CRIA 2021), the Reflora Virtual Herbarium (REFLORA 2021) 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. 2001).All the maps presented here were generated through the Quantum GIS 3.8 software (QGIS 2021).

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. 2011).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).

RESULTS
Taxonomic and morphological aspects of Terminalia s.s.
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).Bras Cienc (2022) 94(4) e20210265 6 | 19 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 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.4) in different units (Table I).
The species with the highest EOO was T. amazonia (2,511,901,232 km 2 ) and the smallest were T. ramatuella and T. yapacana (0,000 km 2 ), whose species were represented by few collections.T. dichotoma stands out with the largest AOO area (92,000 km 2 ), while T. yapacana presented the smallest (4,000 km 2 ).More detailed information can be found in species comments and in Table I.
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) 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. 2020).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 km 2 and endangered (EN) due to its AOO of 68,000 km 2 (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).
Notes: Terminalia amazonia, both in the original work and in the revision by Stace (2010), 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).
Terminalia argentea is distinguished by its narrow-elliptic, elliptic to ovate leaves with acuminate apex, dense-sericeous indument on adaxial surface when young, eucamptodromousbrochidodromous 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) 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  (2022) 94(4) e20210265 10 | 19 (Central-West, North, Northeast, Southeast and South) (Ribeiro et al. 2020).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 km 2 and endangered (EN) due to its AOO of 24,000 km 2 (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).
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. 2020).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 km 2 and endangered (EN) due to its AOO of 28,000 km 2 (Table I).The species has not yet been registered in protected areas in the Amazon (Table I).
Selected examined material: BRAZIL.Acre: Rio Juruá, 1 km upstream from Colônia Rodriguez Alvez, Oct. 1986, (fr) 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 and in sandy environments, such as Coastal Forest.The species has been defi ned here as least concern (LC) due to its EOO of 1,071,85,167 km 2 and endangered (EN) due to its AOO of 80,000 km 2 (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).Terminalia oblonga is distinguished from the other species by elliptic-oblong, oblong to obovate-oblong leaves, acute to short-acuminate apex, attenuate base, elongated infl orescence, style dense-villous from the proximal half to the apex and fruits 2-winged with wings rounded or subtriangular, coriaceous.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 km 2 and endangered (EN) due to its AOO of 64,000 km 2 (Table I).The taxon occurs in protected areas and indigenous lands in the Amazon, among which includes the Raimundo Irineu Serra APA.
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) 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. 2020).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 km 2 and as endangered (EN) due to its AOO of 12,000 km 2 (Table I).Based on the records, it was not possible to verify this taxon in protected areas in the Amazon.
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 cinereoussericeous 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.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 km 2 and critically endangered (CR) due to its AOO of 4,000 km 2 (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. 2003, Ribeiro et al. 2018).
According to Ribeiro et al. ( 2018), 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 2010).
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 2017, Gomes et al. 2019).
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), 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).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 1966, Haffer & Prance 2002, Ribeiro et al. 2018).
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), 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) and Cardoso et al. (2017), 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. 2018, Herrera et al. 2019).
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) 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) and Steege et al. (2015) 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. 2018, Gomes et al. 2019).
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.
RAYANE T. M. RIBEIRO, MARIA I.B.LOIOLA & MARGARETH F. DE SALES Terminalia s.s.IN THE BRAZILIAN AMAZON An Acad Bras Cienc