The genera Bernardia Houst. ex Mill. and Tragia L. (Euphorbiaceae, Acalyphoideae) in Northeastern Brazil

: Bernardia and Tragia are genera of the subfamily Acalyphoideae, with species occurring in tropical and subtropical regions. Studies concerning those genera are scarce in Brazil, including Northeastern Brazil. The present study was designed to study the taxonomy of species occurring there, and provides illustrations, keys, descriptions, and comments concerning taxonomic affinities, as well as information concerning their geographic distributions and environmental preferences. A total of 13 species were encountered, eight of Bernardia and five of Tragia . Of those, B. hamadryadica and T. cearensis are endemic to Northeastern Brazil and B. celastrinea , B. pulchella , and T. chlorocaulon are new records for the region. The two genera occur in moist Atlantic forests, in forest borders, and anthropically impacted areas. New occurrences were recorded in all of the states, totaling 21 new records. The principal diagnostic characters for distinguish were: the sexuality of the plant (monoecious or dioecious), the presence of foliar glands, the types of inflorescence and trichomes, and the numbers of stamens. Among the 13 species encountered, six are illustrated here for the first time.

Acalyphoideae is the largest and most complex subfamily of Euphorbiaceae, comprising 99 genera and 3,000 species (Webster 2014). It is separated from the other subfamilies by the absence of milky latex; laticifers usually absent, or if present, non-articulate; and pollen grains binucleate, but other characteristics are also useful. The absence of petals on the staminate and pistillate flowers is common; only a few taxa (e.g., Chrozophora Necker ex A. Juss. and Ditaxis Vahl ex A. Juss.) have petals at least in staminate flowers. Most seeds do not have a caruncle, and the pollen does not show the Croton pattern of sexine ornamentation: tectate with triangular processes frequently forming continuous arrays (Webster 2014, Gillespie & Ambruster 1997. Bernardia Houst. ex Mill. and Tragia L. are among the most diverse genera, with 68 and ca. 150 species, respectively (Cardinal-McTeague & Gillespie 2016, Govaerts et al. 2000. Bernardia is the largest genus of tribe Bernardieae Webster and it has a neotropical distribution, with Brazil and Mexico being the main centers of diversity (Webster 1994, Govaerts et al. 2000, Cervantes et al. 2009). Pax & Hoffmann (1914) (Carrión 2018).
In spite of the great richness and morphological diversity of the species of Euphorbiaceae in Brazil, studies of the genera Bernardia and Tragia have been very rare there. The treatment of Euphorbiaceae published by Müller Argoviensis (1874) in the Flora brasiliensis comprised 16 species of Bernardia and 22 of Tragia. There are records of species of both genera in floristic surveys undertaken in the Serra do Cipó in Minas Gerais State (Cordeiro 1992), areas of inselbergs in Milagres (Carneiro et al. 2002), sandy caatingas both in Bahia State (Sátiro & Roque 2008), and in caatinga vegetation in Porto Folha, Sergipe State (Oliveira 2013 Despite recent progress, there has been little research on those two genera in Northeastern Brazil, and few collections are encountered in regional herbaria, moreover there is a lack of taxonomists specialized in these groups, consequently many specimens remain unidentified or misidentified in herbaria. In that context, the present work examined the taxonomy of the species of Bernardia and Tragia occurring in Northeastern Brazil to contribute to a better understanding of those genera, provide keys, morphological descriptions, illustrations, and data concerning their geographic distributions and preferred habitats, to amplify our knowledge of that region's vegetation and to serve as a basis for future taxonomic revisions.

Study area
Northeastern Brazil is the third largest geographic area in Brazil, covering approximately 1,540,827 km 2 (Schneeberger & Farago 2003). The vegetation there is predominantly caatinga (fully deciduous, thorny, xeric vegetation) but, depending on the landscape and elevation, significant areas of forests (ombrophilous and seasonal), savannas (cerrado), campos rupestres, dunes, and mangrove swamps are also present (Barbosa et al. 2006).
Northeastern Brazil is known for its hot, sunny weather, with mean temperatures between 20º and 28ºC. It is divided into four sub-regions: the Mid-North, which corresponds to the transition between the Amazon region and the dry sertão (also known as the Mata do Cocais); the sertão itself, where the climate is semiarid and the vegetation is caatinga; the agreste, which corresponds to the transition between the sertão and the forest zone; and the forest zone, characterized by abundant rainfall (Vieira et al. 2008).

Taxonomic study
The present study was based on field collections made between April/2016 and December/2017, concentrated principally in the states of Bahia, Paraíba, Pernambuco, and Sergipe (where the largest numbers of species have been recorded). We also examined approximately 1,000 specimens of Bernardia and Tragia deposited in the principal herbaria in the northeastern region (ALCB, CEPEC, EAC, , HRB, HUEFS, HUNEB, IAN, IPA, JPB, PEUFR, UFP, and HESBRA and HST of Federal Rural of Pernambuco), as well as in a herbarium in southeastern Brazil (RB); acronyms according to Thiers 2018 (continuously updated). Protologues of all of the species studied were consulted, as well as digitized specimens (especially of the type collections deposited in K [https://www.kew.org/]), NYBG (http://sweetgum.nybg.org/science/ vh/), P (http://www.mnhn.fr/fr/collections/ensembles-collections/ botanique), and other herbaria material available online on speciesLink (http://www.splink.org.br).
The species were identified using analytical keys from classic publications, regional floras, and taxonomic revisions (e.g., Pax & Hoffmann 1914, 1919, Múlgura & Sanguinetti 1989, Gillespie 1993, 1994a, Urtecho 1996, Gillespie & Armbruster 1997, or by comparisons with protologues and type collections. Standardization of the terminology for the vegetative and reproductive structures of the species was based on Harris & Harris (1994). Croizat (1943) was adopted for the shapes of the foliar basilaminar glands.
Information concerning the geographic distributions of the taxa were ascertained from the aforementioned sources, the site of the Flora do Brasil (http://www.floradobrasil.jbrj.gov.br), as well as observations of the species in the study area; data concerning flowering, fruiting, vegetation types, and soils were extracted from the herbarium specimen labels.
We opted not to treat infraspecific categories for Bernardia and Tragia because there are many gaps in the available information and ongoing discussions concerning their correct identifications and infraspecific classifications.

Results and Discussion
Thirteen species were recorded in the study area, eight of Bernardia and five of Tragia, representing 35% of the Brazilian species of Bernardia and 31% of Tragia. Among the species recorded, seven are endemic to Brazil (Bernardia axillaris, B. celastrinea (Baill.) Müll. Arg., B. gambosa, B. hamadryadica, B. scabra, B. tamanduana and T cearensis) and occur in almost all regions of the country. Bernardia hamadryadica and Tragia cearensis are endemic to Northeastern Brazil. The non-endemic species are found also in Argentina (T. bahiensis, T. volubilis), Bolivia (B. pulchella [Baill.] Müll. Arg., T. chlorocaulon Baill., T. friesii), and Mexico (B. sidoides). Tragia cuneata and B. major were cited for Northeastern Brazil in Flora do Brasil 2020, but these species were not found in the herbaria. Specimens previously identified as T. cuneata are in fact T. volubilis (e.g., Santos,T.S. 423) or other genera (e.g., Bia Klotzsch and Caperonia A.St.-Hil.). Bernardia celastrinea, B. pulchella, and T. chlorocaulon are cited here for the first time for that region, thereby increasing the number of species cited in Northeastern for Bernardia from seven to nine, and for Tragia from four to five. The genus Bernardia is most diverse in the state of Bahia (eight species) and Tragia is more numerous in the state of Ceará (five species). Tragia volubilis stands out as having the widest distribution, found in almost all states in Northeastern Brazil; Bernardia sidoides likewise occurs in almost all of those states, with the exception of Maranhão.
New records were encountered for almost all of the states in that region, with 21 new occurrences, such as: Bernardia axillaris for Paraíba; B. celastrinea and B. pulchella for Bahia; T. cearensis for Alagoas, Paraíba, Rio Grande do Norte and Sergipe; T. chlorocaulon for Maranhão; T. friesii for Alagoas, Bahia, Ceará, Sergipe and Paraíba; and T. volubilis for Alagoas, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, and Sergipe. New records were encountered principally in caatinga and atlantic forest vegetation, with some occurrences also in cerrado (T. bahiensis, T. chlorocaulon, and T. volubilis), on different types of soils (sandy, clayey, rocky), and in areas with granite or limestone outcrops, being most frequent in open areas such as forest edges and anthropogenically impacted environments at elevations between 22 and 1,010 m above sea level elevation.
The significant number of new records may be related to a previous lack of research on these two genera in Northeastern Brazil, the few collections encountered in regional herbarium and the lack of specialized taxonomists in this group. This shows the importance of this kind of research and the need for new studies in both genera.
The principal diagnostic characteristics of the taxa of Bernardia include their habit, the presence or absence of basilaminar glands (when present in different numbers and locations, with some species showing paired glands), phyllotaxy, and the type of the staminate inflorescence. Tragia species can be distinguished by their types of trichomes, the number of stamens, and the length of the pedicel of the fruit.

Key to the genera Bernardia and
It is very similar to B. scabra by its leave elliptic, with margin completely serrate. However, these species can be distinguished by the number of leaf glands (3-4 glands in B. axillaris vs. 9-12 in B. scabra). Additionally, the styles of B. axillaris are glabrescent while those of B. scabra are velutinous. The number of stamens can also distinguish these taxa (5-6 stamens in B. axillaris vs. 7-8 in B. scabra).
Bernardia celastrinea can be recognized by having staminate inflorescences in pseudoracemes, fruits up to 5 mm diam., and seeds light brown. Among the species found in Northeastern Brazil was possible to observe monoecious individuals of B. celastrinea and B. pulchella, but B. celastrinea has elliptic leaves, the margin completely serrate, and 3-5 unpaired glands, contrasting with B. pulchella which has leaves obovate, the margin serrate only on the distal half, and only two paired glands.
According to Carrión (2018), B. gambosa is endemic to Brazil and its occurrence has been confirmed for Bahia State, with a possible occurrence in Rio de Janeiro (Southeast region). The species is found in Atlantic Forest vegetation in areas of semi-deciduous seasonal and ombrophilous forests. In the study area, it has also been observed in areas of caatinga and areas of restinga vegetation on clayey soils at altitudes between 22 and 400 m elevation. Flowers and fruits were encountered most of the year.
It is morphologically similar to B. pulchella by the shape and margin of the leaves. However, B. hamadryadica has leaves up to 3.5 cm long and with three to five prominent basilaminar glands (vs. leaves up to 12.8 cm long and with two non-prominent basilaminar glands).

Bernardia scabra
According to Carrión (2018), B. scabra is known only from Northeastern Brazil, in Bahia State, with possible occurrence in Rio de Janeiro in Southeastern Brazil; it is common in areas of semi-deciduous seasonal and ombrophilous forests. It was also encountered in gallery forests, restinga, and humid forest sites on clayey soils, at elevations between 40 and 860 m elevation. Flowers were observed in October and fruits in December.
Bernardia sidoides occurs in Brazil, Costa Rica, Guatemala, Guyana, Mexico, Nicaragua, and Venezuela (Cervantes 2006). In Brazil, it has been recorded in the states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, and Sergipe in caatinga vegetation, seasonal deciduous forests, and also on rock outcrops (Carrión 2018). Flowers and fruits were recorded throughout the year.
This is the only species in the study area with verticillate leaves. It is also the only herbaceous monoecious plant with staminate and pistillate inflorescences in terminal.
Bernardia tamanduana is characterized as a dioecious shrub, ca. 4 m tall, with its inflorescences terminal, spicate. It is morphologically similar to B. gambosa; the two species are compared under the latter.

Key to the species of Tragia in Northeastern Brazil
This species occurs in Argentina, Bolivia, Brazil, and Paraguay (Múlgura 1991). In Brazil, it is known from the states of Bahia, Mato Grosso, Minas Gerais, Paraná, Rio Grande do Sul, and São Paulo, in the Caatinga and Cerrado domains and in areas of campo limpo (Flora do Brasil 2020 under construction). It grows in arboreal-shrub caatinga vegetation on sandy and rocky soils and on gray limestone outcrops between 60-1,000 m elevation. Individuals with flowers and fruits were collected from April to August.

Tragia friesii
Tragia friesii occurs in Bolivia and Brazil (Foster 1958, Múlgura & Sanguinetti 1989. In Brazil, it was only known from Pernambuco State, in the Caatinga domain (Múlgura & Sanguinetti 1989, Flora do Brasil 2020 under construction). It is recorded here for the first time in the states of the Alagoas, Bahia, Paraíba and Sergipe, were it was found growing in Atlantic Forest vegetation, along the edges and interiors of forests, as well as in anthropogenically modified environments on clayey and sandy soils at elevations from 250 to 1,086 m elevation. Flowers and fruits were encountered from January to July.
The species is characterized by having leaves with base cordate and apex acute, and pistillate flowers with pubescent styles. Tragia friesii can be confused with T. bahiensis since both share glandular trichomes and dark brown seeds. They can be distinguished by the bases and apices of their leaves and the distributions of the glandular trichomes: in T. bahiensis, the leaf base is subcordate and the apex attenuate, and glandular trichomes are restricted to the reproductive parts of the plant (vs. leaves with base cordate and apex acute, and glandular trichomes on all parts of the plant in T. friesii).