Nomenclatural and taxonomic updates in Rourea subgen. Rourea sect. Multifoliolatae (Connaraceae)

Abstract The pantropical genus Rourea Aubl. (Connaraceae) is composed of ca. 70 species, most of which occur in the Neotropics. Rourea is currently subdivided into three subgenera, with the American taxa included in Rourea subgen. Rourea. Forero (1976) recognised six sections for the species of the New World, with Rourea subgen. R. sect. Multifoliolatae being exclusive to Brazil, characterised by multifoliolate leaves, relatively small leaflets and the staminal tube (0.8–)1–1.5 mm long. Following Forero’s (1976) treatment, additional botanical collections have become available in Brazilian herbaria, allowing re-evaluation of species concepts. This work recognises and revises 12 species in this section, mainly restricted to southeastern Brazil and southern Bahia. A nomenclatural and taxonomic study of these species is here presented, including an identification key, morphological descriptions, illustrations and geographic distribution maps. A new species is also described.


Introduction
Rourea Aubl. is the second largest genus in Connaraceae and includes about 70 species (Lemmens 1989a), mainly from lowland tropical forests and savannahs of South America, Central Africa and Asia (Leenhouts 1958;Jongkind 1989;Lemmens 1989a). Its centre of species richness lies on the Neotropics, especially in the Amazon and Atlantic domains, comprising ca. 45 American species (Forero 1983). Rourea differs morphologically from other Connaraceae genera by the leaves usually 5 or more foliolate, petals epunctate, flowers 5-carpelate, fruits with calyx accrescent and seeds without endosperm (Forero 1983;Lemmens et al. 2004).
The most recent phylogenetic study and currently accepted classification of Connaraceae was an early cladistic study, based exclusively on morphological evidences (Lemmens 1989b). Four tribes were recognised in the family, with Rourea included in Cnestideae Planch., sister to a clade formed by the genera Cnestidium Planch. and Cnestis Juss.
The circumscription of Rourea has varied greatly since the publication of the genus by Aublet (1775). De Candolle (1825), for example, treated the genus as a synonym of Connarus L. Later, Planchon (1850) included Rourea within the tribe Connareae and described new genera and recognised others that are currently treated in synonymy of Rourea, such as Bernardinia Planch., Byrsocarpus Schumach. and Roureopsis Planch. Schellenberg (1938) was even more liberal: he followed Planchon's concepts and segregated additional taxa from Rourea, which resulted in the description of new generic names (e.g. Santaloides G. Schellenb). On the other hand, Baillon (1869) and Leenhouts (1958) adopted a broader concept for the genus and placed several genera -including some mentioned above -in Rourea, resulting in new synonymisations and combinations. Most of their contributions -although with minor changes -have been followed in modern taxonomic treatments (Forero 1983;Jongkind 1989;Lemmens et al. 2004).
This treatment includes the species belonging to Rourea subgen. Rourea sect. Multifoliolatae, which are restricted to Brazil and morphologically characterised by the leaves (3-)9-41-foliolate, leaflets usually oblong or narrowly elliptic and smaller than those found in other neotropical Rourea and flowers with staminal tubes (0.8-)1-1.5 mm long (Forero , 1983.
After  revisional work, new collections of R. subgen. Rourea sect. Multifoliolatae have been available in Brazilian herbaria thanks to modern field expeditions in the country. This has allowed identification of overlooked morphological characters and, thus, re-evaluation of species concepts in this group. It is also of note that many species of this section are very common in the Brazilian territory, although widely misidentified in herbarium collections. This study presents morphological descriptions of the referred taxa, an identification key, illustrations, geographic distribution maps and detailed taxonomic and nomenclatural notes, along with a new species.

Methods
The present study was primarily developed based on consultation of literature specific to the genus (Planchon 1850;Baker 1871;Schellenberg 1938;andForero 1976, 1983) and analysis of specimens from the following herbaria (acronyms according to Thiers 2020): ALCB, BHCB, BR, C, CEN, CEPEC, COL, CVRD, EAC, ESA, F, G, HUEFS, HUEG, HUFU, HUTO, IAN, K, M, MBM, MBML, MG, MO, MPU, NY, P, R, RB, S, SPF, UB, UEC, US, VIC, VIES and W. Fieldwork was carried out by the first author, which allowed collection of botanical samples, photographs and observation of species in their natural habitat. These expeditions took place in Brazil, comprising the municipalities of Conceição da Barra and Guarapari (Espírito Santo) and the district of Gama (Distrito Federal).
General morphological terms mainly follow Font Quer (1953) and Radford et al. (1974), while the venation pattern is based on Ellis et al. (2009) and inflorescence architecture on Weberling (1992).
Geographic distribution maps were prepared using ArcGIS 10.5 (ESRI 2016), based on the localities indicated on herbarium sheet labels. The lists of specimens examined follow alphabetical order by states, then by collectors.
Distribution, habitat and phenology. This species has only been found in Bahia and Espírito Santo (Fig. 3). In BA, populations of R. bahiensis are distributed in the southern portion of the state, occurring mainly in coastal areas from the municipality of Una to Porto Seguro and Alcobaça. In ES, specimens have been collected both in the interior of the state and coastal zones, ranging from northern to southern portions.  Individuals of Rourea bahiensis are lianas or scandent shrubs up to 7 m tall. This species occurs in the Atlantic Rain Forest, growing on "Tabuleiro" or swamp forests, although sometimes it is also found in degraded areas. Specimens have been collected with flowers from October to November and with fruits from September to January. Recognition and notes. Rourea bahiensis is morphologically similar to R. prostrata due to their narrowly elliptic or oblong leaflets usually measuring 0.9-2.2 × 0.5-1 cm. However, they are differentiated because R. bahiensis is a lianescent species without glandular trichomes, while R. prostrata is a prostrate subshrub with glandular trichomes. Rourea bahiensis can also be mistaken for R. discolor, from which it mainly differs by the smaller leaflets (1.1-2.2(-2.4) × 0.7-1 cm) and inflorescence rachis 0.3-1.7(-3.7) cm long vs. larger leaflets ((1.3-)2.2-4.5(-5.8) × (0.8-)1.2 × 1.7(-2.3) cm) and inflorescence rachis 3.5-11.8 cm long in R. discolor. Additionally, the petiole and leaf rachis are subglabrous to villous and the fruits are smaller (1.1-1.3 × 0.4-0.5 cm) in R. bahiensis, while, in R. discolor, the petiole and leaf rachis are glabrous and the fruits are larger (1.2-1.7 × 0.4-0.6 cm).
Distribution, habitat and phenology. This species is only known from the type location (Fig. 3). It has a shrubby habit and grows in areas of cerrado, at ca. 900 m altitude. The only flowering specimen was collected in November.
Distribution, habitat and phenology. Most of the known specimens of R. blanchetiana are old collections with no precise locations. The most recently analysed specimen was collected in the municipality of Nilo Peçanha, which is located in southern Bahia (Fig. 3). Therefore, it seems that R. blanchetiana is a rare species and most likely restricted to the south portion of Bahia. This is a lianescent species growing on ombrophilous forests of the Atlantic domain. The specimen J. S. Blanchet s. n. (NY barcode NY00393553) was collected with flowers and fruits in August. Recognition and notes. Rourea blanchetiana is easily recognised by the leaves with 27-39 leaflets, which are usually membranaceous, oblong and abaxially glaucous, aside from the flowers congested in the inflorescences, comparatively larger peduncle and petals 9-14 mm long. It is similar to R. discolor due to the leaflets abaxially glaucous and pedicel relatively long, but differs by the hirsute inflorescence rachis, elliptic flower buds and petals 9-14 mm long vs. glabrous or subglabrous inflorescence rachis, orbicular or ovate flower buds and petals (4-)6-8 mm long.
In the protologue of the basionym of Rourea blanchetiana from Flora Brasiliensis, the only specimen cited by Progel (1877) was Blanchet 1050, without indication of herbarium. Schellenberg (1938) inadvertently selected the lectotype from P. However, of the six specimens of R. blanchetiana, collected by Blanchet in P, none is annotated with number 1050. Specimens of Blanchet 1050 were found in BR, G, S and W and only the collection from G is fruiting, the rest, only flowering. Of these, the specimen from BR has an original label of "Herbarium Martii", identified as "Eichleria blanchetiana Prog. in Mart. fl. Br." and bears an attached pencil drawing containing floral details of the referred species. The characteristics of the branchlet of this specimen (number and shape of leaflets, inflorescence architecture and flower structures) and the detailed drawing match accurately with the illustration in Progel (1877, plate 116). In addition, considering that Progel worked in M and the original Flora Brasiliensis collection from M was sold to BR, then the specimen Blanchet 1050, deposited in the latter, seems the best candidate to be lectotype of R. blanchetiana, which is here proposed.
Distribution, habitat and phenology. Rourea chrysomalla is apparently restricted to Distrito Federal (DF), in the midwest region of Brazil (Fig. 5). The type specimen label indicates that the material was collected in Goiás state, but it is more likely to have been collected in DF (within the current boundaries of Goiás), which is supported by evidence from several sources. Firstly, the herbarium sheet label of Glaziou's specimen is from "Chemin du Rio Paranauá, a Chico Lobo"; although the name of this river has been taken as "Parananá", the penultimate letter more closely resembles a "U", than an "N". Secondly, Paranauá stands for Paranoá, a river course from DF, subject of study by Glaziou between 1894 and 1895. This can be confirmed by reports and letters from Glaziou to Missão Cruls (Cruls' mission), a large scientific expedition in the Brazilian Central Plateau, promoted to investigate the viability of transferring the capital of Brazil to the Midwest (available at: http://doc.brazilia.jor.br/HistDocs/Relatorios/1896-missao-Cruls-Glaziou-lago-Paranoa.shtml). Glaziou sent detailed reports on aspects of vegetation, soil quality and climate around the Paranoá River and clearly demonstrated his advice to dam its riverbed to set up an artificial lake, which was undertaken only in 1959. This lake is called Lago Paranoá and it was probably built following Glaziou's reports, suggesting that the botanist indeed collected in areas that are today part of DF. It is also of note that Glaziou's reports are contemporaneous with his collection of R. chrysomalla. Lastly, according to the description of his itinerary (Glaziou 1906), the author collected in Goiás from 1894 to 1895 and visited sites around and within what is now DF, indicating that his collections from Goiás also included specimens from DF. This evidence, in addition to the fact that R. chrysomalla is only found in DF, suggests that the type was collected in the present DF. Unfortunately, no information on "Chico Lobo" location was found.
In DF, individuals of R. chrysomalla can be found in the districts of Brasília, Gama, Riacho Fundo, Sobradinho and Taguatinga. This species is a subshrub up to 65(-80) cm tall, occurring in the central Brazilian Cerrado, more specifically in areas of cerrado s. s. or "campo sujo". Rourea chrysomalla is apparently the only species of the genus in which the roots develop a xylopodium. Specimens have been collected with flowers from August to October and in April and with fruits from September to October.  Recognition and notes. Rourea chrysomalla is easily distinguished by the combination of the following characters: branchlets velutinous, leaflets sessile, coriaceous, abaxially densely hirsute, sepals coriaceous, petals with glandular trichomes and fruits with outer surface completely velutinous. This species can be confused with R. prostrata due to their sub-shrubby habit; however, R. chrysomalla is an erect subshrub (vs. prostrate subshrub), has coriaceous leaflets (vs. chartaceous), inflorescences usually terminal (vs. axillary) and fruits measuring 1-1.4 × 0.4-0.6 cm, completely velutinous externally (vs. fruits 0.8-1 × 0.3-0.4 cm, sparsely hirsute especially at apex). Rourea chrysomalla is also similar to R. glazioui, but differs by the subshrubby habit, coriaceous leaflets and petals and stamens with glandular trichomes vs. lianescent habit, chartaceous leaflets and petals and stamens eglandular.

Rourea cnestidifolia
Distribution, habitat and phenology. There are only few records of this species, which seems to be restricted to central and northeastern Minas Gerais (Fig. 6). This shrubby species occurs in the Atlantic Forest or at the transition with the Cerrado, where it is distributed in areas of "Cerradão" and seasonal forests; it grows in rocky or limestone outcrops, at approximately 600-1,000 m altitude. Specimens have been collected with flowers from August to November and with fruits from October to December. Recognition and notes. Rourea cnestidifolia is recognised by the presence of glandular trichomes, relatively large middle and apical leaflets (4-7.2 × 1.6-3.2 cm), obtuse, acute or narrowly-rounded leaflet apex, a long peduncle (2.8-8 cm long) and a short pedicel (3-5 mm long).
The morphological limits separating Rourea cnestidifolia and R. glazioui present slight discontinuities, but these, along with distribution patterns, are sufficient to distinguish them. They are similar in the presence of glandular trichomes on petiole, leaf rachis and inflorescences, leaflet size and shape and in overall characteristics of flowers and fruits. Schellenberg (1938) separated them based on pedicel length, while Forero ( , 1983) used number of leaflets. These are useful distinctions despite some overlapping characters, so this revision considers that R. cnestidifolia differs from R. glazioui by the leaves 9-13-foliolate (Fig. 1D), peduncle 2.8-8 cm long, flowers congested in the inflorescence apex and pedicel 3-5 mm long vs. leaves 13-27-foliolate (Fig. 10), peduncle 0.2-1.7 cm long, flowers loosely disposed in the inflorescences and pedicel 5-10(-14) mm long. Additionally, the indumentum of branchlets and leaflets (lower surface) is denser in R. glazioui than it is in R. cnestidifolia. Geographic distribution may also be useful for recognition: R. cnestidifolia is apparently restricted to central and northeast portions of Minas Gerais, while R. glazioui is very common in the coastal zone between southern Bahia and central Rio de Janeiro (Fig. 6).  selected the lectotype of R. cnestidifolia, as the type from B is considered missing. The specimen indicated by  from K has no collection date, although the author cited "18 Nov 1864", probably because he considered it the same collection of specimen Warming 1849/3 from C (barcode C 10009584) and Warming 1849/1 from GH (barcode GH 00043365). However, there are, in C, many specimens Warming 1849, in which collection number is subdivided from 1 to 5 and present different collection dates. All specimens of Warming 1849 from C, GH and K seem to correspond to the same gathering, but as they do not match in collection dates and subdivision of main collection number, the lectotype from K is here considered a unicate. Diagnosis. Akin to R. martiana due to the presence of glandular trichomes, relatively small leaves and leaflets and flowers and fruits with similar characteristics, but differs by the leaves 5-9(-13)-foliolate (vs. 9-15-foliolate), leaflet apices narrowly rounded or obtuse (vs. rounded) and pedicels 5-13 mm long (vs. ca. 2 mm long).
Distribution, habitat and phenology. Rourea diamantina is only known from the east side of Chapada Diamantina, a mountain range of about 41,700 km 2 and approximately 2,000 m altitude, located in the centre of Bahia (Fig. 8). Individuals of the new species are mostly shrubs with scandent branches, occurring in seasonal forests of Inselbergs. Specimens have been collected with flowers from September to December and with fruits from November to February and in July.   Etymology. The specific epithet "diamantina" refers to Chapada Diamantina (Bahia, Brazil), where the new species is presumed to be endemic. This epithet is a noun in apposition (Turland et al. 2018, Art. 23.5).
Recognition and notes. Rourea diamantina is recognised by the leaves 5-9(-13)-foliolate, leaflets abaxially hirsute or villous, pedicel with glandular trichomes and sepals with indumentum sericeous internally. An interesting characteristic is the leaves whose leaflets become significantly larger towards the apex. The new species is similar to R. martiana, but differs by the reduced number of leaflets (usually 5-9), which are normally narrowly ovate with obtuse or narrowly-rounded apex, and longer pedicel (5-13 mm long) vs. leaves 9-15-foliolate, leaflets normally oblong or narrowly elliptic with rounded apex and a shorter pedicel (ca. 2 mm long). Additionally, both species are geographically isolated by the Chapada Diamantina (Fig. 8).

Rourea discolor
Distribution, habitat and phenology. Rourea discolor is exclusive to Bahia, where the individuals are distributed mainly in the southern coastal zone (Fig. 9). Its limits range from the municipality of Valença (near Itacaré) to the municipality of Porto Seguro. This is a lianescent species up to 3 m tall and occurs in dense ombrophilous, "Tabuleiro" or swamp forests, sometimes reaching areas of restinga (coastal vegetation), growing on clay or sandy soils. Specimens have been collected with flowers from August to September and with fruits from October to February. Recognition and notes. Rourea discolor is recognised by the glabrous or subglabrous inflorescence rachis measuring 3.5-11.5 cm long and pedicel 6-16 mm long. It is morphologically similar to R. glazioui due to the number and shape of its leaflets; however, individuals of R. discolor do not have glandular trichomes and the inflorescence rachis is glabrous or subglabrous, while in R. glazioui, they have glandular trichomes and the inflorescence rachis is hirsute or densely so. Rourea discolor can be confused with R. bahiensis as well, although they are differentiated by the characteristics of the leaflets and inflorescences (see "Recognition and notes" section of R. bahiensis).
In the original description, Baker (1871) indicated only the specimen Luschnath s. n., without mentioning either herbarium, collector number or date. This specimen is deposited in BR and is likely to be the holotype, as no other duplicate has been found.

Rourea glazioui G. Schellenb., in Engler
Distribution, habitat and phenology. Rourea glazioui is found in Bahia, Espírito Santo and Rio de Janeiro (Fig. 6). In ES, the species has been widely collected along the central and east parts of the state, whereas in BA it is restricted to the southern region, and in RJ, it is sparsely distributed in the eastern side. The type location (Rezende, RJ) might be mistaken as no other record has been found nearby. It is a liana or scandent shrub up to 1.5 m tall, mainly occurring in areas of ombrophilous or "Tabuleiro" forests, although sometimes found in swamp forests or disturbed environments, such as small fragments or in Eucalyptus plantations, growing on clay or sandy soils. Specimens have been collected with flowers and fruits almost throughout the year, although more frequently during the spring season. Recognition and notes. Rourea glazioui resembles R. cnestidifolia as they have glandular trichomes and similar characteristics of leaflet shape and size, flowers and fruits. However, the former has leaves (9-)15-27-foliolate, peduncle 0.2-1.5 cm long, flowers loosely disposed on the inflorescences and pedicel 5-10(-14) mm long, while the latter has leaves 9-13-foliolate, peduncle 2.8-8 cm long, flowers congested in the inflorescence apex and pedicel 3-5 mm long. Rourea glazioui is commonly confused with R. chrysomalla in herbarium specimens, but differs in the characteristics described in the "Recognition and notes" section of R. chrysomalla.
In the protologue, Rourea glazioui was named as R. polyphylla (Schellenberg 1938). After noticing that he created a homonym of R. polyphylla Blume (1849), Schellenberg (1938) added an appendix in the same work and replaced R. polyphylla for R. glazioui. This does not preclude valid publication of R. glazioui, as this replaced name, although indicated in the same work, presented a clear and crossed reference of a corresponding description (Turland et al. 2018, Art. 41.3).

Rourea martiana
Distribution, habitat and phenology. This species occurs in central and northeast Minas Gerais and southwest Bahia (Fig. 8). Rourea martiana is a shrub, occasionally with climbing branches and grows in the Cerrado or in transitional areas with Caatinga or Atlantic Forest. Specimens have been collected with flowers in April and August and with fruits in October. Recognition and notes. Rourea martiana is recognised by possessing glandular trichomes, a relatively long-peduncle (0.9-3.8 cm) and a short pedicel (ca 2 mm long). Baker (1871) described Rourea martiana based on the collections of Martius 1675 and Warming 1849, without mentioning the type; the former is only deposited in M, while the latter is deposited in C, GH and K. Schellenberg (1938) inadvertently indicated the lectotype of R. martiana (Martius 1675) and described R. cnestidifolia, citing Warming 1849 as paratype. Forero (1976) followed Schellenberg's position, although he called the specimen Martius 1675 holotype of R. martiana, and selected Warming 1849 from K as lectotype of R. cnestidifolia after the holotype from B (Sellow s. n.) was considered missing. Baker (1871) indeed described R. martiana based on two specimens that should be treated as different taxa, so Schellenberg (1938) was right in selecting a type for R. martiana and describing R. cnestidifolia. The former differs by the middle and apical leaflets up to 4 cm long with usually rounded apex, while in the latter, leaflets are longer than 4 cm with obtuse, acute or narrowly rounded apex.
After fixing the application of R. martiana to Martius 1675, however, both Schellenberg (1938) and Forero ( , 1983 seem to have confused the identity of the species and grouped specimens morphologically distinct and geographically isolated. The type of R. martiana was collected in Minas Gerais and, although without a precise location, this specimen matches those collected in central and northeast of the state and south-western Bahia, which are characterised by leaves 9-15-foliolate and a short pedicel (ca. 2 mm long). The specimens, here treated under a new species (R. diamantina) -but identified as R. martiana by Schellenberg (1938) and Forero ( , 1983 -are restricted to central Bahia and characterised by leaves 5-9(-13)-foliolate and a longer pedicel (5-13 mm long). Additionally, leaflets in R. martiana become slightly larger towards the apex and are usually oblong or narrowly elliptic with rounded apex (Fig. 1B), whereas in R. diamantina, they become significantly larger towards the apex and are usually narrowly ovate with obtuse or narrowly-rounded apex (Fig. 7B). Both species are morphologically similar due to the presence of glandular trichomes, leaves and leaflets relatively small and flowers and fruits with similar characteristics. Geographically, these two species are separated by the Chapada Diamantina (Fig. 8), a mountain range located in central Bahia approximately 41,700 km 2 long and altitudes up to 2,000 m. They also occur in different environments: R. martiana grows in areas of Cerrado s. s. (occasionally with rocky soils), while R. diamantina grows in seasonal forests on Inselbergs.
The position taken by Schellenberg (1938) and Forero ( , 1983) may be explained because the specimens from Minas Gerais were not available at the time. Nevertheless, the disjunct distribution and the morphological differences are consistent enough to recognise R. martiana and R. diamantina as distinct species.