Taxonomic revision of neotropical Connarus (Connaraceae) identifies three undescribed species

Abstract: An ongoing taxonomic revision of neotropical Connarus has identified three undescribed species of the genus, which are published here. One of them, C. foreroi, is known only from a single gathering from central Peru, probably reflecting scarcity of botanical inventories. Connarus revolutus, on the other hand, seems to be more common, but it is restricted to northeastern Espírito Santo and southern Bahia, Brazil. Connarus pedicellatus, originally described as a variety of C. erianthus, is elevated to the rank of species; it is distributed widely in the Amazon forest of Brazil, extending to southern Suriname. The present study describes and illustrates these three new species and provides a geographic distribution map, comparisons, information on habitat, phenology and preliminary conservation risk assessments, along with a key to distinguish them from similar taxa. Citation: Toledo C. A. P., Souza V. C. & Lucas E. J. 2021: Taxonomic revision of neotropical Connarus (Connaraceae) identifies three undescribed species. – Willdenowia 51: 171–180. Version of record first published online on 9 June 2021 ahead of inclusion in August 2021 issue.


Introduction
With more than 75 species, Connarus L. is the largest genus in Connaraceae (Lemmens & al. 2004). It is a pantropical group, represented especially by lianas, scandent shrubs or small trees, mainly from lowland tropical wet forests or savannas of South America, central Africa and southeastern Asia (Leenhouts 1958;Forero 1983;Lemmens 1989a). Its species richness is centred in the neotropics, where c. 55 species are found, mostly dispersed in the Amazon and Atlantic forests, to which several taxa are restricted (Forero 1983).
Connarus is morphologically characterized by the lenticellate branchlets, alternate, compound and imparipinnate leaves without stipules, inflorescences usually in thyrses (or variations thereof), heterostylous, pentamerous and actinomorphic flowers, androecium with two whorls of ten stamens alternating in length, gynoecium with a single carpel, and follicular fruits with black seeds bearing colourful arils (description largely based on Forero 1983;Lemmens 1989a;Lemmens & al. 2004). While the most inclusive phylogenetic study of Connaraceae -based exclusively on morphological data -recognized Connarus as sister to the clade formed by the African genera Burttia Baker f. & Exell, Ellipanthus Hook. f., Hemandradenia Stapf and Vismianthus Mildbr. (Lemmens 1989b), a recent preliminary genomic approach to the Plant and Fungal Tree of Life (https://treeoflife.kew.org/tree-of-life) came up with different conclusions, in which Connarus forms a monophyletic group with Ellipanthus, Jollydora Pierre ex Gilg and Vismianthus, although Burttia and Heman dradenia were not included. Connarus differs from other Connaraceae by the imparipinnate leaves, punctate perianth, a single carpel, relatively broader follicular fruits 172 Toledo & al.: Revision of neotropical Connarus identifies three undescribed species and seeds without endosperm (Forero 1983;Lemmens & al. 2004;Toledo & al. 2020). Forero's (1983) contribution to the taxonomic knowledge of neotropical Connarus was enormous and several new species were described at the time. After his revisionary work, more than 35 years ago, several other taxonomic novelties in neotropical Connarus have been identified, reflecting relative neglect of modern systematic studies for this genus.
While developing a taxonomic revision of Connarus in the neotropics, three new species of this genus were discovered (including a new specific status for a previously published variety). These species are described and illustrated here. The present study also includes a geographic distribution map, information on habitat, phenology and conservation status, taxonomic discussions and an identification key to separate the new species from similar taxa.

Material and methods
The new species presented in this study were described based on examination of specimens deposited in the following herbaria (herbarium codes according to Thiers 2020+): COL, CVRD, ESA, IAN, INPA, K, MA, MG, NY, P, RB, U, UB , UFACPZ and US. General morphological terms applied in the descriptions are based on Font Quer (1953), while venation patterns follow Ellis & al. (2009) and inflorescence architecture follows Weberling (1992).
The geographic distribution map was prepared using ArcGIS 10.5 (ESRI 2016), based on the localities indicated on herbarium sheet labels. Preliminary conservation risk assessments were inferred according to IUCN (2012IUCN ( , 2017 guidelines and criteria, with Extent of Occurrence (EOO) calculated in GeoCAT (Bachman & al. 2011).
The identification key following and accessory to the treatments of the three new species was built with the intention of facilitating the prompt recognition of the new species when compared to morphologically similar taxa.
Distribution, habitat and phenology -The only known specimen of Connarus foreroi was collected in the department of Huánuco, central Peru ( Fig. 1). This individual was reported as a shrub c. 1.5 m tall, growing along river margins in a dense, wet forest, at 300 -400 m elevation. This fruiting specimen was collected in November.
Etymology -The specific epithet was chosen in order to honour Dr. Enrique Forero, given his consistent contribution to the taxonomy of neotropical Connaraceae.
Conservation status -As Connarus foreroi is here described based on a single gathering, and considering that it was acquired in a poorly collected area, this species is here assigned the category Data Deficient (DD) according to the IUCN (2012, 2017).
Remarks -Even though this new species is known from a single gathering, it is distinguished from other neotropical Connarus by the 5-foliolate leaves, large, obovate leaflets, cauliflorous inflorescences with rachises bearing only simple trichomes, and fruits glabrous or subglabrous on the inner surface. This combination of characters is unique among the neotropical species of the genus. Con narus fasciculatus also has cauliflorous inflorescences, but with rachises covered by dendroid trichomes, which are not seen in C. foreroi. Willdenowia 51 -2021 Connarus pedicellatus (Forero)  Description -Shrubs, treelets or trees, 2 -14(-18) m tall; branchlets tomentose to glabrescent, indumentum with dendroid and simple trichomes, lenticels absent or inconspicuous. Leaves 7 -11-foliolate; petiole 2.5 -9 cm long, glabrous; rachis 6.5 -17.2(-28) cm long, glabrous; pulvinuli 3 -7 mm long, glabrous or subglabrous; leaflets opposite to alternate, concolorous or slightly discolorous, flat, chartaceous; basal pair symmetric to asymmetric, ovate or elliptic, less frequently narrowly ovate, 3.8 -10.3 × 2 -4.5 cm, base asymmetric or slightly so, rounded or obtuse; other leaflets symmetric to asymmetric, ovate, narrowly ovate, elliptic or narrowly elliptic (apical leaflet usually elliptic), 5 -16.4 × 2.5 -5.7 cm, base asymmetric or slightly so, rounded, obtuse or acute, apex long acuminate to cuspidate, acumen 5 -23 mm long; all leaflets: both surfaces glabrous or subglabrous, adaxial surface dull, margin flat; secondary veins 5 -7 pairs, forming angle of 45 -65° with midvein, arcuate or slightly so, abaxially slightly prominent, adaxially flat, rarely slightly impressed; tertiary veins percurrent, abaxially flat or slightly prominent, adaxially flat, rarely slightly prominent. Inflorescences axillary, 1 -6 per axil, rarely ramiflorous, in simple, determinate thyrses; peduncle 0.   Distribution, habitat and phenology -Connarus pedi cellatus is exclusively found in the Amazon forest, where it is widely distributed, especially in the Brazilian states of Acre, Amapá, Amazonas and Pará, with few collections known from Mato Grosso (Brazil) and southern Suriname (Fig. 1). Individuals of this species are shrubs or trees usually up to 14 m tall, occurring in upland forests, flooded areas (igapó) or along watercourses (igarapé) of the Amazon, at elevations ranging from 50 -500 m. It has been collected with flowers from April to August and with fruits from June to December.
Etymology -The specific epithet refers to the pedicellate flowers of this taxon. This is a diagnostic feature distinguishing Connarus pedicellatus from C. erianthus Benth. ex Baker, which has sessile flowers.
Conservation status -Connarus pedicellatus is widely distributed in the Brazilian Amazon, and the Extent of Occurrence (EOO) of the species is estimated at more than 1,800,000 km 2 . In addition, despite significant degradation of this phytogeographic domain in the past years, it is still the largest tropical forest worldwide, and several populations of C. pedicellatus exist in protected areas. Given both the EOO and what is currently known of its distribution, C. pedicellatus is here assigned the category Least Concern (LC) according to the IUCN (2012IUCN ( , 2017. Remarks -Among the neotropical species of Connarus with dendroid trichomes on branchlets and inflorescences, C. pedicellatus is distinguished by the shrubby or arboreal habit, leaves 7 -11-foliolate, leaflet base asymmetric, inflorescences in thyrses, and fruits lanate to glabrescent on the outer surface, with stipe 2 -4 mm long. Connarus pedicel latus is similar to C. erianthus and was previously treated as a variety of that species, but it differs by the chartaceous leaflets with flat margins (vs. usually coriaceous leaflets with revolute margins in C. erianthus), branched inflorescences with dendroid and simple, unicellular trichomes (vs. unbranched inflorescences with dendroid and simple, unicellular and multicellular trichomes), pedicellate flowers (vs. sessile flowers) and fruits with stipe 2 -4 mm long (vs. fruits sessile). These characteristics are strongly consistent to recognize two separate species. Besides Connarus erianthus var. pedicellatus, Forero (1980) also described C. erianthus var. stipitatus, distinguished from the other two varieties by the sessile or shortly pedicellate flowers and stipitate fruits (Forero 1983). However, after conducting a careful revision of neotropical Connarus, it became clear that Forero's (1980Forero's ( , 1983 concept of C. erianthus var. stipitatus also included flowers with pedicels of variable length, which was difficult to measure because the specimens analysed by the author under C. erianthus var. stipitatus included only fruiting material, so it may have led to the conclusion that the pedicels of C. erianthus var. pedicellatus are significantly longer than in C. erianthus var. stipitatus, which is not the case. Considering that both C. erianthus var. pedi cellatus and C. erianthus var. stipitatus have inflorescences in thyrses, pedicellate flowers and stipitate fruits, then only one taxon should be recognized. The former name is here chosen over the latter because the diagnostic character (pedicellate flowers) can be visualized both in flowering or fruiting specimens. Therefore, C. erianthus var. stipitatus is here treated as a synonym of C. pedicellatus.
Diagnosis -Morphologically similar to Connarus co riaceus G. Schellenb. in the sepals being hairy on the inner surface and the long-stipitate fruits, but differing by the strongly revolute leaflet margins (vs. flat or slightly revolute in C. coriaceus), ferruginous inflorescence rachis (vs. aureous) and petals being pubescent on the outer surface (vs. glabrous or subglabrous).
Distribution, habitat and phenology -Connarus revo lutus is found only in northeastern Espírito Santo and southern Bahia, in the limits between the northeastern and southeastern regions of Brazil (Fig. 1). This lianescent species occurs close to coastal areas of the Atlantic Forest, growing in semideciduous forests on sandy soils (tabuleiro) or in coastal vegetation (restinga), at low elevations. Flowering specimens have been collected in September and fruiting specimens in October.
Etymology -The specific epithet refers to the strongly revolute leaflet margins, which are very distinctive in this species, observed in all analysed specimens.
Conservation status -Connarus revolutus is currently known to be restricted to a very few sites along the limits of the states of Bahia and Espírito Santo, Brazil. As a result, an EOO of approximately 900 km 2 was estimated for this species. Although some of the areas where the new species was collected are protected by law, some others belong to private properties or fragments along sideroads, which have been severely fragmented in the region, especially due to monoculture of eucalyptus (one of the largest in Brazil). Therefore, considering the restricted distribution and the reduced number of individuals as well, it is suggested here that C. revolutus be assigned the category Endangered (EN), based on the criteria B1ab(iii,iv), according to the IUCN (2012IUCN ( , 2017.
Remarks -Connarus revolutus is morphologically recognized by having leaves always 3-foliolate, leaflets coriaceous with strongly revolute margin, secondary veins strongly prominent, tertiary veins percurrent, sepals pubescent on the inner surface, petals pubescent on the outer surface, and fruit stipe 4 -8 mm long. Among the neotropical species, it can be confused with C. coriaceus due to having sepals hairy on the inner surface and longstipitate fruits, but C. revolutus is restricted to the Atlantic Forest, characterized by strongly revolute leaflet margins, inflorescence rachis with ferruginous indumentum and petals pubescent on the outer surface, whereas C. co riaceus is widely distributed in Amazonia, characterized